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    Modeling Posidonia oceanica shoot density and rhizome primary production

    Study area and environmental variables
    The data set used in this study included 192 sites in which lepidochronological data and shoot density were acquired between 1994 and 2003. Clearly, the rhizome primary production of P. oceanica was estimated as defined by Pergent-Martini et al.12.
    The spatial coverage of the data set was not uniform across the Italian Seas. In fact, the sampling sites were mainly concentrated in five Italian regions, i.e. Liguria, Tuscany, Lazio, Basilicata and Apulia (Fig. 1).
    Figure 1

    Sampling sites from which field data and indirect measurements have been collected (red circles). Data about several sampling stations are available at each site (N = 6 to 15).

    Full size image

    The environmental variables were all acquired from maps and other related information sources (Table 1), according to the main aim of the study. A detailed explanation of these variables and of the methodology for their acquisition is given in the supplementary materials.
    Table 1 Environmental factors used as predictive variables for developing P. oceanica models.
    Full size table

    Since these environmental factors were used as predictive variables in the modeling procedure, their selection was based on the ecological nature of the modelled processes, taking into account their influence on the latter. For instance, it is well known that depth plays a crucial role in determining the properties of P. oceanica meadows, such as density and productivity, as it is strictly related to other fundamental environmental factors, e.g. light. Therefore, both depth and gradient were considered as predictive variables, as well as the profile of the isobaths, described as either linear, convex or concave. The presence of sources of disturbance, such as sewage discharge or similar pollution, was also taken into account, as an increase in turbidity following an excessive enrichment from nutrient inputs might entail a reduction of water transparency and light penetration, which in turn can alter the ecological proprieties of a P. oceanica meadow. As for the sea floor typologies, i.e. sand, rock and matte, sources of disturbance have been represented as binary variables because of the intention of using only indirect methods for data acquisition, e.g. maps. Clearly, with such types of data source it was possible to perform, with good confidence, only a qualitative assessment. A quantitative coding of those predictive variables would indeed require expensive and time-consuming efforts for field activities, leading to a major drawback of the proposed approach.
    The data set was partitioned into two subsets, i.e. training and test sets, for modeling purposes. Data partitioning represents a critical step in modeling, whose aim is obtaining two subsets that are as much as possible independent from each other, while simultaneously representative of the modelled problem, in order to avoid modeling artifacts and to ensure the applicability of the resulting models18.
    Accordingly, the partitioning was not based on random selection of the data, rather the subsets were obtained on the basis of the following approach. The data were stratified according to depth, i.e. they were sorted on the basis of their depth and assigned to one of the following bathymetric classes, i.e.[0,5] m, (5,10] m, (10,15] m, (15,20] m, (20,25] m, (25,35] m. These classes comprised 16.67%, 23.96%, 27.08%, 17.71%, 9.90% and 4.69% of the total number of records, respectively. Subsequently, within each bathymetric class, about 70% of the data, i.e. n = 136, were assigned to the training set, while the remaining ones, i.e. n = 56, to the test set. While the former subset comprising the majority of the data was used for the training procedure of the Machine Learning algorithm, i.e. Random Forest19, the test subset was only used a posteriori to evaluate model performance.
    The rationale behind the aforementioned approach is that the depth has a paramount ecological role in regulating both P. oceanica shoot density and rhizome primary production, as previously noted. In fact, a wide range of environmental conditions are related to depth, such as light, water movement and sedimentation flows, which in turn strictly affected the structure, the functioning and the ecological condition of P. oceanica meadows. Therefore, using the abovementioned strategy in the data allocation, the inherent variability of the ecological patterns was properly distributed among the subsets, thus ensuring the possibility of obtaining ecologically sound models.
    Random Forest
    The Random Forest (RF) is a Machine Learning technique which fits an ensemble of Classification Trees and combines their predictions into a single model19.
    RF has proven effective in a wide range of applications as it is able to address, for example, both regression and classification problems20, to perform cluster analysis and missing values imputation21,22.
    RF has been used for predicting current and potential future spatial distribution of plant species23, as well as for estimating the marine biodiversity on the basis of the sea floor hardness24. RF has been also applied in ecological applications as a classification tool for the assessment of the vulnerability of P. oceanica meadows over a large spatial scale25, and for land cover classification using remote sensing data26,27.
    This method relies upon one of the main features of Machine Learning methods, namely that an ensemble of ‘weak learners’ usually outperforms a single ‘strong learner’19. As a matter of fact, each Classification Tree in the forest represents a weak learner, i.e. a single model, trained on a partly independent data subset, i.e. on a bootstrap sample. Each Classification Tree provides predictions based on the data contained in its bootstrap sample, and many trees are combined into an ensemble model, i.e. into a ‘forest’. The overall output of a RF is obtained by averaging the outcomes of all the trees for regression applications, while it is based on majority voting for classification problems.
    The diversity of the trees in the forest is ensured by the use of random subsets of data for the tree-building process, i.e. bootstrap samples, as well as by making a random subset of predictive variables available for the tree splitting procedure. These features allow the RF to reduce the correlation among its Classification Trees, while keeping the variance relatively small, thus leading to a more robust model19.
    The selection of a random subset of predictive variables at each split ensures maintaining a certain level of randomness during the tree construction process28, and is necessary for the proper functioning of RF. As a matter of fact, the size of the random subset of predictive variables available for the tree splitting procedure represents a tuning parameter, defined as mtry. The latter together with the minimum number of records to be contained in each leaf, called nodesize, are the main tuning parameters that deeply affect RF performance21,29.
    In its original work, Breiman19 suggested to set the mtry value equal to p/3 for regression applications, being p is the total number of predictors, and tuning it from half to twice its original value. On the other hand, nodesize and ntree (the latter parameter is the total number of Classification Trees in the forest) are more related to the generalization ability of the RF, and to the overall complexity of the model. Growing a very large forest, e.g. ntree  > 500, or growing the trees to achieve a high degree of purity at their leaves, e.g. nodesize  More

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    Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

    Main features of mycorrhizal genomes
    We compared 62 draft genomes from mycorrhizal fungi, including 29 newly released genomes, and predicted 9344–31,291 protein-coding genes per species (see “Methods”, Supplementary Information and Supplementary Data 1). This set includes new genomes from the early diverging fungal clades in the Russulales, Thelephorales, Phallomycetidae, and Cantharellales (Basidiomycota), and Helotiales and Pezizales (Ascomycota). We combined these mycorrhizal fungal genomes with 73 fungal genomes from wood decayers, soil/litter saprotrophs, and root endophytes (Fig. 1 and Supplementary Data 2). There was little variation in the completeness of the gene repertoires, based on Benchmarking Universal Single-Copy Orthologs (BUSCO) analysis (coefficient of variation, c.v. = 7.98), despite variation in assembly contiguity (Fig. 1). Genome size varied greatly within each phylum, with genomes of mycorrhizal fungi being larger than those of saprotrophic species (Figs. 1 and 2, and Supplementary Data 2; P  More

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    Drivers of wildfire carbon emissions

    1.
    Cohen, J. et al. Nat. Geosci. 7, 627–637 (2014).
    CAS  Article  Google Scholar 
    2.
    Xiao, J. & Zhuang, Q. Environ. Res. Lett. 2, 044003 (2007).
    Article  Google Scholar 

    3.
    Veraverbeke, S. et al. Nat. Clim. Change 7, 529–534 (2017).
    Article  Google Scholar 

    4.
    Balshi, M. S. et al. J. Geophys. Res. 112, G02029 (2007).
    Article  Google Scholar 

    5.
    Kelly, R., Genet, H., McGuire, A. D. & Hu, F. S. Nat. Clim. Change 6, 79–82 (2016).
    CAS  Article  Google Scholar 

    6.
    Walker, X. J. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-020-00920-8 (2020).

    7.
    Harden, J. W. et al. Glob. Chang. Biol. 6, 174–184 (2000).
    Article  Google Scholar 

    8.
    Harmon, M. E. J. For. 99, 24–29 (2001).
    Google Scholar 

    9.
    Loehman, R. A., Reinhardt, E. & Riley, K. L. For. Ecol. Manag. 317, 9–19 (2014).
    Article  Google Scholar 

    10.
    Fauria, M. M. & Johnson, E. A. J. Geophys. Res.-Biogeo. 111, G04008 (2006).
    Google Scholar 

    11.
    Holden, Z. A. & Jolly, W. M. For. Ecol. Manag. 262, 2133–2141 (2011).
    Article  Google Scholar 

    12.
    Johnstone, J. F., Hollingsworth, T. N., Chapin, F. S. & Mack, M. C. Glob. Chang. Biol. 16, 1281–1295 (2010).
    Article  Google Scholar  More

  • in

    Individual species provide multifaceted contributions to the stability of ecosystems

    1.
    Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).
    CAS  Article  Google Scholar 
    2.
    Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).
    CAS  PubMed  Article  Google Scholar 

    3.
    Naeem, S., Duffy, J. E. & Zavaleta, E. The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012).
    CAS  PubMed  Article  Google Scholar 

    4.
    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).
    CAS  PubMed  Article  Google Scholar 

    5.
    Pimm, S. L. et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).
    CAS  PubMed  Article  Google Scholar 

    6.
    Ceballos, G., Ehrlich, P. R. & Raven, P. H. Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. Proc. Natl Acad. Sci. USA 117, 13596–13602 (2020).
    CAS  PubMed  Article  Google Scholar 

    7.
    Loreau, M. et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).
    CAS  Article  Google Scholar 

    8.
    Lefcheck, J. S. et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6, 6936 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Donohue, I. et al. On the dimensionality of ecological stability. Ecol. Lett. 16, 421–429 (2013).
    PubMed  Article  Google Scholar 

    10.
    Macdougall, A. S., McCann, K. S., Gellner, G. & Turkington, R. Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494, 86–89 (2013).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    11.
    Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    12.
    Kéfi, S. et al. Advancing our understanding of ecological stability. Ecol. Lett. 22, 1349–1356 (2019).
    PubMed  Article  PubMed Central  Google Scholar 

    13.
    Donohue, I. et al. Loss of predator species, not intermediate consumers, triggers rapid and dramatic extinction cascades. Glob. Change Biol. 23, 2962–2972 (2017).
    Article  Google Scholar 

    14.
    Sanders, D., Thébault, E., Kehoe, R. & Frank van Veen, F. J. Trophic redundancy reduces vulnerability to extinction cascades. Proc. Natl Acad. Sci. USA 115, 2419–2424 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    O’Connor, N. E., Bracken, M. E., Crowe, T. P. & Donohue, I. Nutrient enrichment alters the consequences of species loss. J. Ecol. 103, 862–870 (2015).
    Article  Google Scholar 

    16.
    O’Connor, N. E. & Donohue, I. Environmental context determines multi-trophic effects of consumer species loss. Glob. Change Biol. 19, 431–440 (2013).
    Article  Google Scholar 

    17.
    O’Connor, N. E. & Crowe, T. P. Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species. Ecology 86, 1783–1796 (2005).
    Article  Google Scholar 

    18.
    Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188–190 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    19.
    Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    20.
    Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).
    Article  Google Scholar 

    21.
    O’Gorman, E. J. & Emmerson, M. C. Perturbations to trophic interactions and the stability of complex food webs. Proc. Natl Acad. Sci. USA 106, 13393–13398 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    22.
    May, R. M. Will a large complex system be stable? Nature 238, 413–414 (1972).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    23.
    May, R. M. Stability and Complexity in Model Ecosystems (Princeton Univ. Press, 1973).

    24.
    McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).
    CAS  Article  Google Scholar 

    25.
    Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    26.
    Allesina, S. & Tang, S. Stability criteria for complex ecosystems. Nature 483, 205–208 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    27.
    Loreau, M. & de Mazancourt, C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    28.
    Pennekamp, F. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    29.
    Paine, R. T. Food web complexity and species diversity. Am. Nat. 100, 65–75 (1966).
    Article  Google Scholar 

    30.
    Terborgh, J. et al. Ecological meltdown in predator-free forest fragments. Science 294, 1923–1927 (2001).
    CAS  PubMed  Article  Google Scholar 

    31.
    Díaz, S., Symstad, A. J., Chapin, F. S., Wardle, D. A. & Huenneke, L. F. Functional diversity revealed by removal experiments. Trends Ecol. Evol. 18, 140–146 (2003).
    Article  Google Scholar 

    32.
    Borrvall, C. & Ebenman, B. Early onset of secondary extinctions in ecological communities following the loss of top predators. Ecol. Lett. 9, 435–442 (2006).
    PubMed  Article  Google Scholar 

    33.
    Petchey, O. L., Eklöf, A., Borrvall, C. & Ebenman, B. Trophically unique species are vulnerable to cascading extinction. Am. Nat. 171, 568–579 (2008).
    PubMed  Article  Google Scholar 

    34.
    Kardol, P., Fanin, N. & Wardle, D. A. Long-term effects of species loss on community properties across contrasting ecosystems. Nature 557, 710–713 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Donohue, I. et al. Navigating the complexity of ecological stability. Ecol. Lett. 19, 1172–1185 (2016).
    PubMed  Article  Google Scholar 

    36.
    Pimm, S. L. The complexity and stability of ecosystems. Nature 307, 321–326 (1984).
    Article  Google Scholar 

    37.
    de Mazancourt, C. et al. Predicting ecosystem stability from community composition and biodiversity. Ecol. Lett. 16, 617–625 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    38.
    Neubert, M. & Caswell, H. Alternatives to resilience for measuring the responses of ecological systems to perturbations. Ecology 78, 653–665 (2012).
    Article  Google Scholar 

    39.
    Arnoldi, J. F., Loreau, M. & Haegeman, B. Resilience, reactivity and variability: a mathematical comparison of ecological stability measures. J. Theor. Biol. 389, 47–59 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    40.
    Naeem, S. Advancing realism in biodiversity research. Trends Ecol. Evol. 23, 414–416 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    41.
    Mrowicki, R. J., Maggs, C. A. & O’Connor, N. E. Consistent effects of consumer species loss across different habitats. Oikos 124, 1555–1563 (2015).
    Article  Google Scholar 

    42.
    Hillebrand, H. et al. Decomposing multiple dimensions of stability in global change experiments. Ecol. Lett. 21, 21–30 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    43.
    Hillebrand, H. & Kunze, C. Meta-analysis on pulse disturbances reveals differences in functional and compositional recovery across ecosystems. Ecol. Lett. 23, 575–585 (2020).
    PubMed  Article  PubMed Central  Google Scholar 

    44.
    Hoover, D. L., Knapp, A. K. & Smith, M. D. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95, 2646–2656 (2014).
    Article  Google Scholar 

    45.
    Johns, K. A., Osborne, K. O. & Logan, M. Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33, 553–563 (2014).
    Article  Google Scholar 

    46.
    Gülzow, N., Muijsers, F., Ptacnik, R. & Hillebrand, H. Functional and structural stability are linked in phytoplankton metacommunities of different connectivity. Ecography 40, 719–732 (2016).
    Article  Google Scholar 

    47.
    Garnier, A., Pennekamp, F., Lemoine, M. & Petchey, O. L. Temporal scale dependent interactions between multiple environmental disturbances in microcosm ecosystems. Glob. Change Biol. 23, 5237–5248 (2017).
    Article  Google Scholar 

    48.
    Yang, Q., Fowler, M. S., Jackson, A. L. & Donohue, I. The predictability of ecological stability in a noisy world. Nat. Ecol. Evol. 3, 251–259 (2019).
    PubMed  Article  Google Scholar 

    49.
    Pimm, S. L., Donohue, I., Montoya, J. M. & Loreau, M. Measuring resilience is essential to understand it. Nat. Sustain. 2, 895–897 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    50.
    Cardinale, B. J. et al. Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc. Natl Acad. Sci. USA 104, 18123–18128 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    51.
    Mrowicki, R. J., O’Connor, N. E. & Donohue, I. Temporal variability of a single population can determine the vulnerability of communities to perturbations. J. Ecol. 104, 887–897 (2016).
    Article  Google Scholar 

    52.
    Griffin, J. N. et al. Spatial heterogeneity increases the importance of species richness for an ecosystem process. Oikos 118, 1335–1342 (2009).
    Article  Google Scholar 

    53.
    Emmerson, M. C., Solan, M., Emes, C., Paterson, D. M. & Raffaelli, D. Consistent patterns and the idiosyncstatic effects of biodiversity in marine ecosystems. Nature 411, 73–77 (2001).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    54.
    Baert, J. M., Eisenhauer, N., Janssen, C. R. & de Laender, F. Biodiversity effects on ecosystem functioning respond unimodally to environmental stress. Ecol. Lett. 21, 1191–1199 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    55.
    Vye, S., Dick, J. T. A., Emmerson, M. C. & O’Connor, N. E. Cumulative effects of an invasive species and nutrient enrichment on rock pool communities. Mar. Ecol. Prog. Ser. 594, 39–50 (2018).
    CAS  Article  Google Scholar 

    56.
    Thiébaut, E. et al. Changes in a benthic system exposed to multiple stressors: a 40-year time-series in the English Channel. PeerJ Prepr. 6, e26745v1 (2018).
    Google Scholar 

    57.
    Houbin, C., Thiébaut, E. & Hoebeke, M. Study of specific diversity of macrobenthic communities in the ‘Pierre Noire’ site: Dataset/Sampling event (Station Biologique de Roscoff – Sorbonne Université-CNRS, 2018); https://doi.org/10.21411/kfms-pq29

    58.
    O’Connor, N. E., Donohue, I., Crowe, T. P. & Emmerson, M. C. Importance of consumers on exposed and sheltered rocky shores. Mar. Ecol. Prog. Ser. 443, 65–75 (2011).
    Article  Google Scholar 

    59.
    O’Connor, N. E., Emmerson, M. C., Crowe, T. P. & Donohue, I. Distinguishing between direct and indirect effects of predators in complex ecosystems. J. Anim. Ecol. 82, 438–448 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    60.
    Byrnes, J. E. & Stachowicz, J. J. The consequences of consumer diversity loss: different answers from different experimental designs. Ecology 90, 2879–2888 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    61.
    Firth, L. B. & Crowe, T. P. Competition and habitat suitability: small-scale segregation underpins large-scale coexistence of key species on temperate rocky shores. Oecologia 162, 163–174 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    62.
    Crowe, T. P. et al. Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8, e66238 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Benedetti-Cecchi, L., Tamburello, L., Maggi, E. & Bulleri, F. Experimental perturbations modify the performance of early warning indicators of regime shift. Curr. Biol. 25, 1867–1872 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    64.
    Griffin, J. N. et al. Consumer effects on ecosystem functioning in rock pools: roles of species richness and composition. Mar. Ecol. Prog. Ser. 420, 45–56 (2010).
    Article  Google Scholar 

    65.
    Griffin, J. N., Méndez, V., Johnson, A. F., Jenkins, S. R. & Foggo, A. Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118, 37–44 (2009).
    Article  Google Scholar 

    66.
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 

    67.
    McArdle, B. H. & Anderson, M. J. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297 (2001).
    Article  Google Scholar 

    68.
    Clarke, K. R. Non‐parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).
    Article  Google Scholar 

    69.
    White, L., O’Connor, N., Yang, Q., Emmerson, M. & Donohue, I. Individual species provide multifaceted contributions to the stability of ecosystems_Dataset (Version 1). Zenodo https://doi.org/10.5281/zenodo.3974299 (2020).

    70.
    Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).
    CAS  PubMed  Article  Google Scholar 

    71.
    Whittaker, F. Evolution and measurement of species diversity. Taxon 21, 213–251 (1972).
    Article  Google Scholar 

    72.
    Lande, R. Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76, 5–13 (1996).
    Article  Google Scholar 

    73.
    Olden, J. D., Poff, N. L. R., Douglas, M. R., Douglas, M. E. & Fausch, K. D. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol. Evol. 19, 18–24 (2004).
    PubMed  Article  Google Scholar 

    74.
    France, K. E. & Duffy, J. E. Diversity and dispersal interactively affect predictability of ecosystem function. Nature 441, 1139–1143 (2006).
    CAS  PubMed  Article  Google Scholar 

    75.
    Wang, S. et al. An invariability-area relationship sheds new light on the spatial scaling of ecological stability. Nat. Commun. 8, 15211 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    76.
    Wang, S. & Loreau, M. Biodiversity and ecosystem stability across scales in metacommunities. Ecol. Lett. 19, 510–518 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    77.
    Gravel, D., Massol, F. & Leibold, M. A. Stability and complexity in model meta-ecosystems. Nat. Commun. 7, 12457 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar  More

  • in

    Increasing decision relevance of ecosystem service science

    1.
    IPBES Summary for Policymakers. In Global Assessment Report on Biodiversity and Ecosystem Services (eds Díaz, S. et al.) (IPBES Secretariat, 2019).
    2.
    Schaefer, M., Goldman, E., Bartuska, A. M., Sutton-Grier, A. & Lubchenco, J. Nature as capital: advancing and incorporating ecosystem services in United States federal policies and programs. Proc. Natl Acad. Sci. USA 112, 7383–7389 (2015).
    CAS  Article  Google Scholar 

    3.
    Mastrángelo, M. E. et al. Key knowledge gaps to achieve global sustainability goals. Nat. Sustain. https://doi.org/10.1038/s41893-019-0412-1 (2019).

    4.
    Olander, L. et al. So you want your research to be relevant? Building the bridge between ecosystem services research and practice. Ecosyst. Serv. 26, 170–182 (2017).
    Article  Google Scholar 

    5.
    Polasky, S., Tallis, H. & Reyers, B. Setting the bar: standards for ecosystem services. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1406490112 (2015).

    6.
    Rieb, J. et al. When, where and how nature matters for ecosystem services: challenges for the next generation of ecosystem service models. BioScience 67, 820–833 (2017).
    Article  Google Scholar 

    7.
    Natural Capital Protocol (Natural Capital Coalition, 2016).

    8.
    Mandle, L., Ouyang, Z., Salzman, J. & Daily, G. C. Green Growth that Works: Natural Capital Policy and Finance Mechanisms from the World (Island Press, 2019).

    9.
    Transforming our World: The 2030 Agenda for Sustainable Development (UN, 2015).

    10.
    Díaz, S. et al. Assessing nature’s contributions to people: recognizing culture, and diverse sources of knowledge, can improve assessments. Science 359, 270–272 (2018).
    Article  Google Scholar 

    11.
    Arkema, K. K. et al. Embedding ecosystem services in coastal planning leads to better outcomes for people and nature. Proc. Natl Acad. Sci. USA 112, 7390–7395 (2015).
    CAS  Article  Google Scholar 

    12.
    Van Wensem, J. et al. Identifying and assessing the application of ecosystem services approaches in environmental policies and decision making. Integr. Environ. Assess. Manag. 13, 41–51 (2017).
    Article  Google Scholar 

    13.
    Ricketts, T. H. & Lonsdorf, E. Mapping the margin: comparing marginal values of tropical forest remnants for pollination services. Ecol. Appl. 23, 1113–1123 (2013).
    Article  Google Scholar 

    14.
    Mandle, L., Tallis, H., Sotomayor, L. & Vogl, A. L. Who loses? Tracking ecosystem service redistribution from road development and mitigation in the Peruvian Amazon. Front. Ecol. Environ. 13, 309–315 (2015).
    Article  Google Scholar 

    15.
    Wieland, R., Ravensbergen, S., Gregr, E. J., Satterfield, T. & Chan, K. M. A. Debunking trickle-down ecosystem services: the fallacy of omnipotent, homogeneous beneficiaries. Ecol. Econ. 121, 175–180 (2016).
    Article  Google Scholar 

    16.
    Polasky, S. & Segerson, K. Integrating ecology and economics in the study of ecosystem services: some lessons learned. Annu. Rev. Resour. Econ. 1, 409–434 (2009).
    Article  Google Scholar 

    17.
    Keeler, B. L. et al. Linking water quality and well-being for improved assessment and valuation of ecosystem services. Proc. Natl Acad. Sci. USA 109, 18619–18624 (2012).
    CAS  Article  Google Scholar 

    18.
    Vogl, A. L. et al. Valuing investments in sustainable land management in the Upper Tana River basin, Kenya. J. Environ. Manag. 195, 78–91 (2017).
    Article  Google Scholar 

    19.
    Arkema, K., Guannel, G. & Verutes, G. Coastal habitats shield people and property from sea-level rise and storms. Nat. Clim. Change 3, 913–918 (2013).
    Article  Google Scholar 

    20.
    Plummer, M. L. Assessing benefit transfer for the valuation of ecosystem services. Front. Ecol. Environ. 7, 38–45 (2009).
    Article  Google Scholar 

    21.
    Tallis, H., Polasky, S., Lozano, J. S. & Wolny, S. in Inclusive Wealth Report 2012: Measuring Progress Toward Sustainability 195–214 (Cambridge Univ. Press, 2012).

    22.
    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change https://doi.org/10.1016/j.gloenvcha.2014.04.002 (2014).

    23.
    Granek, E. F. et al. Ecosystem services as a common language for coastal ecosystem-based management. Conserv. Biol. 24, 207–216 (2010).
    Article  Google Scholar 

    24.
    Ruckelshaus, M. et al. Notes from the field: lessons learned from using ecosystem service approaches to inform real-world decisions. Ecol. Econ. https://doi.org/10.1016/j.ecolecon.2013.07.009 (2013).

    25.
    Ellis, A. M., Myers, S. S. & Ricketts, T. H. Do pollinators contribute to nutritional health? PLoS ONE 10, e114805 (2015).
    Article  Google Scholar 

    26.
    Olsson, P., Folke, C. & Hughes, T. P. Navigating the Transition to Ecosystem-Based Management of the Great Barrier Reef, Australia. Proc. Natl Acad. Sci. USA 105, 9489–9494 (2008).
    CAS  Article  Google Scholar 

    27.
    Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).
    CAS  Article  Google Scholar 

    28.
    SEEA Experimental Ecosystem Accounting Revision (System of Environmental Economic Accounting, 2020); https://go.nature.com/2sqGqFn

    29.
    Aburto-Oropeza, O. et al. Mangroves in the Gulf of California increase fishery yields. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.0804601105 (2008).

    30.
    Keeler, B. L. et al. The social costs of nitrogen. Sci. Adv. 2, e1600219 (2016).
    Article  Google Scholar 

    31.
    Kenter, J. O. et al. What are shared and social values of ecosystems? Ecol. Econ. 111, 86–99 (2015).
    Article  Google Scholar 

    32.
    Pascual, U. et al. Valuing nature’s contributions to people: the IPBES approach. Curr. Opin. Environ. Sustain. 26–27, 7–16 (2017).
    Article  Google Scholar 

    33.
    Samberg, L. H., Gerber, J. S., Ramankutty, N., Herrero, M. & West, P. C. Subnational distribution of average farm size and smallholder contributions to global food production. Environ. Res. Lett. 11, 124010 (2016).
    Article  Google Scholar 

    34.
    Jean, N. et al. Combining satellite imagery and machine learning to predict poverty. Science 353, 790–794 (2016).
    CAS  Article  Google Scholar 

    35.
    Wolff, S., Schulp, C. J. E. & Verburg, P. H. Mapping ecosystem services demand: a review of current research and future perspectives. Ecol. Indic. 55, 159–171 (2015).
    Article  Google Scholar 

    36.
    Dawson, N. & Martin, A. Assessing the contribution of ecosystem services to human wellbeing: a disaggregated study in western Rwanda. Ecol. Econ. 117, 62–72 (2015).
    Article  Google Scholar 

    37.
    Daw, T., Brown, K., Rosendo, S. & Pomeroy, R. Applying the ecosystem services concept to poverty alleviation: the need to disaggregate human well-being. Environ. Conserv. 38, 370–379 (2011).
    Article  Google Scholar 

    38.
    Ruhl, J. B. & Salzman, J. The effects of wetland mitigation banking on people. Natl Wetl. Newsl. 28, 7–13 (2006).
    Google Scholar 

    39.
    Kabisch, N. & Haase, D. Green justice or just green? Provision of urban green spaces in Berlin, Germany. Landsc. Urban Plan. 122, 129–139 (2014).
    Article  Google Scholar 

    40.
    Farley, K. A. & Bremer, L. L. ‘Water Is Life’: local perceptions of páramo grasslands and land management strategies associated with payment for ecosystem services. Ann. Am. Assoc. Geogr. 107, 371–381 (2017).
    Google Scholar 

    41.
    Pascual, U. et al. Social equity matters in payments for ecosystem services. BioScience 64, 1027–1036 (2014).
    Article  Google Scholar 

    42.
    Mastrangelo, M. E. & Laterra, P. From biophysical to social-ecological trade-offs: integrating biodiversity conservation and agricultural production in the Argentine Dry Chaco. Ecol. Soc. 20, 20 (2015).
    Article  Google Scholar 

    43.
    Guerry, A. D. et al. Natural capital and ecosystem services informing decisions: from promise to practice. Proc. Natl Acad. Sci. USA 112, 7348–7355 (2015).
    CAS  Article  Google Scholar 

    44.
    Rieb, J. T. et al. When, where, and how nature matters for ecosystem services: challenges for the next generation of ecosystem service models. BioScience 67, 820–833 (2017).
    Article  Google Scholar 

    45.
    Villa, F., Bagstad, K. J., Voigt, B., Johnson, G. W. & Portela, R. A methodology for adaptable and robust ecosystem services assessment. PLoS ONE 9, e91001 (2014).
    Article  Google Scholar 

    46.
    Díaz, S. et al. Assessing nature’s contributions to people. Science 359, 270–272 (2018).
    Article  Google Scholar 

    47.
    Millennium Ecosystem Assessment Ecosystems and Human Well-being: A Framework for Assessment (Island Press, 2003).

    48.
    Fleiss, J. L. Measuring nominal scale agreement among many raters. Psychol. Bull. 76, 378–382 (1971).
    Article  Google Scholar 

    49.
    Gamer, M., Lemon, J., Fellows, I. & Singh, P. irr: Various Coefficients of Interrater Reliability and Agreement (2012).

    50.
    Landis, J. R. & Koch, G. G. The measurement of observer agreement for categorical data. Biometrics 33, 159–174 (1977).
    CAS  Article  Google Scholar 

    51.
    Tallis, H. et al. A global system for monitoring ecosystem service change. BioScience 62, 977–986 (2012).
    Article  Google Scholar 

    52.
    Daily, G. C. et al. Ecosystem services in decision making: time to deliver. Front. Ecol. Environ. 7, 21–28 (2009).
    Article  Google Scholar  More

  • in

    Size-specific recolonization success by coral-dwelling damselfishes moderates resilience to habitat loss

    1.
    Fahrig, L. Effects of habitat fragmentation on biodiversity. Ann. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).
    Article  Google Scholar 
    2.
    Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    3.
    Nee, S. & May, R. M. Dynamics of metapopulations: Habitat destruction and competitive coexistence. J. Anim. Ecol. 1, 37–40 (1992).
    Article  Google Scholar 

    4.
    Petit, S., Moilanen, A., Hanski, I. & Baguette, M. Metapopulation dynamics of the bog fritillary butterfly: Movements between habitat patches. Oikos 292, 491–500 (2001).
    Article  Google Scholar 

    5.
    Munday, P. L. Does habitat availability determine geographical-scale abundances of coral-dwelling fishes?. Coral Reefs 21, 105–116 (2002).
    ADS  Article  Google Scholar 

    6.
    Wong, M. Y., Fauvelot, C., Planes, S. & Buston, P. M. Discrete and continuous reproductive tactics in a hermaphroditic society. Anim. Behav. 84, 897–906 (2012).
    Article  Google Scholar 

    7.
    Chase, T. J., Pratchett, M. S., Walker, S. P. & Hoogenboom, M. O. Small-scale environmental variation influences whether coral-dwelling fish promote or impede coral growth. Oecologia 176, 1009–1022 (2014).
    ADS  CAS  PubMed  Article  Google Scholar 

    8.
    Kuwamura, T., Yogo, Y. & Nakashima, Y. Population dynamics of goby Paragobiodon echinocephalus and host coral Stylophora pistillata. Mar. Ecol. Prog. Ser. 6, 17–23 (1994).
    ADS  Article  Google Scholar 

    9.
    Holbrook, S. J., Forrester, G. E. & Schmitt, R. J. Spatial patterns in abundance of a damselfish reflect availability of suitable habitat. Oecologia 122, 109–120 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    10.
    Boström-Einarsson, L., Bonin, M. C., Munday, P. L. & Jones, G. P. Strong intraspecific competition and habitat selectivity influence abundance of a coral-dwelling damselfish. J. Exp. Mar. Biol. Ecol. 448, 85–92 (2013).
    Article  Google Scholar 

    11.
    Munday, P. L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Change Biol. 10, 1642–1647 (2004).
    ADS  Article  Google Scholar 

    12.
    Wilson, S. K. et al. Habitat utilization by coral reef fish: Implications for specialists vs. generalists in a changing environment. J. Anim. Ecol. 77, 220–228 (2008).
    PubMed  Article  Google Scholar 

    13.
    Emslie, M. J., Cheal, A. J. & Johns, K. A. Retention of habitat complexity minimizes disassembly of reef fish communities following disturbance: A large-scale natural experiment. PLoS ONE 9, e105384. https://doi.org/10.1371/journal.pone.0105384 (2014).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    14.
    Bellwood, D. R. et al. Coral recovery may not herald the return of fishes on damaged coral reefs. Oecologia 170, 567–573 (2012).
    ADS  PubMed  Article  Google Scholar 

    15.
    Pratchett, M. S., Coker, D. J., Jones, G. P. & Munday, P. L. Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss. Ecol. Evol. 2, 2168–2180 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    16.
    Ortiz, J. C. et al. Impaired recovery of the Great Barrier Reef under cumulative stress. Sci. Adv. 4, eaar6127. https://doi.org/10.1126/sciadv.aar6127 (2018).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    17.
    Bellwood, D. R. et al. Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biol. Conserv. 236, 604–615 (2019).
    Article  Google Scholar 

    18.
    Gilmour, J. P. et al. The state of Western Australia’s coral reefs. Coral Reefs 38, 651–667 (2019).
    ADS  Article  Google Scholar 

    19.
    Pisapia, C., Burn, D. & Pratchett, M. S. Changes in the population and community structure of corals during recent disturbances (February 2016–October 2017) on Maldivian coral reefs. Sci. Rep. 9, 8402. https://doi.org/10.1038/s41598-019-44809-9 (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    20.
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 

    21.
    Bruno, J. F. & Valdivia, A. Coral reef degradation is not correlated with local human population density. Sci. Rep. 6, 29778. https://doi.org/10.1038/srep29778 (2016).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    22.
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    23.
    Bruno, J. F. & Selig, E. R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2, e711. https://doi.org/10.1371/journal.pone.0000711 (2017).
    ADS  Article  Google Scholar 

    24.
    Kayal, M. et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7, e47363. https://doi.org/10.1371/journal.pone.0047363 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    25.
    Mellin, C. et al. Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts. Glob. Change Biol. 25, 2431–2445 (2019).
    Google Scholar 

    26.
    Chesher, R. H. Destruction of Pacific corals by sea star Acanthaster planci. Science 165, 280–283 (1969).
    ADS  CAS  PubMed  Article  Google Scholar 

    27.
    Pratchett, M. S., Schenk, T. J., Baine, M., Syms, C. & Baird, A. H. Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea. Mar. Environ. Res. 67, 230–236 (2009).
    CAS  PubMed  Article  Google Scholar 

    28.
    Kayal, M., Lenihan, H. S., Pau, C., Penin, L. & Adjeroud, M. Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak. Coral Reefs 30, 827–837 (2011).
    ADS  Article  Google Scholar 

    29.
    Pratchett, M. S., Caballes, C. F., Rivera-Posada, J. A. & Sweatman, H. P. A. Limits to understanding and managing outbreaks of crown-of-thorns stafish (Acanthaster spp.). Oceanogr. Mar. Biol. Ann. Rev. 52, 133–199 (2014).
    Google Scholar 

    30.
    Glynn, P. W. Some ecological consequences of coral-crustacean guard mutualisms in the Indian and Pacific Oceans. Symbiosis 4, 301–323 (1987).
    Google Scholar 

    31.
    Pratchett, M. S. Influence of coral symbionts on feeding preferences of crown-of-thorns starfish Acanthaster planci in the western Pacific. Mar. Ecol. Prog. Ser. 214, 111–119 (2001).
    ADS  Article  Google Scholar 

    32.
    McKeon, C. S., Stier, A. C., McIlroy, S. E. & Bolker, B. M. Multiple defender effects: Synergistic coral defense by mutualist crustaceans. Oecologia 169, 1095–1103 (2012).
    ADS  PubMed  Article  Google Scholar 

    33.
    Weber, J. N. & Woodhead, P. M. Ecological studies of coral predator Acanthaster planci in South Pacific. Mar. Biol. 6, 12–17 (1970).
    Article  Google Scholar 

    34.
    Birkeland, C. & Lucas, J. S. Acanthaster planci: Major Management Problem of Coral Reefs (CRC Press, Boca Raton, 1990).
    Google Scholar 

    35.
    Lassig, B. R. Communication and coexistence in a coral community. Mar. Biol. 42, 85–92 (1977).
    Article  Google Scholar 

    36.
    Cowan, Z. L., Dworjanyn, S. A., Caballes, C. F. & Pratchett, M. S. Predation on crown-of-thorns starfish larvae by damselfishes. Coral Reefs 35, 1253–1262 (2016).
    ADS  Article  Google Scholar 

    37.
    Cowan, Z. L., Ling, S. D., Caballes, C. F., Dworjanyn, S. A. & Pratchett, M. S. Crown-of-thorns starfish larvae are vulnerable to predation even in the presence of alternative prey. Coral Reefs 39, 293–303 (2020).
    Article  Google Scholar 

    38.
    Bonin, M. C. Specializing on vulnerable habitat: Acropora selectivity among damselfish recruits and the risk of bleaching-induced habitat loss. Coral Reefs 31, 287–297 (2012).
    ADS  Article  Google Scholar 

    39.
    Wilson, S. K., Graham, N. A. J., Pratchett, M. S., Jones, G. P. & Polunin, N. V. C. Multiple disturbances and the global degradation of coral reefs: Are reef fishes at risk or resilient?. Global Change Biol. 12, 2220–2234 (2006).
    ADS  Article  Google Scholar 

    40.
    Pratchett, M. S. et al. Effects of climate-induced coral bleaching on coral-reef fishes—Ecological and economic consequences. Oceanogr. Mar. Biol. Ann. Rev. 46, 257–302 (2008).
    Google Scholar 

    41.
    Pratchett, M. S., Thompson, C. A., Hoey, A. S., Cowman, P. F. & Wilson, S. K. Effects of coral bleaching and coral loss on the structure and function of reef fish assemblages. In Coral Bleaching (eds. van Oppen, M. J. & Lough, J. M.) 265–293 (Springer, Berlin, 2018).

    42.
    Bernal, M. A. et al. Species-specific molecular responses of wild coral reef fishes during a marine heatwave. Sci. Adv. 6, eaay3423. https://doi.org/10.1126/sciadv.aay3423 (2020).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    43.
    Magel, J. M., Dimoff, S. A. & Baum, J. K. Direct and indirect effects of climate change-amplified pulse heat stress events on coral reef fish communities. Ecol. Appl. https://doi.org/10.1002/eap.2124 (2020).
    Article  PubMed  Google Scholar 

    44.
    Booth, D. J. Opposing climate-change impacts on poleward-shifting coral-reef fishes. Coral Reefs 39, 577–581 (2020).
    Article  Google Scholar 

    45.
    Coker, D. J., Walker, S. P., Munday, P. L. & Pratchett, M. S. Social group entry rules may limit population resilience to patchy habitat disturbance. Mar. Ecol. Prog. Ser. 493, 237–242 (2013).
    ADS  Article  Google Scholar 

    46.
    Thompson, C. A., Matthews, S., Hoey, A. S. & Pratchett, M. S. Changes in sociality of butterflyfishes linked to population declines and coral loss. Coral Reefs 38, 527–537 (2019).
    ADS  Article  Google Scholar 

    47.
    Sano, M., Shimizu, M. & Nose, Y. Long-term effects of destruction of hermatypic corals by Acanthaster planci infestation on reef fish communities at Iriomote Island, Japan. Mar. Ecol. Prog. Ser. 37, 191–199 (1987).
    ADS  Article  Google Scholar 

    48.
    Jones, G. P., McCormick, M. I., Srinivasan, M. & Eagle, J. V. Coral decline threatens fish biodiversity in marine reserves. Proc. Nat. Acad. Sci. USA 101, 8251–8253 (2004).
    ADS  CAS  PubMed  Article  Google Scholar 

    49.
    Feary, D. A., Almany, G. R., McCormick, M. I. & Jones, G. P. Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153, 727–737 (2007).
    ADS  PubMed  Article  Google Scholar 

    50.
    McCormick, M. I. Lethal effects of habitat degradation on fishes through changing competitive advantage. Proc. R. Soc. B. 279, 3899–3904 (2012).
    PubMed  Article  Google Scholar 

    51.
    Coker, D. J., Pratchett, M. S. & Munday, P. L. Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav. Ecol. 20, 1204–1210 (2009).
    Article  Google Scholar 

    52.
    Coker, D. J., Wilson, S. K. & Pratchett, M. S. of live coral habitat for reef fishes. Rev. Fish Biol. Fish. 24, 89–126 (2014).
    Article  Google Scholar 

    53.
    Pratchett, M. S., Hoey, A. S., Wilson, S. K., Hobbs, J. P. & Allen, G. R. Habitat-use and specialisation among coral reef damselfishes. In Biology of Damselfishes (ed. Frederich, B. & Parmentier, E.) 84–121 (Taylor & Francis, London, 2016).

    54.
    Sale, P. F. Extremely limited home range in a coral reef fish, Dascyllus aruanus (Pisces, Pomacentridae). Copeia 1971, 324–327 (1971).
    Article  Google Scholar 

    55.
    Robertson, D. R. & Lassig, B. Spatial distribution patterns and coexistence of a group of territorial damselfishes from the Great Barrier Reef. Bull. Mar. Sci. 30, 187–203 (1980).
    Google Scholar 

    56.
    D’Agostino, D. et al. The influence of thermal extremes on coral reef fish behaviour in the Arabian/Persian Gulf. Coral Reefs 39, 733–744 (2019).
    Article  Google Scholar 

    57.
    Adam, T. C. et al. How will coral reef fish communities respond to climate-driven disturbances? Insight from landscape-scale perturbations. Oecologia 176, 285–296 (2014).
    ADS  PubMed  Article  Google Scholar 

    58.
    Coker, D. J., Pratchett, M. S. & Munday, P. L. Influence of coral bleaching, coral mortality and conspecific aggression on movement and distribution of coral-dwelling fish. J. Exp. Mar. Biol. Ecol. 414, 62–68 (2012).
    Article  Google Scholar 

    59.
    Chase, T. J., Pratchett, M. S., Frank, G. E. & Hoogenboom, M. O. Coral-dwelling fish moderate bleaching susceptibility of coral hosts. PLoS ONE 13, e0208545. https://doi.org/10.1371/journal.pone.0208545 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    60.
    Wismer, S., Tebbett, S. B., Streit, R. P. & Bellwood, D. R. Spatial mismatch in fish and coral loss following 2016 mass coral bleaching. Sci. Total Environ. 50, 1487–1498 (2019).
    ADS  Article  CAS  Google Scholar 

    61.
    Wilson, S. K. et al. Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28, 3–14 (2009).
    ADS  Article  Google Scholar 

    62.
    Wilson, S. K., Robinson, J. P., Chong-Seng, K., Robinson, J. & Graham, N. A. Boom and bust of keystone structure on coral reefs. Coral Reefs 38, 625–635 (2019).
    ADS  Article  Google Scholar 

    63.
    Schmidt-Roach, S. et al. Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32, 161–172 (2013).
    ADS  Article  Google Scholar 

    64.
    Booth, D. J. & Beretta, G. A. Changes in a fish assemblage after a coral bleaching event. Mar. Ecol. Prog. Ser. 245, 205–212 (2002).
    ADS  Article  Google Scholar 

    65.
    Sano, M., Shimizu, M. & Nose, Y. Changes in structure of coral reef fish communities by destruction of hermatypic corals: Observational and experimental views. Pac. Sci. 38, 51–79 (1984).
    Google Scholar 

    66.
    Bonin, M. C., Munday, P. L., McCormick, M. I., Srinivasan, M. & Jones, G. P. Coral-dwelling fishes resistant to bleaching but not to mortality of host corals. Mar. Ecol. Prog. Ser. 394, 215–222 (2009).
    ADS  Article  Google Scholar 

    67.
    Paddack, M. J. et al. Recent region-wide declines in Caribbean reef fish abundance. Curr. Biol. 19, 590–595 (2009).
    CAS  PubMed  Article  Google Scholar 

    68.
    Booth, D. J. Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill. J. Exp. Mar. Biol. Ecol. 155, 85–104 (1992).
    Article  Google Scholar 

    69.
    Sweatman, H. P. A. The influence of adults of some coral reef fishes on larval recruitment. Ecol. Monogr. 55, 469–485 (1985).
    Article  Google Scholar 

    70.
    Karplus, I., Katzenstein, R. & Goren, M. Predator recognition and social facilitation of predator avoidance in coral reef fish Dascyllus marginatus juveniles. Mar. Ecol. Prog. Ser. 319, 215–223 (2006).
    ADS  Article  Google Scholar 

    71.
    Forrester, G. E. Social rank, individual size and group composition as determinants of food consumption by humbug damselfish, Dascyllus aruanus. Anim. Behav. 42, 701–711 (1991).
    Article  Google Scholar 

    72.
    Holbrook, S. J., Brooks, A. J., Schmitt, R. J. & Stewart, H. L. Effects of sheltering fish on growth of their host corals. Mar. Biol. 155, 521–530 (2008).
    Article  Google Scholar 

    73.
    Noonan, S. H., Jones, G. P. & Pratchett, M. S. Coral size, health and structural complexity: Effects on the ecology of a coral reef damselfish. Mar. Ecol. Prog. Ser. 456, 127–137 (2012).
    ADS  Article  Google Scholar 

    74.
    Holbrook, S. J. & Schmitt, R. J. Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83, 2855–2868 (2002).
    Article  Google Scholar 

    75.
    Turgeon, K. & Kramer, D. L. Immigration rates during population density reduction in a coral reef fish. PLoS ONE 11, e0156417. https://doi.org/10.1371/journal.pone.0156417 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    76.
    Shpigel, M. & Fishelson, L. Behavior and physiology of coexistence in 2 species of Dascyllus (Pomacentridae, Teleostei). Environ. Biol. Fish. 17, 253–265 (1986).
    Article  Google Scholar 

    77.
    Wong, M. Y., Buston, P. M., Munday, P. L. & Jones, G. P. The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish. Proc. R. Soc. B. 274, 1093–1099 (2007).
    PubMed  Article  Google Scholar 

    78.
    Hixon, M. A. & Carr, M. H. Synergistic predation, density dependence, and population regulation in marine fish. Science 277, 946–949 (1997).
    CAS  Article  Google Scholar 

    79.
    Almany, G. R. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141, 105–113 (2004).
    ADS  PubMed  Article  Google Scholar 

    80.
    Wilson, S. K. et al. Influence of nursery microhabitats on the future abundance of a coral reef fish. Proc. R. Soc. B. 283, 20160903. https://doi.org/10.1098/rspb.2016.0903 (2016).
    Article  PubMed  Google Scholar 

    81.
    Graham, N. A. J., McClanahan, T. R., MacNeil, M. A., Wilson, S. K. & Polunin, N. V. C. Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems. PLoS ONE 3, e3039. https://doi.org/10.1371/journal.pone.0003039 (2008).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    82.
    Hing, M. L., Klanten, O. S., Dowton, M., Brown, K. R. & Wong, M. Y. Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes. PLoS ONE 13, e0202407. https://doi.org/10.1371/journal.pone.0202407 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    83.
    Hughes, et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    84.
    Emslie, M. J., Pratchett, M. S. & Cheal, A. J. Effects of different disturbance types on butterflyfish communities of Australia’s Great Barrier Reef. Coral Reefs 30, 461–471 (2011).
    ADS  Article  Google Scholar 

    85.
    Buchanan, J. R. et al. Living on the edge: Vulnerability of coral-dependent fishes in the Gulf. Mar. Poll. Bull. 105, 480–488 (2016).
    CAS  Article  Google Scholar 

    86.
    Pratchett, M. S. Dynamics of an outbreak population of Acanthaster planci at Lizard Island, northern Great Barrier Reef (1995–1999). Coral Reefs 24, 453–462 (2005).
    ADS  Article  Google Scholar 

    87.
    Pratchett, M. S. et al. Spatial, temporal and taxonomic variation in coral growth—Implications for the structure and function of coral reef ecosystems. Oceanogr. Mar. Biol. Ann. Rev. 53, 215–295 (2015).
    Google Scholar 

    88.
    Manly, B. F., McDonald, L., Thomas, D. L., McDonald, T. L. & Erickson, W. P. Resource selection by animals (Kluwer Academic Publishers, Dordrecht, 2010).
    Google Scholar 

    89.
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and nonlinear mixed effects models. https://CRAN.R-project.org/package=nlme (2020).

    90.
    R Core Team. R: A language and environment for statistical computing. https://www.R-project.org (2016). More

  • in

    Extracellular heme recycling and sharing across species by novel mycomembrane vesicles of a Gram-positive bacterium

    1.
    Faust K, Raes J, Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol. 2012;10:538–50.
    CAS  PubMed  Article  Google Scholar 
    2.
    Phelan VV, Liu WT, Pogliano K, Dorrestein PC. Microbial metabolic exchange—the chemotype-to-phenotype link. Nat Chem Biol. 2011;8:26–35.
    PubMed  Article  CAS  Google Scholar 

    3.
    Natale P, Brüser T, Driessen AJM. Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane: Distinct translocases and mechanisms. Biochim Biophys Acta. 2007;1778:1735–56.
    PubMed  Article  CAS  Google Scholar 

    4.
    Holland IB. The extraordinary diversity of bacterial protein secretion mechanisms. Meth Mol Biol. 2010;619:1–20.
    CAS  Article  Google Scholar 

    5.
    Guerrero-Mandujano A, Hernández-Cortez C, Ibarra JA, Castro-Escarpulli G. The outer membrane vesicles: Secretion system type zero. Traffic. 2017;18:425–32.
    CAS  PubMed  Article  Google Scholar 

    6.
    Orench‐Rivera N, Kuehn MJ. Environmentally controlled bacterial vesicle‐mediated export. Cell Microbiol. 2016;18:1525–36.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    7.
    Kim JH, Lee J, Park J, Gho YS, editors. Gram-negative and Gram-positive bacterial extracellular vesicles. Semin Cell Dev Biol. 2015;40:97–104.

    8.
    Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13:605–19.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    McBroom AJ, Kuehn MJ. Release of outer membrane vesicles by Gram‐negative bacteria is a novel envelope stress response. Mol Microbiol. 2007;63:545–58.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    10.
    Arntzen MO, Varnai A, Mackie RI, Eijsink VGH, Pope PB. Outer membrane vesicles from Fibrobacter succinogenes S85 contain an array of carbohydrate-active enzymes with versatile polysaccharide-degrading capacity. Environ Microbiol. 2017;19:2701–14.
    CAS  PubMed  Article  Google Scholar 

    11.
    Nordstrom T, Blom AM, Tan TT, Forsgren A, Riesbeck K. Ionic binding of C3 to the human pathogen Moraxella catarrhalis is a unique mechanism for combating innate immunity. J Immunol. 2005;175:3628–36.
    PubMed  Article  Google Scholar 

    12.
    Fulsundar S, Harms K, Flaten GE, Johnsen PJ, Chopade B, Nielsen KM. Gene transfer potential of outer membrane vesicles of Acinetobacter baylyi and effects of stress on vesiculation. Appl Environ Microb. 2014;80:3469–83.
    Article  CAS  Google Scholar 

    13.
    Mashburn LM, Whiteley M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature. 2005;437:422–5.
    CAS  PubMed  Article  Google Scholar 

    14.
    Toyofuku M, Morinaga K, Hashimoto Y, Uhl J, Shimamura H, Inaba H, et al. Membrane vesicle-mediated bacterial communication. ISME J. 2017;11:1504–9.
    PubMed  PubMed Central  Article  Google Scholar 

    15.
    Lee EY, Choi DY, Kim DK, Kim JW, Park JO, Kim S, et al. Gram‐positive bacteria produce membrane vesicles: proteomics‐based characterization of Staphylococcus aureus‐derived membrane vesicles. Proteomics. 2009;9:5425–36.
    CAS  PubMed  Article  Google Scholar 

    16.
    Prados-Rosales R, Baena A, Martinez LR, Luque-Garcia J, Kalscheuer R, Veeraraghavan U, et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Investig. 2011;121:1471–83.
    PubMed  Article  CAS  Google Scholar 

    17.
    Prados-Rosales R, Brown L, Casadevall A, Montalvo-Quiros S, Luque-Garcia JL. Isolation and identification of membrane vesicle-associated proteins in Gram-positive bacteria and mycobacteria. MethodsX. 2014;1:124–9.
    PubMed  PubMed Central  Article  Google Scholar 

    18.
    White DW, Elliott SR, Odean E, Bemis LT, Tischler AD. Mycobacterium tuberculosis Pst/SenX3-RegX3 regulates membrane vesicle production independently of ESX-5 activity. mBio. 2018;9:e00778–18.
    CAS  PubMed  PubMed Central  Google Scholar 

    19.
    Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. PNAS. 2008;105:3963–7.
    CAS  PubMed  Article  Google Scholar 

    20.
    Ganz T, Nemeth E. Iron homeostasis in host defence and inflammation. Nat Rev Immunol. 2015;15:500–10.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Huber DL. Synthesis, properties, and applications of iron nanoparticles. Small. 2005;1:482–501.
    CAS  PubMed  Article  Google Scholar 

    22.
    Wandersman C, Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol. 2004;58:611–47.
    CAS  PubMed  Article  Google Scholar 

    23.
    Morel FM, Price N. The biogeochemical cycles of trace metals in the oceans. Science. 2003;300:944–7.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    24.
    Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC, et al. Community proteomics of a natural microbial biofilm. Science. 2005;308:1915–20.
    CAS  PubMed  Article  Google Scholar 

    25.
    Cao B, Shi L, Brown RN, Xiong Y, Fredrickson JK, Romine MF, et al. Extracellular polymeric substances from Shewanella sp. HRCR‐1 biofilms: characterization by infrared spectroscopy and proteomics. Environ Microbiol. 2011;13:1018–31.
    CAS  PubMed  Article  Google Scholar 

    26.
    Vong L, Laës A, Blain S. Determination of iron–porphyrin-like complexes at nanomolar levels in seawater. Anal Chim Acta. 2007;588:237–44.
    CAS  PubMed  Article  Google Scholar 

    27.
    Létoffé S, Nato F, Goldberg ME, Wandersman C. Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol Microbiol. 1999;33:546–55.
    PubMed  Article  Google Scholar 

    28.
    Tong Y, Guo M. Bacterial heme-transport proteins and their heme-coordination modes. Arch Biochem Biophys. 2009;481:1–15.
    CAS  PubMed  Article  Google Scholar 

    29.
    Pilpa RM, Robson SA, Villareal VA, Wong ML, Phillips M, Clubb RT. Functionally distinct NEAT (NEAr Transporter) domains within the Staphylococcus aureus IsdH/HarA protein extract heme from methemoglobin. J Biol Chem. 2009;284:1166–76.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    30.
    Gat O, Zaide G, Inbar I, Grosfeld H, Chitlaru T, Levy H, et al. Characterization of Bacillus anthracis iron‐regulated surface determinant (Isd) proteins containing NEAT domains. Mol Microbiol. 2008;70:983–99.
    CAS  PubMed  PubMed Central  Google Scholar 

    31.
    Choby JE, Skaar EP. Heme synthesis and acquisition in bacterial pathogens. J Mol Biol. 2016;428:3408–28.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    32.
    Allen CE, Schmitt MP. HtaA is an iron-regulated hemin binding protein involved in the utilization of heme iron in Corynebacterium diphtheriae. J Bacteriol. 2009;191:2638–48.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    33.
    Allen CE, Schmitt MP. Novel hemin binding domains in the Corynebacterium diphtheriae HtaA protein interact with hemoglobin and are critical for heme iron utilization by HtaA. J Bacteriol. 2011;193:5374–85.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    34.
    Duckworth AW, Grant S, Grant WD, Jones BE, Meijer D. Dietzia natronolimnaios sp. nov., a new member of the genus Dietzia isolated from an East African soda lake. Extremophiles. 1998;2:359–66.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Mayilraj S, Suresh K, Kroppenstedt R, Saini H. Dietzia kunjamensis sp. nov., isolated from the Indian Himalayas. Int J Syst Evol Microbiol. 2006;56:1667–71.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    36.
    Li J, Chen C, Zhao G-Z, Klenk H-P, Pukall R, Zhang Y-Q, et al. Description of Dietzia lutea sp. nov., isolated from a desert soil in Egypt. Syst Appl Microbiol. 2009;32:118–23.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    37.
    Fang H, Qin X-Y, Zhang K-D, Nie Y, Wu X-L. Role of the Group 2 Mrp sodium/proton antiporter in rapid response to high alkaline shock in the alkaline-and salt-tolerant Dietzia sp. DQ12-45-1b. Appl Microbiol Biotechnol. 2018;102:3765–77.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    38.
    Wang X-B, Chi C-Q, Nie Y, Tang Y-Q, Tan Y, Wu G, et al. Degradation of petroleum hydrocarbons (C6–C40) and crude oil by a novel Dietzia strain. Bioresour Technol. 2011;102:7755–61.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    39.
    Rédei GP M9 Bacterial Minimal Medium. In: Rédei GP, editors. Encyclopedia of genetics, genomics, proteomics and informatics, 3rd edn. Dordrecht: Springer Group; 2008. pp. 484–6.

    40.
    Van Kessel JC, Hatfull GF. Recombineering in Mycobacterium tuberculosis. Nat Methods. 2007;4:147–52.
    PubMed  Article  CAS  Google Scholar 

    41.
    Liang J, Jiangyang J, Nie Y, Wu X. Regulation of the alkane hydroxylase CYP153 gene in a Gram-positive alkane-degrading bacterium, Dietzia sp. strain DQ12-45-1b. Appl Environ Microbiol. 2016;82:608–19.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    42.
    Lu S, Nie Y, Tang Y-Q, Xiong G, Wu X-L. A critical combination of operating parameters can significantly increase the electrotransformation efficiency of a Gram-positive Dietzia strain. J Microbiol Methods. 2014;103:144–51.
    CAS  PubMed  Article  Google Scholar 

    43.
    Szvetnik A, Bihari Z, Szabo Z, Kelemen O, Kiss I. Genetic manipulation tools for Dietzia spp. J Appl Microbiol. 2010;109:1845–52.
    CAS  PubMed  Google Scholar 

    44.
    Deininger PL. Molecular cloning: a laboratory manual. Anal Biochem. 1990;186:182–3.
    Article  Google Scholar 

    45.
    McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol. 2006;188:5385–92.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    46.
    Prados-Rosales R, Weinrick BC, Pique DG, Jacobs WR Jr, Casadevall A, Rodriguez GM. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J Bacteriol. 2014;196:1250–6.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    47.
    Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Biochem Cell Biol. 1959;37:911–7.
    CAS  Google Scholar 

    48.
    Keddie RM, Cure GL. The cell wall composition and distribution of free mycolic acids in named strains of coryneform bacteria and in isolates from various natural sources. J Appl Microbiol. 1977;42:229–52.
    CAS  Google Scholar 

    49.
    Liu Y, Zhang Q, Hu M, Yu K, Fu J, Zhou F, et al. Proteomic analyses of intracellular Salmonella enterica serovar Typhimurium reveal extensive bacterial adaptations to infected host epithelial cells. Infect Immun. 2015;83:2897–906.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    50.
    Calderoncelis F, Encinar JR, Sanzmedel A. Standardization approaches in absolute quantitative proteomics with mass spectrometry. Mass Spectrom Rev. 2018;37:715–37.
    CAS  Article  Google Scholar 

    51.
    Liang J-L, Gao Y, He Z, Nie Y, Wang M, JiangYang J-H, et al. Crystal structure of TetR family repressor AlkX from Dietzia sp. strain DQ12-45-1b implicated in biodegradation of n-alkanes. Appl Environ Microbiol. 2017;83:e01447–17.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    52.
    Tashiro Y, Hasegawa Y, Shintani M, Takaki K, Ohkuma M, Kimbara K, et al. Interaction of bacterial membrane vesicles with specific species and their potential for delivery to target cells. Front Microbiol. 2017;8:571.
    PubMed  PubMed Central  Article  Google Scholar 

    53.
    Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2014;43:D222–D6.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    54.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    55.
    Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010;26:1608–15.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    Song H, Sandie R, Wang Y, Andrade-Navarro MA, Niederweis M. Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis. 2008;88:526–44.
    CAS  PubMed  Article  Google Scholar 

    57.
    Daffé M, Quémard A, Marrakchi H. Mycolic acids: from chemistry to biology. In: Geiger O, editors. Biogenesis of fatty acids, lipids and membranes. Cham: Springer; 2017. p. 1–36.

    58.
    Choi D, Kim D, Choi SJ, Lee J, Choi J, Rho S, et al. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics. 2011;11:3424–9.
    CAS  PubMed  Article  Google Scholar 

    59.
    Marchand CH, Salmeron C, Bou Raad R, Meniche X, Chami M, Masi M, et al. Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J Bacteriol. 2012;194:587–97.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    60.
    Daffe M, Marrakchi H. Unraveling the structure of the mycobacterial envelope. Microbiol Spectr. 2019;7:1087–95.
    Article  Google Scholar 

    61.
    Nishiuchi Y, Baba T, Yano I. Mycolic acids from Rhodococcus, Gordonia, and Dietzia. J Microbiol Methods. 2000;40:1–9.
    CAS  PubMed  Article  Google Scholar 

    62.
    Collins M, Goodfellow M, Minnikin D. A survey of the structures of mycolic acids in Corynebacterium and related taxa. Microbiology. 1982;128:129–49.
    CAS  Article  Google Scholar 

    63.
    Rath P, Saurel O, Czaplicki G, Tropis M, Daffé M, Ghazi A, et al. Cord factor (trehalose 6, 6′-dimycolate) forms fully stable and non-permeable lipid bilayers required for a functional outer membrane. Biochim Biophys Acta-Biomemb. 2013;1828:2173–81.
    CAS  Article  Google Scholar 

    64.
    Caruana JC, Walper SA. Bacterial membrane vesicles as mediators of microbe – microbe and microbe – host community interactions. Front Microbiol. 2020;11:432.
    PubMed  PubMed Central  Article  Google Scholar 

    65.
    Rich PR, Maréchal A 8.5 electron transfer chains: structures, mechanisms and energy coupling. In: Egelman EH, editor. Comprehensive biophysics. Amsterdam: Elsevier; 2012. p. 72–93.

    66.
    Butaitė E, Baumgartner M, Wyder S, Kümmerli R. Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities. Nat Commun. 2017;8:1–12.
    Article  CAS  Google Scholar 

    67.
    Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffé M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol. 2008;190:5672–80.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    68.
    Sani M, Houben ENG, Geurtsen J, Pierson J, De Punder K, Van Zon M, et al. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog. 2010;6:e1000794.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020;18:152–63.
    CAS  PubMed  Article  Google Scholar 

    70.
    Rakoff-Nahoum S, Coyne MJ, Comstock LE. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol. 2014;24:40–9.
    CAS  PubMed  Article  PubMed Central  Google Scholar  More