More stories

  • in

    Assessing data bias in visual surveys from a cetacean monitoring programme

    Data processingIn 2019, the CETUS data spanning between 2012 and 2017 was published open access through the Flanders Marine Institute (VLIZ) IPT portal and distributed by EMODnet and OBIS, in a first version of the CETUS dataset9. The data collected between 2018 and 2019 was prepared as the 2012–2017 data9. Methods for photographic verification/validation and to evaluate the MMOs experience were applied (see below), in order to include new variables on data quality in an updated version of the dataset. Currently, the CETUS dataset is updated, with a 2nd version available10. It comprises data from 2012 to 2017, with the following two new columns on the observers’ experience: “most experienced observer” and “least experienced observer”; and a new column associated with validation of the sightings’ identifications: “photographic validation”. The results here presented correspond to the analysis of the data from 2012 to 2019, and the open-access dataset will soon be further updated with the 2018–2019 data.Photographic verificationAll the former MMOs who have integrated the CETUS Project, between 2012 and 2019, were contacted and asked to provide any available photographic or video records of cetaceans collected during their on board periods. The collection of sighting’s images was not a requirement of the CETUS protocol, and so these records were obtained opportunistically, with availability and quality depending on several factors: observers on board having personal cameras, camera quality, intention of the observer taking the photograph (e.g., for aesthetic or identification purposes).The images obtained were organized in a folder hierarchy from the year to the day of recording. However, not all the images had metadata up to the day of recording, so these were inserted into the most appropriate hierarchy-level of the folder organization. For each set of records corresponding to a single-taxon sighting, the photos/videos with the better quality or framing (i.e., that allowed for an easier species identification) were selected for that sighting. The remaining photos/videos were only consulted in case of doubt (e.g., to look for additional details that could help with the identification).Verification consisted of the process of matching the photographic/video records with the dataset sighting registers. Whenever possible and ideally, the file metadata was used for the process. However, often, the date and/or time of the file metadata were wrong, non-existent, or in different time zones. In these cases, a conservative methodology was applied using all available information to match as many sightings as possible. An estimation of time lag was attempted (based on, at least, two obvious matches between photographs/videos and dataset registers, e.g., unique sighting of the day, close to the boat, easy/obvious identification). When not possible, further evaluation consisted in assessing whether the sighting and image record was too obvious, and accounting for unique complementary information on the sighting (e.g., the number of animals or the side of the sighting were unique for that day and/or for that species/group).Photographic validationAfter the verification process, the validation of the matched records was carried out, to confirm or correct the species identification of sightings in the 1st version of the CETUS dataset (i.e., reported by the MMOs on board). The validation approach involved, for more dubious identification through the photo/video records, the discussion between four experienced observers of the CETUS team. In cases where no consensual agreement was achieved, an external expert on cetacean identification was also consulted. Identifications made through the photographic/video records required 100% certainty, and these were then compared with the cetacean identifications provided in the 1st version of the CETUS dataset. Then, the occurrence records with originally misidentifications of cetaceans, as well as those records where validation allowed to achieve an identification to a lower taxon, were corrected in the 2nd version of the dataset (i.e., a delphinid sighting validated as common dolphin, will now appear as common dolphin). A new column “photographic validation” was added to the dataset with the following categories: “yes” (i.e., validated with photograph/video), “no” (i.e., not validated with photograph/video), and “to the family” (i.e., validation only to the family taxon).For further analysis, specifically for the model process on the identification success (see below), registers were considered “completely validated” if it was possible to complete the photographic/video identification process up to the species level (then, differentiating if the original identification from the MMOs was or not correct). For Globicephala sp. and Kogia sp., validation to the genus was considered complete, since the species from both genera are visually hardly differentiated, especially at sea.Creating a data quality criteria: evaluating MMOs experienceQuality criteria were created to evaluate the MMOs experience based on the information collected from their curricula vitae (CVs) (alumni MMOs provided as many CVs as the years of their participation in CETUS). The following quality criteria were considered: (i) the experience at sea, (ii) the experience with cetaceans’ ID, (iii) the number of species they have worked with, and (iv) the experience working with the CETUS Project protocol. Each of these quality criteria was ranked from 0 to 5, and then these were summed to generate an evaluation score, on a scale of 0 to 20, attributed to each MMO (Table 4).Table 4 Quality criteria for MMOs evaluation.Full size tableThe MMOs evaluations were computed for each cruise (i.e., the trip from one port to another), considering the experience of the MMOs based on the CV obtained for that year, plus the experience acquired during CETUS participation in previous cruises that year. Since most of the times, the team of observers on board each cruise was constituted by two MMOs, two final evaluation scores were attributed to each cruise in the 2nd version of the CETUS dataset, into two new columns: “most experienced observer” and “least experienced observer”. On rare occasions where there is only one observer on board that cruise, only the evaluation of the single observer was included under the column “most experienced observer”, leaving the column “least experienced observer” as “NULL”. To investigate the experience of MMOs on board, both individually and cumulative (LEO + MEO), the combination of the score values was computed by cruise. These were then trimmed to unique combinations of evaluation scores.The names of observers, previously presented in the online dataset for each cruise, were removed for anonymity purposes, as there is now ancillary information regarding their experience.Model fittingTwo Generalized Additive Models (GAM) were fitted to assess bias on the number of sightings recorded per survey and on the identification success of cetacean species. Details for each model are presented below. Both models were fitted in R (Version 4.1.0). Prior to modelling, Pearson correlations were calculated between all pairs of explanatory variables, considered for each model (see below), to exclude highly correlated variables, considering a threshold of 0.7524,25,28. Since the variables regarding MMOs’ experience were correlated (LEO or MEO correlated with cumulative and mean experience; and cumulative experience correlated with mean experience – Supplementary Fig. S3), these variables were not included in the first fitting stage (backward selection) but included later through forward selection (see below). Multicollinearity among explanatory variables was measured through the Variance Inflation Factor (VIF), with a threshold of 3 (Supplementary Tables S4)24,25,29. After removing the MMOs evaluation scores, no multicollinearity was observed, so all the other variables were kept for the first fitting stage.For model selection, a backward selection was applied to oversaturated models18,24,25,30,31. The Akaike Information Criterion (AIC) was used as a measure of adequation of fitness, choosing the model with the lowest AIC value at each step of the model fitting process, i.e., comparing nested models (larger model incorporating one more explanatory variable compared with the smaller model). If the AIC-difference between the two models was less than 2, an Analysis of Variance (ANOVA), through chi-square test, was used to check if the AIC-difference was significant24,25,32. If this difference was not statistically significant (p  > 0.05), the simplest model (smaller model) was kept. Through a forward selection process, the variables regarding the MMOs evaluation scores were added, one at a time, to the best model obtained in the previous backward selection. After comparing the models with each other (separate variables for LEO + MEO vs. Cumulative Evaluation vs Mean Evaluation), the best model, considering the AIC value, was kept. A final backward selection process was then applied.All GAMs were fitted with the “mgcv” package (https://cran.r-project.org/web/packages/mgcv) and a maximum of four splines (k = 4) was chosen to limit the complexity of smoothers describing the effects of the explanatory variables25,31. If a spline was close to linear (with estimated degrees of freedom of ~1), the smooth term was removed, and a linear function was fitted. To check for model quality, the “gam.check” function was used to verify the diagnostic plots and the adequacy of the number of splines (Supplementary Figs. S5 and S6). Existence of influential data points was assessed (with the threshold of 0.25 for the Hat values), as well as the correlation between model residuals and explanatory variables. In both final models, number of splines was adequate and there were no influential data points or clear correlation between residuals and explanatory variables (Supplementary Figs. S7 and S8)24,32.Bias modelling of number of sightingsTo assess the bias parameters on the number of sightings recorded per survey (i.e., a full day monitoring, from sunrise to sunset), the following detectability factors were considered as explanatory variables: weather conditions (i.e., the minimums and maximums of the sea state, wind state, and visibility), the experience of MMOs (i.e., the evaluation scores of the least and the most experienced observers, as well as the mean and cumulative evaluations of the MMOs experience) and kilometres sampled “on-effort” (i.e., periods of active survey). Sampling periods were divided into “On-effort” and “Off-effort” conditions, based on four meteorological variables: sea state (Douglas scale), wind state (Beaufort scale), visibility (measured in a categorical scale ranging from 0–10 and estimated from the distance to the horizon line and possible reference points at a known range, e.g., ships with an automatic identification system,  > 1000 km), and the occurrence of rain (see Supplementary Table S9)10. For the model fitting, only “on-effort” periods of sampling were considered. Given that the response variable was count data, a Poisson distribution was tested (with a log link function). Then, the resulting first oversaturated model was checked for overdispersion, through a Pearson estimator. Since it tested positive for overdispersion (φ = 1.99), a negative binomial distribution (with a log link function) was fitted.Bias modelling of identification successA binary response variable, based on the success in the species identification for each sighting, was generated, and a model with binomial distribution (with a logit link function) was fitted. As in the previous model, only “on-effort” records were used. The total number of non-successful identifications across the dataset (the 0 s of the model) was extrapolated from the proportion of wrong identifications obtained in the validation process. To calculate this proportion, only complete validated sightings registered “on-effort” were used. Proportions were computed and extrapolated to Odontoceti and Mysticeti, separately. This resulted in 78 non-successful identifications in delphinids, plus 17 misidentifications in baleen whales, i.e., a total of 95 “on-effort” sightings randomly selected from the dataset were defined as unsuccessful identifications (0 s in the response variable for model fitting). The remaining records were considered successful identifications (1 s in the response variable for model fitting). To assess the bias parameters on the identification success, the following independent variables were considered in the analysis: the group (i.e., Group A: Odontoceti sightings, excluding sperm whale (Physeter macrocephalus); and Group B: Mysticeti sightings, plus sperm whale), the size of the group (i.e., the best estimate of the number of animals in a sighting, from the observer’s perspective), sighting distance (i.e., a relative measure according to the scale of the binoculars), weather conditions (i.e., the sea state, wind state, and visibility at the time of each sighting), the experience of MMOs (i.e., the evaluation scores of least and most experienced observers, as well as the mean and cumulative scores of the MMOs teams). Group A and B were settled according to cetacean morphology. However, since sperm whales have closer similarities with Mysticeti species, they were also included in Group B21,33. This categorization was mostly based on body size, as this is likely the main factor, regarding the species morphology, influencing the identification. Group A is constituted by species with a medium length of less than 10 meters, while Group B includes the larger species over 10 meters (Mysticeti plus P. macrocephalus)33. Since in the CETUS Project, different binoculars have been used – with two different reticle scales – it was necessary to standardize binocular distances to the same scale. More

  • in

    Stacked distribution models predict climate-driven loss of variation in leaf phenology at continental scales

    Wright, S. Evolution in Mendelian Populations. Genetics 16, 97–159 (1931).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    DiBattista, J. D. Patterns of genetic variation in anthropogenically impacted populations. Conserv. Genet. 9, 141–156 (2008).
    Google Scholar 
    Ellegren, H. & Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433 (2016).CAS 
    PubMed 

    Google Scholar 
    Nei, M., Maruyama, T. & Chakraborty, R. The Bottleneck Effect and Genetic Variability in Populations. Evolution 29, 1–10 (1975).PubMed 

    Google Scholar 
    Frankham, R. Stress and adaptation in conservation genetics. J. Evol. Biol. 18, 750–755 (2005).CAS 
    PubMed 

    Google Scholar 
    Mimura, M. et al. Understanding and monitoring the consequences of human impacts on intraspecific variation. Evol. Appl. 10, 121–139 (2017).PubMed 

    Google Scholar 
    Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7, 510–523 (2006).CAS 
    PubMed 

    Google Scholar 
    Hughes, A., Inouye, B., Johnson, M., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008).PubMed 

    Google Scholar 
    Hughes, A. R., Stachowicz, J. J. & Williams, S. L. Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159, 725–733 (2009).PubMed 

    Google Scholar 
    Schweitzer, J. A. et al. Genetically based trait in a dominant tree affects ecosystem processes: Plant genetics impact ecosystems. Ecol. Lett. 7, 127–134 (2004).
    Google Scholar 
    Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl Acad. Sci. USA 101, 8998–9002 (2004).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wimp, G. M. et al. Conserving plant genetic diversity for dependent animal communities. Ecol. Lett. 7, 776–780 (2004).
    Google Scholar 
    Reusch, T. B. H., Ehlers, A., Hämmerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. 102, 2826–2831 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).CAS 
    PubMed 

    Google Scholar 
    Salo, T. & Gustafsson, C. The Effect of Genetic Diversity on Ecosystem Functioning in Vegetated Coastal Ecosystems. Ecosystems 19, 1429–1444 (2016).
    Google Scholar 
    Zettlemoyer, M. A. & Peterson, M. L. Does Phenological Plasticity Help or Hinder Range Shifts Under Climate Change? Front. Ecol. Evol. 9, 392 (2021).
    Google Scholar 
    Fei, S. et al. Divergence of species responses to climate change. Sci. Adv. 3, e1603055 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Yiming, L. et al. Latitudinal gradients in genetic diversity and natural selection at a highly adaptive gene in terrestrial mammals. Ecography 44, 206–218 (2021).
    Google Scholar 
    Excoffier, L., Foll, M. & Petit, R. J. Genetic Consequences of Range Expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501 (2009).
    Google Scholar 
    Alsos, I. G. et al. Genetic consequences of climate change for northern plants. Proc. R. Soc. B Biol. Sci. 279, 2042–2051 (2012).
    Google Scholar 
    Stahl, U., Reu, B. & Wirth, C. Predicting species’ range limits from functional traits for the tree flora of North America. Proc. Natl Acad. Sci. 111, 13739–13744 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Van Nuland, M. E. et al. Intraspecific trait variation across elevation predicts a widespread tree species’ climate niche and range limits. Ecol. Evol. 10, 3856–3867 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Peterson, M. L., Angert, A. L. & Kay, K. M. Experimental migration upward in elevation is associated with strong selection on life history traits. Ecol. Evol. 10, 612–625 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Vitasse, Y., Signarbieux, C. & Fu, Y. H. Global warming leads to more uniform spring phenology across elevations. Proc. Natl Acad. Sci. 115, 1004–1008 (2018).CAS 
    PubMed 

    Google Scholar 
    Piao, S. et al. Plant phenology and global climate change: Current progresses and challenges. Glob. Change Biol. 25, 1922–1940 (2019).
    Google Scholar 
    Chen, I.-C., Hill, J., Ohlemüller, R., Roy, D. B. & Thomas, C. Rapid Range Shifts of Species Associated with High Levels of Climate Warming. Science 333, 1024–6 (2011).CAS 
    PubMed 

    Google Scholar 
    Pauls, S. U., Nowak, C., Bálint, M. & Pfenninger, M. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22, 925–946 (2013).PubMed 

    Google Scholar 
    De Kort, H. et al. Life history, climate and biogeography interactively affect worldwide genetic diversity of plant and animal populations. Nat. Commun. 12, 516 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Hampe, A. & Petit, R. J. Conserving biodiversity under climate change: the rear edge matters. Ecol. Lett. 8, 461–467 (2005).PubMed 

    Google Scholar 
    DeMarche, M. L., Doak, D. F. & Morris, W. F. Incorporating local adaptation into forecasts of species’ distribution and abundance under climate change. Glob. Change Biol. 25, 775–793 (2019).
    Google Scholar 
    Bothwell, H. M. et al. Genetic data improves niche model discrimination and alters the direction and magnitude of climate change forecasts. Ecol. Appl. 31, e02254 (2021).Syfert, M. M., Brummitt, N. A., Coomes, D. A., Bystriakova, N. & Smith, M. J. Inferring diversity patterns along an elevation gradient from stacked SDMs: A case study on Mesoamerican ferns. Glob. Ecol. Conserv. 16, e00433 (2018).
    Google Scholar 
    Mateo, R. G., Felicísimo, Á. M., Pottier, J., Guisan, A. & Muñoz, J. Do Stacked Species Distribution Models Reflect Altitudinal Diversity Patterns? PLOS ONE 7, e32586 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ferrier, S. & Guisan, A. Spatial modelling of biodiversity at the community level. J. Appl. Ecol. 43, 393–404 (2006).
    Google Scholar 
    Ware, I. M. et al. Climate-driven reduction of genetic variation in plant phenology alters soil communities and nutrient pools. Glob. Change Biol. 25, 1514–1528 (2019).
    Google Scholar 
    Endler, J. A. Geographic variation, speciation, and clines (Princeton University Press, 1977).May, R. M. & Godfrey, J. Biological Diversity: Differences between Land and Sea [and Discussion]. Philos. Trans. Biol. Sci. 343, 105–111 (1994).
    Google Scholar 
    Des Roches, S. et al. The ecological importance of intraspecific variation. Nat. Ecol. Evol. 2, 57–64 (2018).PubMed 

    Google Scholar 
    Van Nuland, M. E., Bailey, J. K. & Schweitzer, J. A. Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics. Nat. Ecol. Evol. 1, 0150 (2017).
    Google Scholar 
    Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos. Trans. R. Soc. B Biol. Sci. 365, 3227–3246 (2010).
    Google Scholar 
    Richardson, A. D. et al. Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. Tree Physiol. 29, 321–321 (2009).CAS 
    PubMed 

    Google Scholar 
    Huntington, T. G. CO2-induced suppression of transpiration cannot explain increasing runoff. Hydrol. Process. 22, 311–314 (2008).
    Google Scholar 
    Kim, J. H. et al. Warming-Induced Earlier Greenup Leads to Reduced Stream Discharge in a Temperate Mixed Forest Catchment. J. Geophys. Res. Biogeosciences 123, 1960–1975 (2018).
    Google Scholar 
    Ware, I. M. et al. Climate-driven divergence in plant-microbiome interactions generates range-wide variation in bud break phenology. Commun. Biol. 4, 748 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Mori, A. S. et al. Biodiversity–productivity relationships are key to nature-based climate solutions. Nat. Clim. Change 11, 543–550 (2021).
    Google Scholar 
    Woolbright, S. A., Whitham, T. G., Gehring, C. A., Allan, G. J. & Bailey, J. K. Climate relicts and their associated communities as natural ecology and evolution laboratories. Trends Ecol. Evol. 29, 406–416 (2014).PubMed 

    Google Scholar 
    Naiman, R. J., Décamps, H. & McClain, M. E. Riparia: ecology, conservation, and management of streamside communities (Elsevier Academic Press, 2005).Bayliss, S. L. J., Mueller, L. O., Ware, I. M., Schweitzer, J. A. & Bailey, J. K. Plant genetic variation drives geographic differences in atmosphere–plant–ecosystem feedbacks. Plant-Environ. Interact. 1, 166–180 (2020).
    Google Scholar 
    Cooke, J. E. K. & Rood, S. B. Trees of the people: the growing science of poplars in Canada and worldwide. This commentary is one of a selection of papers published in the Special Issue on Poplar Research in Canada. Can. J. Bot. 85, 1103–1110 (2007).
    Google Scholar 
    Evans, L. M., Allan, G. J., Meneses, N., Max, T. L. & Whitham, T. G. Herbivore host- associated genetic differentiation depends on the scale of plant genetic variation examined. Evol. Ecol. 27, 65–81 (2013).
    Google Scholar 
    Evans, L. M. et al. Geographical barriers and climate influence demographic history in narrowleaf cottonwoods. Heredity 114, 387–396 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hargreaves, A. L., Samis, K. E., Eckert, C. G., Schmitz, A. E. O. J. & Bronstein, E. J. L. Are Species’ Range Limits Simply Niche Limits Writ Large? A Review of Transplant Experiments beyond the Range. Am. Nat. 183, 157–173 (2014).PubMed 

    Google Scholar 
    Gotelli, N. J. & Stanton-Geddes, J. Climate change, genetic markers and species distribution modelling. J. Biogeogr. 42, 1577–1585 (2015).
    Google Scholar 
    Cushman, S. A. et al. Landscape genetic connectivity in a riparian foundation tree is jointly driven by climatic gradients and river networks. Ecol. Appl. 24, 1000–1014 (2014).PubMed 

    Google Scholar 
    Bothwell, H. M. et al. Conserving threatened riparian ecosystems in the American West: Precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia). Mol. Ecol. 26, 5114–5132 (2017).PubMed 

    Google Scholar 
    Jimenez-Valverde, A. Sample Size for the evaluation of presence-absence models. Ecol. Indic. 114, 106289 (2020).
    Google Scholar 
    Hamann, A., Wang, T., Spittlehouse, D. L. & Murdock, T. Q. A Comprehensive, High-Resolution Database of Historical and Projected Climate Surfaces for Western North America. Bull. Am. Meteorol. Soc. 94, 1307–1309 (2013).
    Google Scholar 
    Lucinda. M. et al. NHDPlus version 2: user guide (Horizon Systems Corporation, 2012).ESRI. ArcMap (ESRI, 2018).Bayliss, S. L. J., Papeş, M., Schweitzer, J. A. & Bailey, J. K. Aggregate population-level models informed by genetics predict more suitable habitat than traditional species-level model across the range of a widespread riparian tree. PLoS One. 17, e0274892 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Elith, J. & Leathwick, J. R. Species Distribution Models: Ecological Explanation and Prediction Across Space and Time. Annu. Rev. Ecol. Evol. Syst. 40, 677–697 (2009).
    Google Scholar 
    Franklin, J. Mapping species distributions: spatial inference and prediction (Cambridge University Press, 2009).Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48 (2015). (1).
    Google Scholar 
    Elith, J. et al. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57 (2011).
    Google Scholar 
    Elith, J. et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129–151 (2006).
    Google Scholar 
    Pearson, R. G., Raxworthy, C. J., Nakamura, M. & Townsend Peterson, A. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34, 102–117 (2007).
    Google Scholar 
    Swets, J. A. Measuring the Accuracy of Diagnostic Systems. Science 240, 1285–1293 (1988).CAS 
    PubMed 

    Google Scholar 
    Engler, R. et al. 21st century climate change threatens mountain flora unequally across Europe. Glob. Change Biol. 17, 2330–2341 (2011).
    Google Scholar 
    Randin, C. F. et al. Climate change and plant distribution: local models predict high-elevation persistence. Glob. Change Biol. 15, 1557–1569 (2009).
    Google Scholar 
    Knutti, R., Masson, D. & Gettelman, A. Climate model genealogy: Generation CMIP5 and how we got there. Geophys. Res. Lett. 40, 1194–1199 (2013).
    Google Scholar 
    Mateo, R. G., Mokany, K. & Guisan, A. Biodiversity Models: What If Unsaturation Is the Rule? Trends Ecol. Evol. 32, 556–566 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    R. Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2020).Oksanen, J. et al. vegan: community ecology package (2020) http://CRAN.R-project.org/package=vegan. More

  • in

    Site-specific temporal variation of population dynamics in subalpine endemic plant species

    Theurillat, J.-P. & Guisan, A. Potential impact of climate change on vegetation in the European Alps: A review. Clim. Change 50, 77–109 (2001).CAS 

    Google Scholar 
    Diaz, H. F. & Eischeid, J. K. Disappearing “alpine tundra” Köppen climatic type in the western United States. Geophys. Res. Lett. 34, L18707 (2007).ADS 

    Google Scholar 
    Dirnböck, T., Essl, F. & Rabitsch, W. Disproportional risk for habitat loss of high-altitude endemic species under climate change. Glob. Change Biol. 17, 990–996 (2011).ADS 

    Google Scholar 
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauli, H., Gottfried, M., Dirnböck, T., Dullinger, S. & Grabherr, G. Assessing the long-term dynamics of endemic plants at summit habitats. In Alpine Biodiversity in Europe (eds. Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B.) 195–207 (Springer, 2003).Cogoni, D., Sulis, E., Bacchetta, G. & Fenu, G. The unpredictable fate of the single population of a threatened narrow endemic Mediterranean plant. Biodivers. Conserv. 28, 1799–1813 (2019).
    Google Scholar 
    Cursach, J., Besnard, A., Rita, J. & Fréville, H. Demographic variation and conservation of the narrow endemic plant Ranunculus weyleri. Acta Oecol. 53, 102–109 (2013).ADS 

    Google Scholar 
    Dibner, R. R., DeMarche, M. L., Louthan, A. M. & Doak, D. F. Multiple mechanisms confer stability to isolated populations of a rare endemic plant. Ecol. Monogr. 89, e01360 (2019).
    Google Scholar 
    Boyce, M. S., Haridas, C. V., Lee, C. T., NCEAS Stochastic Demography Working Group. Demography in an increasingly variable world. Trends Ecol. Evol. 21, 141–148 (2006).PubMed 

    Google Scholar 
    Buckley, Y. M. et al. Causes and consequences of variation in plant population growth rate: A synthesis of matrix population models in a phylogenetic context. Ecol. Lett. 13, 1182–1197 (2010).PubMed 

    Google Scholar 
    Abbott, R. E., Doak, D. F. & DeMarche, M. L. Portfolio effects, climate change, and the persistence of small populations: Analyses on the rare plant Saussurea weberi. Ecology 98, 1071–1081 (2017).PubMed 

    Google Scholar 
    Villellas, J., Doak, D. F., García, M. B. & Morris, W. F. Demographic compensation among populations: What is it, how does it arise and what are its implications?. Ecol. Lett. 18, 1139–1152 (2015).PubMed 

    Google Scholar 
    Doak, D. F. & Morris, W. F. Demographic compensation and tipping points in climate-induced range shifts. Nature 467, 959–962 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    García-Camacho, R., Albert, M. J. & Escudero, A. Small-scale demographic compensation in a high-mountain endemic: The low edge stands still. Plant Ecol. Divers. 5, 37–44 (2012).
    Google Scholar 
    Andrello, M. et al. Accounting for stochasticity in demographic compensation along the elevational range of an alpine plant. Ecol. Lett. 23, 870–880 (2020).PubMed 

    Google Scholar 
    Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).PubMed 

    Google Scholar 
    Ægisdóttir, H. H., Kuss, P. & Stöcklin, J. Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann. Bot. 104, 1313–1322 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Morente-López, J. et al. Geography and environment shape landscape genetics of Mediterranean alpine species Silene ciliata Poiret. (Caryophyllaceae). Front. Plant Sci. 9, 1698 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Franks, S. J., Weber, J. J. & Aitken, S. N. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7, 123–139 (2014).PubMed 

    Google Scholar 
    Jeong, H., Cho, Y.-C. & Kim, E. Differential plastic responses to temperature and nitrogen deposition in the subalpine plant species, Primula farinosa subsp. modesta. AoB Plants 13, plab061 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sulis, E., Bacchetta, G., Cogoni, D. & Fenu, G. From global to local scale: Where is the best for conservation purpose?. Biodivers. Conserv. 30, 183–200 (2021).
    Google Scholar 
    Hambler, D. & Dixon, J. Primula farinosa L. J. Ecol. 91, 694–705 (2003).
    Google Scholar 
    Arnold, E. & Richards, A. On the occurrence of unilateral incompatibility in Primula section Aleuritia Duby and the origin of Primula scotica Hook. Bot. J. Linn. Soc. 128, 359–368 (1998).
    Google Scholar 
    Tribsch, A. Areas of endemism of vascular plants in the eastern Alps in relation to Pleistocene glaciation. J. Biogeogr. 31, 747–760 (2004).
    Google Scholar 
    Chung, J.-M., Son, S.-W., Kim, S.-Y., Park, G.-W. & Kim, S.-S. Genetic diversity and geographic differentiation in the endangered Primula farinosa subsp. modesta, a subalpine endemic to Korea. Korean J. Plant. Taxon. 43, 236–243 (2013).
    Google Scholar 
    Lindborg, R. & Ehrlén, J. Evaluating the extinction risk of a perennial herb: Demographic data versus historical records. Conserv. Biol. 16, 683–690 (2002).
    Google Scholar 
    Caswell, H. Matrix Population Models, 2nd ed (Sinauer Associates Inc, 2000).Salguero-Gómez, R. & De Kroon, H. Matrix projection models meet variation in the real world. J. Ecol. 98, 250–254 (2010).
    Google Scholar 
    Jongejans, E. et al. Region versus site variation in the population dynamics of three short-lived perennials. J. Ecol. 98, 279–289 (2010).
    Google Scholar 
    Jongejans, E. & De Kroon, H. Space versus time variation in the population dynamics of three co-occurring perennial herbs. J. Ecol. 93, 681–692 (2005).
    Google Scholar 
    Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
    Google Scholar 
    Tomimatsu, H. & Ohara, M. Demographic response of plant populations to habitat fragmentation and temporal environmental variability. Oecologia 162, 903–911 (2010).ADS 
    PubMed 

    Google Scholar 
    Kudernatsch, T., Fischer, A., Bernhardt-Römermann, M. & Abs, C. Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl. Ecol. 9, 263–274 (2008).
    Google Scholar 
    Kim, E. & Donohue, K. Local adaptation and plasticity of Erysimum capitatum to altitude: Its implications for responses to climate change. J. Ecol. 101, 796–805 (2013).
    Google Scholar 
    Forbis, T. A. Seedling demography in an alpine ecosystem. Am. J. Bot. 90, 1197–1206 (2003).PubMed 

    Google Scholar 
    Yenni, G., Adler, P. B. & Ernest, S. M. Strong self-limitation promotes the persistence of rare species. Ecology 93, 456–461 (2012).PubMed 

    Google Scholar 
    Doak, D. F. Source-sink models and the problem of habitat degradation: General models and applications to the Yellowstone grizzly. Conserv. Biol. 9, 1370–1379 (1995).
    Google Scholar 
    Lesica, P. & Crone, E. E. Arctic and boreal plant species decline at their southern range limits in the Rocky Mountains. Ecol. Lett. 20, 166–174 (2017).PubMed 

    Google Scholar 
    Oldfather, M. F. & Ackerly, D. D. Microclimate and demography interact to shape stable population dynamics across the range of an alpine plant. New Phytol. 222, 193–205 (2019).PubMed 

    Google Scholar 
    Ågren, J., Fortunel, C. & Ehrlén, J. Selection on floral display in insect-pollinated Primula farinosa: Effects of vegetation height and litter accumulation. Oecologia 150, 225–232 (2006).ADS 
    PubMed 

    Google Scholar 
    Ehrlén, J., Syrjänen, K., Leimu, R., Begona Garcia, M. & Lehtilä, K. Land use and population growth of Primula veris: An experimental demographic approach. J. Appl. Ecol. 42, 317–326 (2005).
    Google Scholar 
    Ehrlén, J. & Morris, W. F. Predicting changes in the distribution and abundance of species under environmental change. Ecol. Lett. 18, 303–314 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 1–23 (2007).
    Google Scholar 
    Weiss, N. Package ‘wPerm’. https://cran.r-project.org/web/packages/wPerm/wPerm.pdf. (2015).Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32 (2021).
    Google Scholar  More

  • in

    Sugarcane cultivation practices modulate rhizosphere microbial community composition and structure

    Meghana, M. & Shastri, Y. Sustainable valorization of sugar industry waste: Status, opportunities, and challenges. Biores. Technol. 303, 122929 (2020).CAS 

    Google Scholar 
    Petrescu, D. C., Vermeir, I. & Petrescu-Mag, R. M. Consumer understanding of food quality, healthiness, and environmental impact: a cross-national perspective. IJERPH 17, 169 (2019).PubMed Central 

    Google Scholar 
    Kassam, A., Friedrich, T., Shaxson, F. & Pretty, J. The spread of conservation agriculture: justification, sustainability and uptake. Int. J. Agric. Sustain. 7, 292–320 (2009).
    Google Scholar 
    Malviya, M. K. et al. Sugarcane microbiome: role in sustainable production. In Microbiomes and Plant Health 225–242 (Elsevier, 2021). https://doi.org/10.1016/B978-0-12-819715-8.00007-0.Chapter 

    Google Scholar 
    Sandhu, H. S., Wratten, S. D. & Cullen, R. Organic agriculture and ecosystem services. Environ. Sci. Policy 13, 1–7 (2010).CAS 

    Google Scholar 
    Schipanski, M. E. et al. Balancing multiple objectives in organic feed and forage cropping systems. Agr. Ecosyst. Environ. 239, 219–227 (2017).
    Google Scholar 
    Knapp, S. & van der Heijden, M. G. A. A global meta-analysis of yield stability in organic and conservation agriculture. Nat. Commun. 9, 3632 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).PubMed 

    Google Scholar 
    Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).CAS 
    PubMed 

    Google Scholar 
    Chialva, M., Lanfranco, L. & Bonfante, P. The plant microbiota: composition, functions, and engineering. Curr. Opin. Biotechnol. 73, 135–142 (2022).CAS 
    PubMed 

    Google Scholar 
    Dastogeer, K. M. G., Tumpa, F. H., Sultana, A., Akter, M. A. & Chakraborty, A. Plant microbiome–an account of the factors that shape community composition and diversity. Curr. Plant Biol. 23, 100161 (2020).
    Google Scholar 
    Yang, B., Wang, Y. & Qian, P.-Y. Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformat. 17, 135 (2016).
    Google Scholar 
    Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47, D259–D264 (2019).CAS 
    PubMed 

    Google Scholar 
    Wright, R. J., Gibson, M. I. & Christie-Oleza, J. A. Understanding microbial community dynamics to improve optimal microbiome selection. Microbiome 7, 85 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Praeg, N. & Illmer, P. Microbial community composition in the rhizosphere of Larix decidua under different light regimes with additional focus on methane cycling microorganisms. Sci. Rep. 10, 22324 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Souza, R. S. C. et al. Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci. Rep. 6, 28774 (2016).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tayyab, M. et al. Sugarcane cultivars manipulate rhizosphere bacterial communities’ structure and composition of agriculturally important keystone taxa. 3 Biotech. 12, 32 (2022).PubMed 

    Google Scholar 
    Tayyab, M. et al. Sugarcane cultivar-dependent changes in assemblage of soil rhizosphere fungal communities in subtropical ecosystem. Environ. Sci. Pollut. Res. 29, 20795–20807 (2022).
    Google Scholar 
    Dakora, F. D., Matiru, V. N. & Kanu, A. S. Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants. Front. Plant Sci. 6, 700 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Chapelle, E., Mendes, R., Bakker, P. A. H. & Raaijmakers, J. M. Fungal invasion of the rhizosphere microbiome. ISME J. 10, 265–268 (2016).CAS 
    PubMed 

    Google Scholar 
    Teheran-Sierra, L. G. et al. Bacterial communities associated with sugarcane under different agricultural management exhibit a diversity of plant growth-promoting traits and evidence of synergistic effect. Microbiol. Res. 247, 126729 (2021).CAS 
    PubMed 

    Google Scholar 
    de Carvalho, L. A. L. et al. Farming systems influence the compositional, structural, and functional characteristics of the sugarcane-associated microbiome. Microbiol. Res. 252, 126866 (2021).PubMed 

    Google Scholar 
    Henneron, L. et al. Fourteen years of evidence for positive effects of conservation agriculture and organic farming on soil life. Agron. Sustain. Dev. 35, 169–181 (2015).
    Google Scholar 
    Hartmann, M., Frey, B., Mayer, J., Mäder, P. & Widmer, F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J. 9, 1177–1194 (2015).PubMed 

    Google Scholar 
    Tayyab, M. et al. Sugarcane monoculture drives microbial community composition, activity and abundance of agricultural-related microorganisms. Environ. Sci. Pollut. Res. 28, 48080–48096 (2021).CAS 

    Google Scholar 
    Pang, Z. et al. Soil Metagenomics reveals effects of continuous sugarcane cropping on the structure and functional pathway of rhizospheric microbial community. Front. Microbiol. 12, 627569 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Orr, C. H., Stewart, C. J., Leifert, C., Cooper, J. M. & Cummings, S. P. Effect of crop management and sample year on abundance of soil bacterial communities in organic and conventional cropping systems. J. Appl. Microbiol. 119, 208–214 (2015).CAS 
    PubMed 

    Google Scholar 
    Brasil. Lei no 10.831, de 23 de dezembro de 2003. Dispõe sobre a agricultura orgânica e dá outras providências. In Publicado no Diário Oficial da União de 24/12/2003 (2003).Europea, C. Reglamento (CE) no 834/2007 del Consejo, de 28 de junio de 2007, sobre producción y etiquetado de los productos ecológicos y por el que se deroga el Reglamento (CEE) no 2092/91. D. Of. Unión Eur. 20, 1–23 (2007).
    Google Scholar 
    Council of the European Union. 889/2008, “Commission Regulation 889/2008/EC of 5 September 2008 laying down detailed rules for the implementation of Council Regulation (EC) No 834/2007 on organic production and labelling of organic products with regard to organic production, labelling and control”. Off. J. Eur. Union (L) 250, 18–19 (2007).
    Google Scholar 
    de Andrade, J. C., Cantarella, H. & Quaggio, J. A. Análise química para avaliação da fertilidade de solos tropicais. (2001).Donagema, G. K., de Campos, D. B., Calderano, S. B., Teixeira, W. G. & Viana, J. M. Manual de métodos de análise de solo. In Embrapa Solos-Documentos (INFOTECA-E) (2011).Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. (2020). at R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020). At Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D. & Dangl, J. L. Practical innovations for high-throughput amplicon sequencing. Nat. Methods 10, 999–1002 (2013).CAS 
    PubMed 

    Google Scholar 
    Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Renaud, G., Stenzel, U., Maricic, T., Wiebe, V. & Kelso, J. deML: robust demultiplexing of Illumina sequences using a likelihood-based approach. Bioinformatics 31, 770–772 (2015).CAS 
    PubMed 

    Google Scholar 
    Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).CAS 
    PubMed 

    Google Scholar 
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    PubMed 

    Google Scholar 
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cole, J. R. et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642 (2014).CAS 
    PubMed 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lahti, L. & Shetty, S. Microbiome R package. (2012).Oksanen, J. et al. vegan: Community Ecology Package. (2019). At Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Dhariwal, A. et al. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 45, W180–W188 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Douglas, G. M. et al. PICRUSt2: an improved and extensible approach for metagenome inference. Bioinformatics https://doi.org/10.1101/672295 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parks, D. H., Tyson, G. W., Hugenholtz, P. & Beiko, R. G. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kohl, M., Wiese, S. & Warscheid, B. Cytoscape: software for visualization and analysis of biological networks. In Data Mining in Proteomics (eds Hamacher, M. et al.) 291–303 (Humana Press, Totowa, NJ, 2011). https://doi.org/10.1007/978-1-60761-987-1_18.Chapter 

    Google Scholar 
    Assenov, Y., Ramírez, F., Schelhorn, S.-E., Lengauer, T. & Albrecht, M. Computing topological parameters of biological networks. Bioinformatics 24, 282–284 (2008).CAS 
    PubMed 

    Google Scholar 
    Shen, Z. et al. Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana fusarium wilt disease suppression induced by bio-organic fertilizer application. PLoS One 9, e98420 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yun, Y. et al. The relationship between pH and bacterial communities in a single karst ecosystem and its implication for soil acidification. Front. Microbiol. 7, 1955 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Wu, Y., Zeng, J., Zhu, Q., Zhang, Z. & Lin, X. pH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution. Sci. Rep. 7, 40093 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, R. et al. Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 7, e51897 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bill, M., Chidamba, L., Gokul, J. K., Labuschagne, N. & Korsten, L. Bacterial community dynamics and functional profiling of soils from conventional and organic cropping systems. Appl. Soil. Ecol. 157, 103734 (2021).
    Google Scholar 
    Xun, W., Shao, J., Shen, Q. & Zhang, R. Rhizosphere microbiome: Functional compensatory assembly for plant fitness. Comput. Struct. Biotechnol. J. 19, 5487–5493 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Semenov, M. V., Krasnov, G. S., Semenov, V. M. & van Bruggen, A. Mineral and organic fertilizers distinctly affect fungal communities in the crop rhizosphere. JoF 8, 251 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, Z., Li, Y., Li, T., Zhao, D. & Liao, Y. Tillage practices with different soil disturbance shape the rhizosphere bacterial community throughout crop growth. Soil Tillage Res. 197, 104501 (2020).
    Google Scholar 
    Gdanetz, K. & Trail, F. The wheat microbiome under four management strategies, and potential for endophytes in disease protection. Phytobiom. J. 1, 158–168 (2017).
    Google Scholar 
    Lazcano, C. et al. The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions. Sci. Rep. 11, 3188 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Leys, N. M. E. J. et al. Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70, 1944–1955 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yin, C. et al. Role of bacterial communities in the natural suppression of rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl. Environ. Microbiol. 79, 7428–7438 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stewart, A. & Hill, R. Applications of trichoderma in plant growth promotion. In Biotechnology and Biology of Trichoderma 415–428 (Elsevier, 2014). https://doi.org/10.1016/B978-0-444-59576-8.00031-X.Chapter 

    Google Scholar 
    Banerjee, S. et al. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol. Biochem. 97, 188–198 (2016).CAS 

    Google Scholar 
    Andargie, M., Congyi, Z., Yun, Y. & Li, J. Identification and evaluation of potential bio-control fungal endophytes against Ustilagonoidea virens on rice plants. World J. Microbiol. Biotechnol. 33, 120 (2017).PubMed 

    Google Scholar 
    Orrù, L. et al. How tillage and crop rotation change the distribution pattern of fungi. Front. Microbiol. 12, 634325 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    van der Heijden, M. G. A. & Hartmann, M. Networking in the plant microbiome. PLoS Biol. 14, e1002378 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Wang, W. et al. Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River. Sci. Rep. 6, 35046 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Silva, T. M. et al. Degradation of 2,4-D herbicide by microorganisms isolated from Brazilian contaminated soil. Braz. J. Microbiol. 38, 522–525 (2007).
    Google Scholar 
    Laura, M., Snchez-Salinas, E., Gonzlez, E. D. & Luisa, M. Pesticide biodegradation: mechanisms, genetics and strategies to enhance the process. In Biodegradation – Life of Science (ed. Chamy, R.) (InTech, 2013). https://doi.org/10.5772/56098.Chapter 

    Google Scholar 
    Upadhyay, L. S. B. & Dutt, A. Microbial detoxification of residual organophosphate pesticides in agricultural practices. In Microbial Biotechnology (eds Patra, J. K. et al.) 225–242 (Springer Singapore, Singapore, 2017). https://doi.org/10.1007/978-981-10-6847-8_10.Chapter 

    Google Scholar 
    Hassan, Y. I., Lepp, D., He, J. & Zhou, T. Draft genome sequences of Devosia sp. strain 17-2-E-8 and Devosia riboflavina strain IFO13584. Genome Announ. https://doi.org/10.1128/genomeA.00994-14 (2014).Article 

    Google Scholar 
    Talwar, C. et al. Defining the environmental adaptations of genus Devosia: insights into its expansive short peptide transport system and positively selected genes. Sci. Rep. 10, 1151 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, F., Chen, L., Zhang, J., Yin, J. & Huang, S. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front. Microbiol. 8, 187 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Ho, A., Lonardo, D. P. D. & Bodelier, P. L. E. Revisiting life strategy concepts in environmental microbial ecology. Microbiol. Ecol. https://doi.org/10.1093/femsec/fix006 (2017).Article 

    Google Scholar 
    Lupatini, M., Korthals, G. W., de Hollander, M., Janssens, T. K. S. & Kuramae, E. E. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front. Microbiol. 7, 2064 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Wang, H. et al. Eight years of manure fertilization favor copiotrophic traits in paddy soil microbiomes. Eur. J. Soil Biol. 106, 103352 (2021).CAS 

    Google Scholar 
    Fließbach, A., Oberholzer, H.-R., Gunst, L. & Mäder, P. Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agric. Ecosyst. Environ. 118, 273–284 (2007).
    Google Scholar 
    Lewin, G. R. et al. Evolution and ecology of Actinobacteria and their bioenergy applications. Annu. Rev. Microbiol. 70, 235–254 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Karanja, E. N. et al. Diversity and structure of prokaryotic communities within organic and conventional farming systems in central highlands of Kenya. PLoS One 15, e0236574 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Francioli, D. et al. Mineral versus organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Front. Microbiol. 7, 1446 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Paungfoo-Lonhienne, C. et al. Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci. Rep. 5, 8678 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pang, Z. et al. Liming positively modulates microbial community composition and function of sugarcane fields. Agronomy 9, 808 (2019).CAS 

    Google Scholar 
    Aira, M., Gómez-Brandón, M., Lazcano, C., Bååth, E. & Domínguez, J. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol. Biochem. 42, 2276–2281 (2010).CAS 

    Google Scholar 
    Ma, M. et al. Responses of fungal community composition to long-term chemical and organic fertilization strategies in Chinese Mollisols. MicrobiologyOpen 7, e00597 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Bellenger, J. P., Darnajoux, R., Zhang, X. & Kraepiel, A. M. L. Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry 149, 53–73 (2020).
    Google Scholar 
    Schmidt, J. E. et al. Effects of agricultural management on rhizosphere microbial structure and function in processing tomato plants. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.01064-19 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Lin, Y. et al. Nitrosospira cluster 8a plays a predominant role in the nitrification process of a subtropical Ultisol under long-term inorganic and organic fertilization. Appl. Environ. Microbiol. 84, e01031-e1118 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chu, H. et al. Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Appl. Environ. Microbiol. 73, 485–491 (2007).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Xun, W. et al. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9, 35 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor

    Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, et al. A genomic catalog of Earth’s microbiomes. Nat Biotechnol. 2021;39:499–509.CAS 
    PubMed 

    Google Scholar 
    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.CAS 
    PubMed 

    Google Scholar 
    Cordovez V, Dini-Andreote F, Carrión VJ, Raaijmakers JM. Ecology and evolution of plant microbiomes. Annu Rev Microbiol. 2019;73:69–88.CAS 
    PubMed 

    Google Scholar 
    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.CAS 
    PubMed 

    Google Scholar 
    Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D, et al. The plant microbiome: From ecology to reductionism and beyond. Annu Rev Microbiol. 2020;74:81–100.CAS 
    PubMed 

    Google Scholar 
    Schmidt R, Ulanova D, Wick LY, Bode HB, Garbeva P. Microbe-driven chemical ecology: past, present and future. ISME J. 2019;13:2656–63.PubMed 
    PubMed Central 

    Google Scholar 
    Tyc O, Song C, Dickschat JS, Vos M, Garbeva P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017;25:280–92.CAS 
    PubMed 

    Google Scholar 
    Romero D, Traxler MF, López D, Kolter R. Antibiotics as signal molecules. Chem Rev. 2011;111:5492–505.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol. 2012;86:628–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol. 2018;20:1–15.PubMed 

    Google Scholar 
    Okada BK, Seyedsayamdost MR. Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev. 2017;41:19–33.CAS 
    PubMed 

    Google Scholar 
    Zhang C, Straight PD. Antibiotic discovery through microbial interactions. Curr Opin Microbiol. 2019;51:64–71.CAS 
    PubMed 

    Google Scholar 
    Traxler MF, Kolter R. Natural products in soil microbe interactions and evolution. Nat Prod Rep. 2015;32:956–70.CAS 
    PubMed 

    Google Scholar 
    Müller DB, Vogel C, Bai Y, Vorholt JA. The plant microbiota: systems-level insights and perspectives. Annu Rev Genet. 2016;50:211–34.PubMed 

    Google Scholar 
    Anckaert A, Arias AA, Hoff G, Calonne-Salmon M, Declerck S, Ongena M. The use of Bacillus spp. as bacterial biocontrol agents to control plant diseases. In: Köhl J, Ravensberg W, editors. Microbial bioprotectants for plant disease management. Cambridge, UK: Burleigh Dodds Science Publishing; 2022. p. 1–54.Dunlap CA. Taxonomy of registered Bacillus spp. strains used as plant pathogen antagonists. Biol Control. 2019;134:82–86.
    Google Scholar 
    Ye M, Tang X, Yang R, Zhang H, Li F, Tao F, et al. Characteristics and application of a novel species of Bacillus: Bacillus velezensis. ACS Chem Biol. 2018;13:500–5.CAS 
    PubMed 

    Google Scholar 
    Grubbs KJ, Bleich RM, Santa Maria KC, Allen SE, Farag S, Shank EA, et al. Large-scale bioinformatics analysis of Bacillus genomes uncovers conserved roles of natural products in bacterial physiology. mSystems 2017;2:e00040–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Harwood CR, Mouillon J-MM, Pohl S, Arnau J. Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev. 2018;42:721–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy. Front Plant Sci. 2019;10:1–19.
    Google Scholar 
    Li Y, Rebuffat S. The manifold roles of microbial ribosomal peptide-based natural products in physiology and ecology. J Biol Chem. 2020;295:34–54.Andrić S, Meyer T, Ongena M. Bacillus responses to plant-associated fungal and bacterial communities. Front Microbiol. 2020;11:1350.PubMed 
    PubMed Central 

    Google Scholar 
    Zhang L, Sun C. Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Appl Environ Microbiol. 2018;84:e00445–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Vela-Corcía D, Petras D, Díaz-Martínez L, Pérez-Lorente AI, Sopeña-Torres S, et al. Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence. Cell Rep. 2021;36:109449.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM, Petras D, et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun. 2019;10:1919.PubMed 
    PubMed Central 

    Google Scholar 
    Almoneafy AA, Kakar KU, Nawaz Z, Li B, Saand MA, Chun-lan Y, et al. Tomato plant growth promotion and antibacterial related-mechanisms of four rhizobacterial Bacillus strains against Ralstonia solanacearum. Symbiosis 2014;63:59–70.CAS 

    Google Scholar 
    Kakar KU, Duan Y-P, Nawaz Z, Sun G, Almoneafy AA, Hassan MA, et al. A novel rhizobacterium Bk7 for biological control of brown sheath rot of rice caused by Pseudomonas fuscovaginae and its mode of action. Eur J Plant Pathol. 2014;138:819–34.
    Google Scholar 
    Raynaud X, Nunan N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE. 2014;9:e87217.PubMed 
    PubMed Central 

    Google Scholar 
    Girard L, Lood C, Höfte M, Vandamme P, Rokni-Zadeh H, van Noort V, et al. The ever-expanding Pseudomonas genus: description of 43 new species and partition of the Pseudomonas putida group. Microorganisms. 2021;9:1–24.
    Google Scholar 
    Hua GKH, Höfte M. The involvement of phenazines and cyclic lipopeptide sessilin in biocontrol of Rhizoctonia root rot on bean (Phaseolus vulgaris) by Pseudomonas sp. CMR12a is influenced by substrate composition. Plant Soil. 2015;388:243–53.CAS 

    Google Scholar 
    Ma Z, Hoang Hua GKH, Ongena M, Höfte M. Role of phenazines and cyclic lipopeptides produced by Pseudomonas sp. CMR12a in induced systemic resistance on rice and bean. Environ Microbiol Rep. 2016;8:896–904.PubMed 

    Google Scholar 
    Olorunleke FE, Hua GKH, Kieu NP, Ma Z, Höfte M. Interplay between orfamides, sessilins and phenazines in the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environ Microbiol Rep. 2015;7:774–81.CAS 
    PubMed 

    Google Scholar 
    van Gestel J, Vlamakis H, Kolter R. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol. 2015;13:1–29.
    Google Scholar 
    Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol. 2012;79:176–91.CAS 
    PubMed 

    Google Scholar 
    Hoff G, Arias AA, Boubsi F, Pršić J, Meyer T, Ibrahim HMM, et al. Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of the Bacillus-plant mutualistic interaction. MBio 2021;12:e01774–21.CAS 
    PubMed Central 

    Google Scholar 
    Andrić S, Meyer T, Rigolet A, Prigent-Combaret C, Höfte M, Balleux G, et al. Lipopeptide interplay mediates molecular interactions between soil bacilli and pseudomonads. Microbiol Spectr. 2021;9:e0203821.PubMed 

    Google Scholar 
    Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 2010;11:395.
    Google Scholar 
    Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.CAS 
    PubMed 

    Google Scholar 
    Bodenhofer U, Bonatesta E, Horejš-Kainrath C, Hochreiter S. msa: an R package for multiple sequence alignment. Bioinformatics. 2015;31:3997–9.CAS 
    PubMed 

    Google Scholar 
    Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004;20:289–90.CAS 
    PubMed 

    Google Scholar 
    Ivica Letunic PB. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–W296.PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team (2020). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.Steinke K, Mohite OS, Weber T, Kovács ÁT. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems. 2021;6:2–10.
    Google Scholar 
    Molinatto G, Puopolo G, Sonego P, Moretto M, Engelen K, Viti C, et al. Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499, a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol. 2016;238:56–59.CAS 
    PubMed 

    Google Scholar 
    Fan B, Wang C, Song X, Ding X, Wu L, Wu H, et al. Bacillus velezensis FZB42 in 2018: The gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol. 2018;9:3389.
    Google Scholar 
    Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13:614–29.PubMed 
    PubMed Central 

    Google Scholar 
    Scholz R, Vater J, Budiharjo A, Wang Z, He Y, Dietel K, et al. Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol. 2014;196:1842–52.PubMed 
    PubMed Central 

    Google Scholar 
    Lembrechts JJ, van den Hoogen J, Aalto J, Ashcroft MB, De Frenne P, Kemppinen J, et al. Global maps of soil temperature. Glob Chang Biol. 2022;28:3110–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blake C, Christensen MN, Kovacs AT. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol Plant-Microbe Interact. 2021;34:15–25.CAS 
    PubMed 

    Google Scholar 
    Arnaouteli S, Bamford NC, Stanley-Wall NR, Kovács ÁT. Bacillus subtilis biofilm formation and social interactions. Nat Rev Microbiol. 2021;19:600–14.CAS 
    PubMed 

    Google Scholar 
    D’aes J, Hua GKH, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, et al. Biological control of Rhizoctonia root rot on bean by phenazine- and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology. 2011;101:996–1004.PubMed 

    Google Scholar 
    Grandchamp GM, Caro L, Shank EA. Pirated siderophores promote sporulation in Bacillus subtilis. Appl Environ Microbiol. 2017;83:e03293–16.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miethke M, Klotz O, Linne U, May JJ, Beckering CL, Marahiel MA. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol Microbiol. 2006;61:1413–27.CAS 
    PubMed 

    Google Scholar 
    Pi H, Helmann JD. Genome-wide characterization of the fur regulatory network reveals a link between catechol degradation and bacillibactin metabolism in Bacillus subtilis. MBio. 2018;9:1–15.
    Google Scholar 
    Adler C, Corbalán NS, Seyedsayamdost MR, Pomares MF, de Cristóbal RE, Clardy J, et al. Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS ONE. 2012;7:e46754.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Trottmann F, Franke J, Ishida K, García-Altares M, Hertweck C. A pair of bacterial siderophores releases and traps an intercellular signal molecule: an unusual case of natural nitrone bioconjugation. Angew Chem. 2019;58:200–4.CAS 

    Google Scholar 
    Mongkolsuk S, Helmann JD. Regulation of inducible peroxide stress responses. Mol Microbiol. 2002;45:9–15.CAS 
    PubMed 

    Google Scholar 
    Cox CD, Rinehart KL, Moore ML, Cook JC. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 1981;78:4256–60.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Youard ZA, Mislin GLA, Majcherczyk PA, Schalk IJ, Reimmann C. Pseudomonas fluorescens CHA0 produces enantio-pyochelin, the optical antipode of the Pseudomonas aeruginosa siderophore pyochelin. J Biol Chem. 2007;282:35546–53.CAS 
    PubMed 

    Google Scholar 
    Ronnebaum TA, Lamb AL. Nonribosomal peptides for iron acquisition: pyochelin biosynthesis as a case study. Curr Opini Struct Biol. 2018;53:1–11.CAS 

    Google Scholar 
    Seipke RF, Song L, Bicz J, Laskaris P, Yaxley AM, Challis GL, et al. The plant pathogen Streptomyces scabies 87-22 has a functional pyochelin biosynthetic pathway that is regulated by TetR- and AfsR-family proteins. Microbiology. 2011;157:2681–93.CAS 
    PubMed 

    Google Scholar 
    Gu S, Wei Z, Shao Z, Friman VP, Cao K, Yang T, et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020;5:1002–10.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Komaki H, Ichikawa N, Hosoyama A, Hamada M, Igarashi Y. In silico analysis of PKS and NRPS gene clusters in arisostatin-and kosinostatin-producers and description of Micromonospora okii sp. nov. Antibiotics. 2021;10:1447.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Engelbrecht A, Saad H, Gross H, Kaysser L. Natural products from Nocardia and their role in pathogenicity. Micro Physiol. 2021;31:217–32.
    Google Scholar 
    Inahashi Y, Zhou S, Bibb MJ, Song L, Al-Bassam MM, Bibb MJ, et al. Watasemycin biosynthesis in Streptomyces venezuelae: thiazoline C-methylation by a type B radical-SAM methylase homologue. Chem Sci. 2017;8:2823–31.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Song J, Qiu S, Zhao J, Han C, Wang Y, Sun X, et al. Pseudonocardia tritici sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L.). Nat Microbiol. 2019;12:470–80.
    Google Scholar 
    Sayed AM, Abdel-Wahab NM, Hassan HM, Abdelmohsen UR. Saccharopolyspora: an underexplored source for bioactive natural products. J Appl Microbiol. 2020;128:314–29.CAS 
    PubMed 

    Google Scholar 
    Nordstedt NP, Jones ML. Genomic analysis of Serratia plymuthica MBSA-MJ1: A plant growth promoting rhizobacteria that improves water stress tolerance in greenhouse ornamentals. Front Microbiol. 2021;12:653556.PubMed 
    PubMed Central 

    Google Scholar 
    Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3:470–80.CAS 
    PubMed 

    Google Scholar 
    Takahashi Y, Malisorn K, Kanchanasin P, Phongsopitanun W, Tanasupawat S, Spain AM, et al. Actinomadura rhizosphaerae sp. nov., isolated from rhizosphere soil of the plant Azadirachta indica. ISME J 2018;68:3012–6.
    Google Scholar 
    Takahashi Y. Genus Kitasatospora, taxonomic features and diversity of secondary metabolites. J Antibiot. 2017;70:506–13.CAS 

    Google Scholar 
    Bennur T, Kumar AR, Zinjarde S, Javdekar V. Nocardiopsis species: Incidence, ecological roles and adaptations. Microbiol Res. 2015;174:33–47.PubMed 

    Google Scholar 
    Walterson AM, Stavrinides J. Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. J Basic Microbiol. 2015;39:33–47.
    Google Scholar 
    Sungthong R, Nakaew N. The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. J Basic Microbiol. 2015;55:554–65.PubMed 

    Google Scholar 
    Müller S, Strack SN, Ryan SE, Kearns DB, Kirby JR. Predation by Myxococcus xanthus induces Bacillus subtilis to form spore-filled megastructures. Appl Environ Microbiol. 2015;81:203–10.PubMed 

    Google Scholar 
    Straight PD, Fischbach MA, Walsh CT, Rudner DZ, Kolter R. A singular enzymatic megacomplex from Bacillus subtilis. Proc Natl Acad Sci USA. 2007;104:305–10.CAS 
    PubMed 

    Google Scholar 
    Barger SR, Hoefler BC, Cubillos-Ruiz A, Russell WK, Russell DH, Straight PD. Imaging secondary metabolism of Streptomyces sp. Mg1 during cellular lysis and colony degradation of competing Bacillus subtilis. Antonie van Leeuwenhoek. 2012;102:435–45.CAS 
    PubMed 

    Google Scholar 
    Ogran A, Yardeni EH, Keren-Paz A, Bucher T, Jain R, Gilhar O, et al. The plant host induces antibiotic production to select the most-beneficial colonizers. Appl Environ Microbiol. 2019;85:1–15.
    Google Scholar 
    Rosenberg G, Steinberg N, Oppenheimer-Shaanan Y, Olender T, Doron S, Ben-Ari J, et al. Not so simple, not so subtle: The interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. npj Biofilms Microbiomes. 2016;2:15027.PubMed 
    PubMed Central 

    Google Scholar 
    Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol. 2006;188:4918–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hoefler BC, Gorzelnik KV, Yang JY, Hendricks N, Dorrestein PC, Straight PD. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc Natl Acad Sci USA. 2012;109:13082–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu Y, Kyle S, Straight PD. Antibiotic stimulation of a Bacillus subtilis migratory response. mSphere 2018;3:e00586–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Qi G, Zhu F, Du P, Yang X, Qiu D, Yu Z, et al. Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides. 2010;31:1978–86.CAS 
    PubMed 

    Google Scholar 
    McCully LM, Bitzer AS, Seaton SC, Smith LM, Silby MW. Interspecies social spreading: interaction between two sessile soil bacteria leads to emergence of surface motility. mSphere. 2019;4:e00696–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14:563–75.CAS 
    PubMed 

    Google Scholar 
    Townsley L, Shank EA. Natural-product antibiotics: cues for modulating bacterial biofilm formation. Trends Microbiol. 2017;25:1016–26.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sun X, Xu Z, Xie J, Hesselberg-Thomsen V, Tan T, Zheng D, et al. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME J. 2022;16:774–87.CAS 
    PubMed 

    Google Scholar 
    Dumas Z, Ross-Gillespie A, Kümmerli R. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc R Soc B Biol Sci. 2013;280:20131055.
    Google Scholar 
    Lee N, Kim W, Chung J, Lee Y, Cho S, Jang KS, et al. Iron competition triggers antibiotic biosynthesis in Streptomyces coelicolor during coculture with Myxococcus xanthus. ISME J. 2020;14:1111–24.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020;18:152–63.CAS 
    PubMed 

    Google Scholar 
    Niehus R, Picot A, Oliveira NM, Mitri S, Foster KR. The evolution of siderophore production as a competitive trait. Evolution. 2017;71:1443–55.CAS 
    PubMed 

    Google Scholar 
    Ho YN, Lee HJ, Hsieh CT, Peng CC, Yang YL. Chemistry and biology of salicyl-capped siderophores. Stud Nat Prod Chem. 2018;59:431–90.Schalk IJ, Rigouin C, Godet J. An overview of siderophore biosynthesis among fluorescent Pseudomonads and new insights into their complex cellular organization. Environ Microbiol. 2020;22:1447–66.PubMed 

    Google Scholar 
    Deveau A, Gross H, Palin B, Mehnaz S, Schnepf M, Leblond P, et al. Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiol Ecol. 2016;92:1–11.
    Google Scholar 
    Jenul C, Keim K, Jens J, Zeiler MJ, Schilcher K, Schurr M, et al. Pyochelin biotransformation shapes bacterial competition. bioRxiv. 2022. https://doi.org/10.1101/2022.04.18.486787.Ho YN, Hoo SY, Wang BW, Hsieh CT, Lin CC, Sun CH, et al. Specific inactivation of an antifungal bacterial siderophore by a fungal plant pathogen. ISME J. 2021;15:1858–61.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lopez-Medina E, Fan D, Coughlin LA, Ho EX, Lamont IL, Reimmann C, et al. Candida albicans inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog. 2015;11:1–34.
    Google Scholar 
    Meisel JD, Panda O, Mahanti P, Schroeder FC, Kim DH. Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell. 2014;159:267–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Finkel OM, Castrillo G, Herrera Paredes S, Salas González I, Dangl JL. Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol. 2017;38:155–63.PubMed 
    PubMed Central 

    Google Scholar 
    Saad MM, Eida AA, Hirt H, Doerner P. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J Exp Bot. 2020;71:3878–901.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ansari FA, Ahmad I. Fluorescent Pseudomonas -FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci Rep. 2019;9:4547.PubMed 
    PubMed Central 

    Google Scholar 
    Domenech J, Reddy MS, Kloepper JW, Ramos B, Gutierrez-Mañero J. Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato. BioControl. 2006;51:245–58.CAS 

    Google Scholar 
    Powers MJ, Sanabria-Valentín E, Bowers AA, Shank EA. Inhibition of cell differentiation in Bacillus subtilis by Pseudomonas protegens. J Bacteriol. 2015;197:2129–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Transmission of stony coral tissue loss disease (SCTLD) in simulated ballast water confirms the potential for ship-born spread

    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    NOAA. Stony Coral Tissue Loss Disease Case Definition. NOAA, Silver Spring, MD 10 (2018).Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front Mar. Sci. 6, 00678 (2019).
    Google Scholar 
    Landsberg, J. H. et al. Stony coral tissue loss disease in Florida is associated with disruption of host–zooxanthellae physiology. Front Mar. Sci. 7, 576013 (2020).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by Stony Coral Tissue Loss Disease. PeerJ 8, 9289 (2020).
    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an endemic zone. Front Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease. Front Mar. Sci. 8, 750658 (2021).
    Google Scholar 
    Veglia, A. J. et al. Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands. Microbiol. Resource Announc. 11, e01199-e1221 (2022).CAS 

    Google Scholar 
    Rosales, S. M. et al. Bacterial metabolic potential and micro-eukaryotes enriched in stony coral tissue loss disease lesions. Front Mar. Sci. 8, 776859 (2022).
    Google Scholar 
    Rosales, S. M., Clark, A. S., Huebner, L. K., Ruzicka, R. R. & Muller, E. M. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11, 681 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Studivan, M. S. et al. Reef sediments can act as a stony coral tissue loss disease vector. Front Mar. Sci. 8, 815698 (2022).
    Google Scholar 
    Meyer, J. L. et al. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front. Microbiol. 10, 2244 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Ushijima, B. et al. Disease diagnostics and potential coinfections by Vibrio coralliilyticus during an ongoing coral disease outbreak in Florida. Front. Microbiol. 11, 2682 (2020).
    Google Scholar 
    Meiling, S. S. et al. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front Mar. Sci. 8, 670829 (2021).
    Google Scholar 
    Becker, C. C., Brandt, M., Miller, C. A. & Apprill, A. Microbial bioindicators of stony coral tissue loss disease identified in corals and overlying waters using a rapid field-based sequencing approach. Environ. Microbiol. 24, 1166–1182 (2021).PubMed 

    Google Scholar 
    Dobbelaere, T., Muller, E. M., Gramer, L. J., Holstein, D. M. & Hanert, E. Coupled epidemio-hydrodynamic modeling to understand the spread of a deadly coral disease in Florida. Front Mar. Sci. 7, 591881 (2020).
    Google Scholar 
    Dobbelaere, T. et al. Connecting the dots: Transmission of stony coral tissue loss disease from the Marquesas to the Dry Tortugas. Front Mar. Sci. 9, 778938 (2022).
    Google Scholar 
    Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front Mar. Sci. 7, 00163 (2020).
    Google Scholar 
    Sharp, W. C., Shea, C. P., Maxwell, K. E., Muller, E. M. & Hunt, J. H. Evaluating the small-scale epidemiology of the stony-coral-tissue-loss-disease in the middle Florida Keys. PLoS ONE 15, e0241871 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williamson, O. M., Dennison, C. E., O’Neil, K. L. & Baker, A. C. Susceptibility of Caribbean brain coral recruits to stony coral tissue loss disease (SCTLD). Front Mar. Sci. 9, 821165 (2022).
    Google Scholar 
    Noonan, K. R. & Childress, M. J. Association of butterflyfishes and stony coral tissue loss disease in the Florida Keys. Coral Reefs 39, 1581–1590 (2020).
    Google Scholar 
    Dahlgren, C., Pizarro, V., Sherman, K., Greene, W. & Oliver, J. Spatial and temporal patterns of stony coral tissue loss disease outbreaks in the Bahamas. Front Mar. Sci. 8, 682114 (2021).
    Google Scholar 
    Rosenau, N. A. et al. Considering commercial vessels as potential vectors of stony coral tissue loss disease. Front Mar. Sci. 8, 709764 (2021).
    Google Scholar 
    Roth, L., Kramer, P., Doyle, E. & O’Sullivan, C. Caribbean SCTLD Dashboard. Available www.agrra.org. Accessed 06 Mar 2021. (2020).Brandt, M. E. et al. The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Front Mar. Sci. 8, 715329 (2021).
    Google Scholar 
    Bailey, S. A. et al. Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective. Divers. Distrib. 26, 1780–1797 (2020).MathSciNet 

    Google Scholar 
    Hewitt, C. L., Gollasch, S. & Minchin, D. The vessel as a vector: Biofouling, ballast water and sediments. In Biological Invasions in Marine Ecosystems Vol. 204 (eds Rilov, G. & Crooks, J. A.) 117–131 (Springer, 2009).
    Google Scholar 
    Zabin, C. J. et al. Small boats provide connectivity for nonindigenous marine species between a highly invaded international port and nearby coastal harbors. Manag. Biol. Invas. 5, 97–112 (2014).
    Google Scholar 
    Ashton, G. V., Zabin, C. J., Davidson, I. C. & Ruiz, G. M. Recreational boats routinely transfer organisms and promote marine bioinvasions. Biol. Invas. 24, 1083–1096 (2022).
    Google Scholar 
    Drake, L. A., Doblin, M. A. & Dobbs, F. C. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar. Pollut. Bull. 55, 333–341 (2007).CAS 
    PubMed 

    Google Scholar 
    Pagenkopp Lohan, K. M., Fleischer, R. C., Carney, K. J., Holzer, K. K. & Ruiz, G. M. Amplicon-based pyrosequencing reveals high diversity of protistan parasites in ships’ ballast water: Implications for biogeography and infectious diseases. Microb. Ecol. 71, 530–542 (2015).PubMed 

    Google Scholar 
    Ruiz, G. M. et al. Global spread of microorganisms by ships. Nature 408, 49–50 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hwang, J., Park, S. Y., Lee, S. & Lee, T. K. High diversity and potential translocation of DNA viruses in ballast water. Mar. Pollut. Bull. 137, 449–455 (2018).CAS 
    PubMed 

    Google Scholar 
    Shikuma, N. J. & Hadfield, M. G. Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae. Biofouling 26, 39–46 (2009).
    Google Scholar 
    Aguirre-Macedo, M. L. et al. Ballast water as a vector of coral pathogens in the Gulf of Mexico: The case of the Cayo Arcas coral reef. Mar. Pollut. Bull. 56, 1570–1577 (2008).CAS 
    PubMed 

    Google Scholar 
    Bruno, J. F. The coral disease triangle. Nat. Clim. Chang. 5, 302–303 (2015).ADS 

    Google Scholar 
    Lakshmi, E., Priya, M. & Achari, V. S. An overview on the treatment of ballast water in ships. Ocean Coast. Manag. 199, 105296 (2021).
    Google Scholar 
    Petersen, N. B., Madsen, T., Glaring, M. A., Dobbs, F. C. & Jørgensen, N. O. G. Ballast water treatment and bacteria: Analysis of bacterial activity and diversity after treatment of simulated ballast water by electrochlorination and UV exposure. Sci. Total Environ. 648, 408–421 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Romero-Martínez, L., Moreno-Andrés, J., Acevedo-Merino, A. & Nebot, E. Evaluation of ultraviolet disinfection of microalgae by growth modeling: Application to ballast water treatment. J. Appl. Phycol. 28, 2831–2842 (2016).
    Google Scholar 
    First, M. R. et al. Stratification of living organisms in ballast tanks: How do organism concentrations vary as ballast water is discharged?. Environ. Sci. Technol. 47, 4442–4448 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Drake, L. A. et al. Microbial ecology of ballast water during a transoceanic voyage and the effects of open-ocean exchange. Mar. Ecol. Prog. Ser. 233, 13–20 (2002).ADS 

    Google Scholar 
    Khandeparker, L., Kuchi, N., Desai, D. V. & Anil, A. C. Changes in the ballast water tank bacterial community during a trans-sea voyage: Elucidation through next generation DNA sequencing. J. Environ. Manag. 273, 111018 (2020).
    Google Scholar 
    Ruiz, G. M., Lorda, J., Arnwine, A. & Lion, K. Shipping patterns associated with the Panama Canal: Effects on biotic exchange? In Bridging Divides Vol. 83 (eds Gollasch, S. et al.) 113–126 (Springer, 2006).
    Google Scholar 
    Pagano, A., Wang, G., Sánchez, O., Ungo, R. & Tapiero, E. The impact of the Panama Canal expansion on Panama’s maritime cluster. Marit. Policy Manag. 43, 164–178 (2016).
    Google Scholar 
    Muirhead, J. R., Minton, M. S., Miller, W. A. & Ruiz, G. M. Projected effects of the Panama Canal expansion on shipping traffic and biological invasions. Divers. Distrib. 21, 75–87 (2015).
    Google Scholar 
    Ros, M. et al. The Panama Canal and the transoceanic dispersal of marine invertebrates: Evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean. Mar. Environ. Res. 99, 204–211 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stehouwer, P. P., Buma, A. & Peperzak, L. A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environ. Technol. 36, 2094–2104 (2015).CAS 
    PubMed 

    Google Scholar 
    Wu, Y., Li, Z., Du, W. & Gao, K. Physiological response of marine centric diatoms to ultraviolet radiation, with special reference to cell size. J. Photochem. Photobiol., B 153, 1–6 (2015).CAS 

    Google Scholar 
    Aguirre, L. E. et al. Diatom frustules protect DNA from ultraviolet light. Sci. Rep. 8, 5138 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    First, M. R. & Drake, L. A. Life after treatment: Detecting living microorganisms following exposure to UV light and chlorine dioxide. J. Appl. Phycol. 26, 227–235 (2014).CAS 

    Google Scholar 
    Liebich, V., Stehouwer, P. P. & Veldhuis, M. Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat. Invas. 7, 29–36 (2012).
    Google Scholar 
    Hess-Erga, O. K., Moreno-Andrés, J., Enger, Ø. & Vadstein, O. Microorganisms in ballast water: Disinfection, community dynamics, and implications for management. Sci. Total Environ. 657, 704–716 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Endresen, Ø., Lee Behrens, H., Brynestad, S., Bjørn Andersen, A. & Skjong, R. Challenges in global ballast water management. Mar. Pollut. Bull. 48, 615–623 (2004).CAS 
    PubMed 

    Google Scholar 
    Vorkapić, A., Radonja, R. & Zec, D. Cost efficiency of ballast water treatment systems based on ultraviolet irradiation and electrochlorination. Promet Traffic Transp. 30, 343–348 (2018).
    Google Scholar 
    King, D., Hagan, P., Riggio, M. & Wright, D. Preview of global ballast water treatment markets. J. Mar. Eng. Technol. 11, 3–15 (2012).
    Google Scholar 
    Wang, Z., Saebi, M., Corbett, J. J., Grey, E. K. & Curasi, S. R. Integrated biological risk and cost model analysis supports a geopolitical shift in ballast water management. Environ. Sci. Technol. 55, 12791–12800 (2021).CAS 
    PubMed 

    Google Scholar 
    Moreno-Andrés, J. & Peperzak, L. Operational and environmental factors affecting disinfection byproducts formation in ballast water treatment systems. Chemosphere 232, 496–505 (2019).ADS 
    PubMed 

    Google Scholar 
    David, M., Linders, J., Gollasch, S. & David, J. Is the aquatic environment sufficiently protected from chemicals discharged with treated ballast water from vessels worldwide? A decadal environmental perspective and risk assessment. Chemosphere 207, 590–600 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    U.S. Environmental Protection Agency. Generic protocol for the verification of ballast water treatment technology, version 5.1. Report number EPA/600/R-10/146. Washington, D.C. 157 (2010).Evans, J. S., Paul, V. J., Ushijima, B. & Kellogg, C. A. Combining tangential flow filtration and size fractionation of mesocosm water as a method for the investigation of waterborne coral diseases. Biol. Methods Protocols 7, bpac007 (2022).
    Google Scholar 
    Fujimoto, M. et al. Application of Ion Torrent sequencing to the assessment of the effect of alkali ballast water treatment on microbial community diversity. PLoS ONE 9, e107534 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    United States Coast Guard. Ballast Water Best Management Practices to Reduce the Likelihood of Transporting Pathogens That May Spread Stony Coral Tissue Loss Disease. Marine Safety Information Bulletin 07–19. Washington, D.C. 2 (2019).Bolton, J. R. & Linden, K. G. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. J. Environ. Eng. 129, 209–215 (2003).CAS 

    Google Scholar 
    Enochs, I. C. et al. The influence of diel carbonate chemistry fluctuations on the calcification rate of Acropora cervicornis under present day and future acidification conditions. J. Exp. Mar. Biol. Ecol. 506, 135–143 (2018).CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Preprint at https://www.r-project.org/ (2019).Therneau, T. M. survival: A package for survival analysis in R. R package version 3.2–13. (2021).Kassambara, A., Kosinski, M. & Biecek, P. survminer: Drawing survival curves using “ggplot2”. R package version 0.4.9. (2021).Bakalar, G. Review of interdisciplinary devices for detecting the quality of ship ballast water. Springerplus 3, 468 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Water Environmental Federation & American Public Health Association. Standard methods for the examination of water and wastewater. Washington, D.C. 21 (2005).Steinberg, M. K., Lemieux, E. J. & Drake, L. A. Determining the viability of marine protists using a combination of vital, fluorescent stains. Mar. Biol. 158, 1431–1437 (2011).
    Google Scholar 
    Oksanen, J. et al. vegan: Community ecology package. R package version 2.0–10. (2015).Martinez Arbizu, P. pairwiseAdonis: Pairwise multilevel comparison using adonis. R package version 0.4. (2020).Studivan, MS. Mstudiva/SCTLD-ballast-transmission: Stony coral tissue loss disease ballast transmission and treatment (Version 1.0), Zenodo, https://doi.org/10.5281/zenodo.6561517 (2022). More

  • in

    Essential oils of plants and their combinations as an alternative adulticides against Anopheles gambiae (Diptera: Culicidae) populations

    WHO. Global plan for insecticide management. (World Health Organisation, Geneva, Switzerland 130, 2012).WHO. Paludisme: situation mondiale. vol. 2507. World Health Organisation, Geneva, Switzerland, (2020).WHO. Procédures pour tester la résistance aux insecticides chez les moustiques vecteurs du paludisme Seconde édition. (World Health Organisation, Geneva, Switzerland, 2017).WHO. Guidelines for Malaria Vector Control. (World Health Organisation, Geneva, Switzerland, 2019).Churcher, T. S., Lissenden, N., Griffin, J. T., Worrall, E. & Ranson, H. The impact of pyrethroid resistance on the efficacy and effectiveness of bednets for malaria control in Africa. Elife 5, 16090 (2016).
    Google Scholar 
    Hemingway, J. et al. Averting a malaria disaster: Will insecticide resistance derail malaria control?. Lancet 387, 1785–1788 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Dabiré, K. R. et al. Trends in insecticide resistance in natural populations of malaria vectors in Burkina Faso, West Africa: 10 Years surveys K. INTECH 32, 479–502 (2012).
    Google Scholar 
    WHO. WHO Global Malaria Programme: Global Plan for insecticide resistance management. (World Health Organisation, Geneva, Switzerland, 2012).Toe, K. H. et al. Do bednets including piperonyl butoxide offer additional protection against populations of Anopheles gambiae s.l. that are highly resistant to pyrethroids? An experimental hut evaluation in Burkina Faso. Med. Vet. Entomol. 32, 407–416 (2018).CAS 
    PubMed 

    Google Scholar 
    Hien, A. S. et al. Evidence supporting deployment of next generation insecticide treated nets in Burkina Faso: Bioassays with either chlorfenapyr or piperonyl butoxide increase mortality of pyrethroid-resistant Anopheles gambiae. Malar. J. 20, 1–12 (2021).
    Google Scholar 
    Zoubiri, S. & Baaliouamer, A. Potentiality of plants as source of insecticide principles. J. Saudi Chem. Soc. 18, 925–938 (2014).
    Google Scholar 
    Tripathi, A. K., Upadhyay, S., Bhuiyan, M. & Bhattacharya, P. R. A review on prospects of essential oils as biopesticide in insect-pest management. J. Pharmacogn. Phytother. 1, 52–63 (2009).CAS 

    Google Scholar 
    Isman, M. B. Plant essential oils for pest and disease management. Crop Prot. 19, 603–608 (2000).ADS 
    CAS 

    Google Scholar 
    Mossa, A. T. H. Green pesticides: Essential oils as biopesticides in insect-pest management. J. Environ. Sci. Technol. 9, 354–378 (2016).CAS 

    Google Scholar 
    Lucia, A. et al. Larvicidal effect of Eucalyptus grandis essential oil and turpentine and their major components on Aedes aegypti larvae. J. Am. Mosq. Control Assoc. 23, 299–303 (2007).CAS 
    PubMed 

    Google Scholar 
    Singh, R., Koul, O. & Rup, P. J. Toxicity of some essential oil constituents and their binary mixtures against Chilo partellus (Lepidoptera: Pyralidae). Int. J. Tropical Insect Sci. 29, 93–101 (2009).CAS 

    Google Scholar 
    Sarma, R., Adhikari, K., Mahanta, S. & Khanikor, B. Combinations of plant essential oil based terpene compounds as larvicidal and adulticidal agent against Aedes aegypti (Diptera: Culicidae). Sci. Rep. 9, 1–13 (2019).ADS 

    Google Scholar 
    Mansour, S. A., Foda, M. S. & Aly, A. R. Mosquitocidal activity of two Bacillus bacterial endotoxins combined with plant oils and conventional insecticides. Ind. Crops Prod. 35, 44–52 (2012).CAS 

    Google Scholar 
    Yaméogo, F., Wendgida, D. W., Sombié, A., Sanon, A. & Badolo, A. Insecticidal activity of essential oils from six aromatic plants against Aedes aegypti, dengue vector from two localities of Ouagadougou Burkina Faso. Arthropod. Plant. Interact. 15, 627–634 (2021).
    Google Scholar 
    Wangrawa, D. W. et al. Essential oils and their binary combinations have synergistic and antagonistic insecticidal properties against Anopheles gambiae s l. (Diptera: Culicidae). Biocatal. Agric. Biotechnol. 42, 102347 (2022).CAS 

    Google Scholar 
    Drabo, S. F., Olivier, G., Bassolé, I. H. N., Nébié, R. C. & Laurence, M. Susceptibility of MED-Q1 and MED-Q3 biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae) populations to essential and seed oils. J. Econ. Entomol. 110, 1031–1038 (2017).
    Google Scholar 
    N’Guessan, R., Corbel, V., Akogbéto, M. & Rowland, M. Treated nets and indoor residual reduced efficacy of insecticide-pyrethroid resistance area benin. Emerg. Infect. Dis. 13, 199–206 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    WHO. Standard operating procedure for testing insecticide susceptibility of adult mosquitoes in WHO tube tests. (World Health Organisation, Geneva, Switzerland 2022).Abbott, W. S. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265–267 (1925).CAS 

    Google Scholar 
    Schelz, Z., Molnar, J. & Hohmann, J. Antimicrobial and antiplasmid activities of essential oils. Fitoterapia 77, 279–285 (2006).CAS 
    PubMed 

    Google Scholar 
    Bassolé, I. H. N. & Juliani, H. R. Essential oils in combination and their antimicrobial properties. Molecules 17, 3989–4006 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    WHO. Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes Second edition. (World Health Organisation, Geneva, Switzerland 2016).Tchoumbougnang, F. et al. Activité larvicide sur Anopheles gambiae giles et composition chimique des huiles essentielles extraites de quatre plantes cultivées au Cameroun. Biotechnol. Agron. Soc. Environ. 13, 77–84 (2009).CAS 

    Google Scholar 
    Ranson, H. & Lissenden, N. Insecticide resistance in African Anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 32, 187–196 (2016).CAS 
    PubMed 

    Google Scholar 
    Wangrawa, D. et al. Insecticidal activity of local plants essential oils against laboratory and field strains of Anopheles gambiae s. L. (Diptera: Culicidae) from Burkina Faso. J. Econ. Entomol. 111, 2844–2853 (2018).CAS 
    PubMed 

    Google Scholar 
    Gbolade, A. A. & Lockwood, G. B. Toxicity of Ocimum sanctum L. essential oil to Aedes aegypti larvae and its chemical composition. J. Essent. Oil Bearing Plants 11, 148–153 (2008).CAS 

    Google Scholar 
    Vani, R. S., Cheng, S. F. & Chuah, C. H. Comparative study of volatile compounds from genus Ocimum. Am. J. Appl. Sci. 6, 523–528 (2009).CAS 

    Google Scholar 
    Bassolé, et al. Ovicidal and larvicidal activity against Aedes aegypti and Anopheles gambiae complex mosquitoes of essential oils extracted from three spontaneous plants of Burkina Faso. Parasitologia 45, 23–26 (2003).
    Google Scholar 
    Peerzada, N. Chemical composition of the essential oil of Hyptis Suaveolens. Molecules 2, 165–168 (1997).CAS 

    Google Scholar 
    Ilboudo, Z. et al. Biological activity and persistence of four essential oils towards the main pest of stored cowpeas, Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). J. Stored Prod. Res. 46, 124–128 (2010).CAS 

    Google Scholar 
    Zulfikar, A. & Sitepu, F. Y. The effect of lemongrass (Cymbopogon nardus) extract as insecticide against Aedes aegypti. Int. J. Mosq. Res. 6, 101–103 (2019).
    Google Scholar 
    Ojewumi, E. M., Oladipupo, A. A. & Ojewumi, O. E. Oil extract from local leaves an alternative to synthetic mosquito repellants. Pharmacophore 9, 1–6 (2018).
    Google Scholar 
    Gnankiné, O. & Bassolé, I. H. N. Essential oils as an alternative to pyrethroids resistance against Anopheles species complex giles (Diptera: Culicidae). Molecules 22, 1321 (2017).PubMed Central 

    Google Scholar 
    Bossou, A. D. et al. Chemical composition and insecticidal activity of plant essential oils from Benin against Anopheles gambiae (Giles). Parasit. Vectors 6, 337 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Balboné, et al. Essential oils from five local plants: An alternative larvicide for Anopheles gambiae s. I. (Diptera: Culicidae) and Aedes aegypti (Diptera: Culicidae) control in Western Burkina Faso. Front. Trop. Dis. 3, 853405 (2022).
    Google Scholar 
    Bekele, J. & Hassanali, A. Blend effects in the toxicity of the essential oil constituents of Ocimum kilimandscharicum and Ocimum kenyense (Labiateae) on two post-harvest insect pests. Phytochemistry 57, 385–391 (2001).CAS 
    PubMed 

    Google Scholar 
    Pavela, R. Acute and synergistic effects of some monoterpenoid essential oil compounds on the house fly (Musca domestica). J. Essent. Oil Bearing Plants 11, 451–459 (2008).CAS 

    Google Scholar 
    Tanprasit, P. Biological control of dengue fever mosquitoes (Aedes aegypti Linn.) using leaf extracts of Chan (Hyptis suaveolens (L) poit.) and hedge flower Lantana camara Linn.). (2005).Park, H. M. et al. Larvicidal activity of myrtaceae essential oils and their components against Aedes aegypti, acute toxicity on Daphnia magna, and aqueous residue. J. Med. Entomol. 48, 405–410 (2011).CAS 
    PubMed 

    Google Scholar 
    Burt, S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 94, 223–253 (2004).CAS 
    PubMed 

    Google Scholar 
    Abbassy, M. A., Abdelgaleil, S. A. M. & Rabie, R. Y. A. Insecticidal and synergistic effects of Majorana hortensis essential oil and some of its major constituents. Entomol. Exp. Appl. 131, 225–232 (2009).CAS 

    Google Scholar 
    Chiasson, H., Bélanger, A., Bostanian, N., Vincent, C. & Poliquin, A. Acaricidal properties of Artemisia absinthium and Tanacetum vulgare (Asteraceae) essential oils obtained by three methods of extraction. J. Econ. Entomol. 94, 167–171 (2001).CAS 
    PubMed 

    Google Scholar 
    Luz, T. R. S. A., deMesquita, L. S. S., Amaral, F. M. M. & Coutinho, D. F. Essential oils and their chemical constituents against Aedes aegypti L. (Diptera: Culicidae) larvae. Acta Trop. 212, 105705 (2020).CAS 
    PubMed 

    Google Scholar 
    Deletre, E., Mallent, M., Menut, C., Chandre, F. & Martin, T. Behavioral response of Bemisia tabaci (Hemiptera: Aleyrodidae) to 20 plant extracts. J. Econ. Entomol. 108, 1890–1901 (2015).
    Google Scholar 
    Berenbaum, M. A. Y. & Neal, J. J. Synergism between myristicin and xanthotoxin, a naturally cooccurring plant toxicant. J. Chem. Ecol. 11, 1349–1358 (1985).CAS 
    PubMed 

    Google Scholar 
    Intirach, J. et al. Chemical constituents and combined larvicidal effects of selected essential oils against Anopheles cracens (Diptera: Culicidae). Psyche (London) https://doi.org/10.1155/2012/591616 (2012).
    Google Scholar 
    Pavela, R. Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) larvae. Ind. Crops Prod. 60, 247–258 (2014).CAS 

    Google Scholar 
    Muturi, E. J., Ramirez, J. L., Doll, K. M. & Bowman, M. J. Combined toxicity of three essential oils against Aedes aegypti (Diptera: Culicidae) larvae. J. Med. Entomol. 54, 1684–1691 (2017).CAS 
    PubMed 

    Google Scholar  More

  • in

    Immune-mediated competition benefits protective microbes over pathogens in a novel host species

    Alizon S, de Roode JC, Michalakis Y (2013) Multiple infections and the evolution of virulence. Ecol Lett 16(4):556–67PubMed 

    Google Scholar 
    Bian G, Zhou G, Lu P, Xi Z (2013) Replacing a native Wolbachia with a novel strain results in an increase in endosymbiont load and resistance to dengue virus in a mosquito vector. PLoS Negl Trop Dis 7(6):e2250PubMed 
    PubMed Central 

    Google Scholar 
    Bjørnstad ON, Harvill ET (2005) Evolution and emergence of Bordetella in humans. Trends Microbiol 13(8):355–9PubMed 

    Google Scholar 
    Bosch TC (2013) Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu Rev Microbiol 67:499–518CAS 
    PubMed 

    Google Scholar 
    Bull JJ, Turelli M (2013) Wolbachia versus dengue: Evolutionary forecasts. Evol Med Public Health 2013(1):197–207PubMed 
    PubMed Central 

    Google Scholar 
    Cabreiro F, Gems D (2013) Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans. EMBO Mol Med 5(9):1300–10CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chen F, Krasity BC, Peyer SM, Koehler S, Ruby EG, Zhang X et al. (2017) Bactericidal permeability-increasing proteins shape host-microbe interactions. mBio 8:e00040–17CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL (2017) Horizontal Transmission of Intracellular Insect Symbionts via Plants. Front Microbiol 8:2237PubMed 
    PubMed Central 

    Google Scholar 
    Chrostek E, Teixeira L (2015) Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol 13(2):e1002065PubMed 
    PubMed Central 

    Google Scholar 
    Cisani G, Varaldo PE, Grazi G, Soro O (1982) High-level potentiation of lysostaphin anti-staphylococcal activity by lysozyme. Antimicrob Agents Chemother 21(4):531–5CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Clark LC, Hodgkin J (2014) Commensals, probiotics and pathogens in the Caenorhabditis elegans model. Cell Microbiol 16(1):27–38CAS 
    PubMed 

    Google Scholar 
    Coolon JD, Jones KL, Todd TC, Carr BC, Herman MA (2009) Caenorhabditis elegans genomic response to soil bacteria predicts environment-specific genetic effects on life history traits. PLOS Genet 5:e1000503PubMed 
    PubMed Central 

    Google Scholar 
    Dierking K, Yang W, Schulenburg H (2016) Antimicrobial effectors in the nematode Caenorhabditis elegans: an outgroup to the Arthropoda. Philos Trans R Soc Lond B Biol Sci 371:1695
    Google Scholar 
    Dong Y, Manfredini F, Dimopoulos G (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5(5):e1000423PubMed 
    PubMed Central 

    Google Scholar 
    Drew GC, King KC (2022) More or less? The effect of symbiont density in protective mutualisms. Am Nat 199(4):443–54PubMed 

    Google Scholar 
    Ford SA, Kao D, Williams D, King KC (2016) Microbe-mediated host defence drives the evolution of reduced pathogen virulence. Nat Commun 7:13430CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ford SA, King KC (2016) Harnessing the Power of Defensive Microbes: Evolutionary Implications in Nature and Disease Control. PLoS Pathog 12(4):e1005465PubMed 
    PubMed Central 

    Google Scholar 
    Ford SA, King KC (2021) In Vivo Microbial Coevolution Favors Host Protection and Plastic Downregulation of Immunity. Mol Biol Evol 38(4):1330–1338CAS 
    PubMed 

    Google Scholar 
    Frank SA (1996) Models of parasite virulence. Q Rev Biol 71(1):37–78CAS 
    PubMed 

    Google Scholar 
    Félix MA, Braendle C (2010) The natural history of Caenorhabditis elegans. Curr Biol 20(22):R965–9PubMed 

    Google Scholar 
    Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, Murray BE et al. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci USA 98(19):10892–7CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gerardo NM, Parker BJ (2014) Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr Opin Insect Sci 4:8–14PubMed 

    Google Scholar 
    Gravato-Nobre MJ, Hodgkin J (2005) Caenorhabditis elegans as a model for innate immunity to pathogens. Cell Microbiol 7(6):741–51CAS 
    PubMed 

    Google Scholar 
    Habets MG, Rozen DE, Brockhurst MA (2012) Variation in Streptococcus pneumoniae susceptibility to human antimicrobial peptides may mediate intraspecific competition. Proc Biol Sci 279(1743):3803–11CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Heath BD, Butcher RD, Whitfield WG, Hubbard SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9(6):313–6CAS 
    PubMed 

    Google Scholar 
    Heikkilä MP, Saris PE (2003) Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 95(3):471–8PubMed 

    Google Scholar 
    Hoffmann AA, Ross PA, Rašić G (2015) Wolbachia strains for disease control: ecological and evolutionary considerations. Evol Appl 8(8):751–68PubMed 
    PubMed Central 

    Google Scholar 
    Hope IA (1999) C. elegans: a practical approach. Oxford University Press, Oxford
    Google Scholar 
    Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 271(1538):509–15CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jaenike J, Polak M, Fiskin A, Helou M, Minhas M (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3(1):23–5CAS 
    PubMed 

    Google Scholar 
    Kaltenpoth M, Engl T (2014) Defensive microbial symbionts in Hymenoptera. Funct Ecol 28(2):315–27
    Google Scholar 
    King KC (2019) Quick guide: defensive symbionts. Curr Biol 29:R78–R80CAS 
    PubMed 

    Google Scholar 
    King KC, Brockhurst MA, Vasieva O, Paterson S, Betts A, Ford SA et al. (2016) Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J 10(8):1915–24CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kong C, Tan MW, Nathan S (2014) Orthosiphon stamineus protects Caenorhabditis elegans against Staphylococcus aureus infection through immunomodulation. Biol Open 3(7):644–55PubMed 
    PubMed Central 

    Google Scholar 
    Kopylova E, Noé L, Touzet H (2012) SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 14(24):3211–17
    Google Scholar 
    Koziel J, Potempa J (2013) Protease-armed bacteria in the skin. Cell Tissue Res 351:325–37CAS 
    PubMed 

    Google Scholar 
    Lysenko ES, Ratner AJ, Nelson AL, Weiser JN (2005) The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog 1(1):e1PubMed 
    PubMed Central 

    Google Scholar 
    Magalhaes T, Bergren NA, Bennett SL, Borland EM, Hartman DA, Lymperopoulos K et al. (2019) Induction of RNA interference to block Zika virus replication and transmission in the mosquito Aedes aegypti. Insect Biochem Mol Biol 111:103169CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Margolis E, Yates A, Levin BR (2010) The ecology of nasal colonization of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus: the role of competition and interactions with host’s immune response. BMC Microbiol 10:59PubMed 
    PubMed Central 

    Google Scholar 
    Marra A, Hanson MA, Kondo S, Erkosar B, Lemaitre B (2021) Drosophila Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance. mBio 12(4):e0082421CAS 
    PubMed 

    Google Scholar 
    Martinez J, Cogni R, Cao C, Smith S, Illingworth CJ, Jiggins FM (2016) Addicted? Reduced host resistance in populations with defensive symbionts. Proc Biol Sci 283:1833
    Google Scholar 
    Martín-Platero AM, Valdivia E, Ruíz-Rodríguez M, Soler JJ, Martín-Vivaldi M, Maqueda M et al. (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe (Upupa epops). Appl Environ Microbiol 72(6):4245–9PubMed 
    PubMed Central 

    Google Scholar 
    Mason KL, Stepien TA, Blum JE, Holt JF, Labbe NH, Rush JS et al. (2011) From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. MBio 2(3):e00065–11PubMed 
    PubMed Central 

    Google Scholar 
    Matthews AC, Mikonranta L, Raymond B (2019) Shifts along the parasite-mutualist continuum are opposed by fundamental trade-offs. Proc Biol Sci 286(1900):20190236CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    May G, Nelson P (2014) Defensive mutualisms: do microbial interactions within hosts drive the evolution of defensive traits? Funct Ecol 28(2):356–63
    Google Scholar 
    Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA et al. (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479PubMed 
    PubMed Central 

    Google Scholar 
    Mergaert P (2018) Role of antimicrobial peptides in controlling symbiotic bacterial populations. Nat prod Rep. 35(4):336–56CAS 
    PubMed 

    Google Scholar 
    Metcalf CJE, Koskella B (2019) Protective microbiomes can limit the evolution of host pathogen defense. Evol Lett 3:534–43PubMed 
    PubMed Central 

    Google Scholar 
    Montalvo-Katz S, Huang H, Appel MD, Berg M, Shapira M (2013) Association with soil bacteria enhances p38-dependent infection resistance in Caenorhabditis elegans. Infect Immun 81(2):514–20CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139(7):1268–78PubMed 

    Google Scholar 
    O’Neill SL, Ryan PA, Turley AP, Wilson G, Retzki K, Iturbe-Ormaetxe I et al. (2018) Scaled deployment of Wolbachia to protect the community from Aedes transmitted arboviruses. Gates Open Res 2:36PubMed 

    Google Scholar 
    Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc Biol Sci 275(1632):293–9PubMed 

    Google Scholar 
    Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world ‘96 advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28(2):341–55
    Google Scholar 
    Pan X, Pike A, Joshi D, Bian G, McFadden MJ, Lu P et al. (2018) The bacterium Wolbachia exploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquito Aedes aegypti. ISME J 12(1):277–88CAS 
    PubMed 

    Google Scholar 
    Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26(5):242–8PubMed 

    Google Scholar 
    Pastar I, O’Neill K, Padula L, Head CR, Burgess JL, Chen V et al. (2020) Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin. Front Immunol 11:550946CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pees B, Kloock A, Nakad R, Barbosa C, Dierking K (2017) Enhanced behavioral immune defenses in a C. elegans C-type lectin-like domain gene mutant. Dev Comp Immunol 74:237–42CAS 
    PubMed 

    Google Scholar 
    Peleg AY, Tampakakis E, Fuchs BB, Eliopoulos GM, Moellering RC, Mylonakis E (2008) Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc Natl Acad Sci USA 105(38):14585–90CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Petersen C, Dirksen P, Schulenburg H (2015) Why we need more ecology for genetic models such as C. elegans. Trends Genet 31(3):120–7CAS 
    PubMed 

    Google Scholar 
    Pimentel H, Bray NL, Puente S, Melsted P, Pachter L (2017) Differential analysis of RNA-seq incorporating quantification uncertainty. Nat Methods 14(7):687–90CAS 
    PubMed 

    Google Scholar 
    Portal-Celhay C, Blaser MJ (2012) Competition and resilience between founder and introduced bacteria in the Caenorhabditis elegans gut. Infect Immun 80(3):1288–99CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Raberg L, de Roode JC, Bell AS, Stamou P, Gray D, Read AF (2006) The role of immune-mediated apparent competition in genetically diverse malaria infections. Am Nat 168(1):41–53PubMed 

    Google Scholar 
    Rafaluk-Mohr C, Ashby B, Dahan DA, King KC (2018) Mutual fitness benefits arise during coevolution in a nematode-defensive microbe model. Evol Lett 2(3):246–56PubMed 
    PubMed Central 

    Google Scholar 
    Ragland SA, Criss AK (2017) From bacterial killing to immune modulation: Recent insights into the functions of lysozyme. PLoS Pathog 13(9):e1006512PubMed 
    PubMed Central 

    Google Scholar 
    Rancès E, Ye YH, Woolfit M, McGraw EA, O’Neill SL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8(2):e1002548PubMed 
    PubMed Central 

    Google Scholar 
    Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H et al. (2019) g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res 47(W1):W191–W198CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Raymann K, Shaffer Z, Moran NA (2017) Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol 15(3):e2001861PubMed 
    PubMed Central 

    Google Scholar 
    Rossouw W, Korsten L (2017) Cultivable microbiome of fresh white button mushrooms. Lett Appl Microbiol 64(2):164–70CAS 
    PubMed 

    Google Scholar 
    Russell JA, Moran NA (2005) Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 71(12):7987–94CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ryu H, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW et al. (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319:777–82CAS 
    PubMed 

    Google Scholar 
    Sellegounder D, Liu Y, Wibisono P, Chen CH, Leap D, Sun J (2019) Neuronal GPCR NPR-8 regulates C. elegans defense against pathogen infection. Sci Adv 5(11):eaaw4717CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sifri CD, Begun J, Ausubel FM, Calderwood SB (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71(4):2208–17CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Singh UB, Malviya D, Wasiullah, Singh S, Pradhan JK, Singh BP et al. (2016) Bio-protective microbial agents from rhizosphere eco-systems trigger plant defense responses provide protection against sheath blight disease in rice (Oryza sativa L.). Microbiol Res 192:300–12CAS 
    PubMed 

    Google Scholar 
    Trevelline BK, Fontaine SS, Hartup BK, Kohl KD (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc Biol Sci 286(1895):20182448PubMed 
    PubMed Central 

    Google Scholar 
    Ulrich Y, Schmid-Hempel P (2012) Host modulation of parasite competition in multiple infections. Proc Biol Sci 279(1740):2982–9PubMed 
    PubMed Central 

    Google Scholar 
    Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O et al. (2011) The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334(653):255–8CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Varahan S, Iyer VS, Moore WT, Hancock LE (2013) Eep confers lysozyme resistance to enterococcus faecalis via the activation of the extracytoplasmic function sigma factor SigV. J Bacteriol 195(14):3125–34CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Visvikis O, Ihuegbu N, Labed SA, Luhachack LG, Alves AF, Wollenberg AC et al. (2014) Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes. Immunity 40(6):896–909CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vorburger C, Ganesanandamoorthy P, Kwiatkowski M (2013) Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecol Evol 3(3):706–13PubMed 
    PubMed Central 

    Google Scholar 
    Wang S, Dos-Santos ALA, Huang W, Liu KC, Oshaghi MA, Wei G et al. (2017) Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria. Science 357(6358):1399–1402CAS 
    PubMed 

    Google Scholar 
    Wilke AB, Marrelli MT (2015) Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 8:342PubMed 
    PubMed Central 

    Google Scholar 
    Wong D, Bazopoulou D, Pujol N, Tavernarakis J, Ewbank J (2007) Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol 8:R194PubMed 
    PubMed Central 

    Google Scholar  More