in

Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community

  • 1.

    Kannenberg, S. A., Schwalm, C. R. & Anderegg, W. R. L. Ghosts of the past: how drought legacy effects shape forest functioning and carbon cycling. Ecol. Lett. 23, 891–901 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Padisak, J. Seasonal succession of phytoplankton in a large shallow lake (Balaton, Hungary)—a dynamic approach to ecological memory, its possible role and mechanisms. J. Ecol. 80, 217–230 (1992).

    Article 

    Google Scholar 

  • 3.

    Power, D. A. et al. What can ecosystems learn? Expanding evolutionary ecology with learning theory. Biol. Direct 10, 69 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 4.

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 5.

    Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287 (2013).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 6.

    Seneviratne, S. I. et al. Changes in climate extremes and their impacts on the natural physical environment. In Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change (IPCC) (eds. Field, C.B. et al.) 109–230 (Cambridge University Press, 2017).

  • 7.

    Pappas, C., Mahecha, M. D., Frank, D. C., Babst, F. & Koutsoyiannis, D. Ecosystem functioning is enveloped by hydrometeorological variability. Nat. Ecol. Evol. 1, 1263–1270 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 8.

    Hawkes, C. V. & Keitt, T. H. Resilience vs. historical contingency in microbial responses to environmental change. Ecol. Lett. 18, 612–625 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Johnstone, J. F. et al. Changing disturbance regimes, ecological memory, and forest resilience. Front. Ecol. Environ. 14, 369–378 (2016).

    Article 

    Google Scholar 

  • 10.

    Ochoa‐Hueso, R. et al. Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Glob. Chang. Biol. 24, 2818–2827 (2018).

  • 11.

    Bastida, F. et al. Differential sensitivity of total and active soil microbial communities to drought and forest management. Glob. Chang. Biol. 23, 4185–4203 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 12.

    Evans, S. E., Wallenstein, M. D. & Burke, I. C. Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought? Ecology 95, 110–122 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 13.

    de Vries, F. T. et al. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9, 3033 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 14.

    Rousk, J., Smith, A. R. & Jones, D. L. Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems. Glob. Chang. Biol. 19, 3872–3884 (2013).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 15.

    Kaisermann, A., de Vries, F. T., Griffiths, R. I. & Bardgett, R. D. Legacy effects of drought on plant–soil feedbacks and plant–plant interactions. New Phytol. 215, 1413–1424 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 16.

    Fuchslueger, L. et al. Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event. J. Ecol. 104, 1453–1465 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 17.

    Meisner, A., De Deyn, G. B., de Boer, W. & van der Putten, W. H. Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proc. Natl Acad. Sci. USA 110, 9835–9838 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 18.

    de Nijs, E. A., Hicks, L. C., Leizeaga, A., Tietema, A. & Rousk, J. Soil microbial moisture dependences and responses to drying–rewetting: the legacy of 18 years drought. Glob. Chang. Biol. 25, 1005–1015 (2019).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    Fuchslueger, L., Bahn, M., Fritz, K., Hasibeder, R. & Richter, A. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol. 201, 916–927 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 20.

    Mooshammer, M., Wanek, W., Zechmeister-Boltenstern, S. & Richter, A. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front. Microbiol. 5, 22 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 21.

    Waring, B. G., Weintraub, S. R. & Sinsabaugh, R. L. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117, 101–113 (2014).

    CAS 
    Article 

    Google Scholar 

  • 22.

    Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 23.

    Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688, (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 24.

    Csonka, L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Mol. Biol. Rev. 53, 121–147 (1989).

    CAS 

    Google Scholar 

  • 25.

    Whitfield, G. B., Marmont, L. S. & Howell, P. L. Enzymatic modifications of exopolysaccharides enhance bacterial persistence. Front. Microbiol. 6, 471 (2015).

  • 26.

    Byrd, M. S. et al. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol. Microbiol. 73, 622–638 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 27.

    El Zoeiby, A., Sanschagrin, F. & Levesque, R. C. Structure and function of the Mur enzymes: development of novel inhibitors. Mol. Microbiol. 47, 1–12 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 28.

    Lebre, P. H., De Maayer, P. & Cowan, D. A. Xerotolerant bacteria: surviving through a dry spell. Nat. Rev. Microbiol. 15, 285–296 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 30.

    Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Chang. 9, 40–43 (2019).

  • 31.

    Seidl, R., Donato, D. C., Raffa, K. F. & Turner, M. G. Spatial variability in tree regeneration after wildfire delays and dampens future bark beetle outbreaks. Proc. Natl Acad. Sci. USA 113, 13075–13080 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

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

  • 33.

    Meisner, A., Jacquiod, S., Snoek, B. L., ten Hooven, F. C. & van der Putten, W. H. Drought legacy effects on the composition of soil fungal and prokaryote communities. Front. Microbiol. 9, 294 (2018).

  • 34.

    Bardgett, R. D. & Caruso, T. Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190112 (2020).

    CAS 
    Article 

    Google Scholar 

  • 35.

    Isobe, K., Bouskill, N. J., Brodie, E. L., Sudderth, E. A. & Martiny, J. B. H. Phylogenetic conservation of soil bacterial responses to simulated global changes. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190242 (2020).

    CAS 
    Article 

    Google Scholar 

  • 36.

    Barberán, A., Caceres Velazquez, H., Jones, S. & Fierer, N. Hiding in plain sight: mining bacterial species records for phenotypic trait information. mSphere 2, e00237–17 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Bouskill, N. J. et al. Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J. 7, 384 (2012).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 38.

    Taketani, R. G. et al. Dry season constrains bacterial phylogenetic diversity in a semi-arid rhizosphere system. Microb. Ecol. 73, 153–161 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 39.

    Naylor, D., DeGraaf, S., Purdom, E. & Coleman-Derr, D. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 11, 2691 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 40.

    Xu, L. et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc. Natl Acad. Sci. USA 115, E4284–E4293 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 41.

    Taniguchi, T., Kitajima, K., Douhan, G. W., Yamanaka, N. & Allen, M. F. A pulse of summer precipitation after the dry season triggers changes in ectomycorrhizal formation, diversity, and community composition in a Mediterranean forest in California, USA. Mycorrhiza 28, 665–677 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 42.

    Ren, C. et al. Responses of soil total microbial biomass and community compositions to rainfall reductions. Soil Biol. Biochem. 116, 4–10 (2018).

    CAS 
    Article 

    Google Scholar 

  • 43.

    Furze, J. R. et al. Resistance and resilience of root fungal communities to water limitation in a temperate agroecosystem. Ecol. Evol. 7, 3443–3454 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 44.

    Deveautour, C., Donn, S., Power, S. A., Bennett, A. E. & Powell, J. R. Experimentally altered rainfall regimes and host root traits affect grassland arbuscular mycorrhizal fungal communities. Mol. Ecol. 27, 2152–2163 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 46.

    Dijkstra, F. A., He, M., Johansen, M. P., Harrison, J. J. & Keitel, C. Plant and microbial uptake of nitrogen and phosphorus affected by drought using 15N and 32P tracers. Soil Biol. Biochem. 82, 135–142 (2015).

    CAS 
    Article 

    Google Scholar 

  • 47.

    Kakumanu, M. L., Ma, L. & Williams, M. A. Drought-induced soil microbial amino acid and polysaccharide change and their implications for C–N cycles in a climate change world. Sci. Rep. 9, 10968 (2019).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 48.

    Sleator, R. D. & Hill, C. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26, 49–71 (2002).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Warren, C. R. Response of osmolytes in soil to drying and rewetting. Soil Biol. Biochem. 70, 22–32 (2014).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 50.

    Bouskill, N. J. et al. Belowground response to drought in a tropical forest soil. I. Changes in microbial functional potential and metabolism. Front. Microbiol. 7, 525 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 51.

    Flemming, H.-C. et al. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Malik, A. A. et al. Drought and plant litter chemistry alter microbial gene expression and metabolite production. ISME J. 14, 2236–2247 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Nunan, N., Raynaud, X. & Schmidt, H. The ecology of heterogeneity: soil bacterial communities and C dynamics. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190249 (2020).

  • 54.

    Li, J. et al. Predictive genomic traits for bacterial growth in culture versus actual growth in soil. ISME J. 13, 2162–2172 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 55.

    Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 56.

    Grigulis, K. et al. Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J. Ecol. 101, 47–57 (2013).

    Article 

    Google Scholar 

  • 57.

    Lau, J. A. & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl Acad. Sci. USA 109, 14058–14062 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Fitzpatrick, C. R. et al. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl Acad. Sci. USA 115, E1157–E1165 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 59.

    Huang, S. et al. Autotrophic and heterotrophic soil respiration responds asymmetrically to drought in a subtropical forest in the Southeast China. Soil Biol. Biochem. 123, 242–249 (2018).

    CAS 
    Article 

    Google Scholar 

  • 60.

    López-Ballesteros, A. et al. Enhancement of the net CO2 release of a semiarid grassland in SE Spain by rain pulses. J. Geophys. Res. Biogeosci. 121, 52–66 (2016).

    Article 
    CAS 

    Google Scholar 

  • 61.

    Schimel, J. P. Life in dry soils: effects of drought on soil microbial communities and processes. Annu. Rev. Ecol. Evol. Syst. 49, 409–432 (2018).

    Article 

    Google Scholar 

  • 62.

    Canarini, A., Kaiser, C., Merchant, A., Richter, A. & Wanek, W. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10, 157 (2019).

  • 63.

    de Vries, F. T. et al. Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytol. 224, 132–145 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 64.

    Teste, F. P. et al. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355, 173–176 (2017).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 65.

    Hu, L. et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 66.

    Canarini, A., Merchant, A. & Dijkstra, F. A. Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere 2, 85–97 (2016).

  • 67.

    Canarini, A. & Dijkstra, F. A. Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol. Biochem. 81, 195–203 (2015).

  • 68.

    Morecroft, M. D. et al. Changing precipitation patterns alter plant community dynamics and succession in an ex-arable grassland. Funct. Ecol. 18, 648–655 (2004).

    Article 

    Google Scholar 

  • 69.

    Strickland, M. S., Osburn, E., Lauber, C., Fierer, N. & Bradford, M. A. Litter quality is in the eye of the beholder: initial decomposition rates as a function of inoculum characteristics. Funct. Ecol. 23, 627–636 (2009).

    Article 

    Google Scholar 

  • 70.

    Allison, S. D. et al. Microbial abundance and composition influence litter decomposition response to environmental change. Ecology 94, 714–725 (2013).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Walker, T. W. N. et al. A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem. Nat. Ecol. Evol. 4, 101–108 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Ogle, K. et al. Quantifying ecological memory in plant and ecosystem processes. Ecol. Lett. 18, 221–235 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Bahn, M., Knapp, M., Garajova, Z., Pfahringer, N. & Cernusca, A. Root respiration in temperate mountain grasslands differing in land use. Glob. Chang. Biol. 12, 995–1006 (2006).

    ADS 
    Article 

    Google Scholar 

  • 74.

    Bahn, M. et al. Soil respiration at mean annual temperature predicts annual total across vegetation types and biomes. Biogeosciences 7, 2147 (2010).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 75.

    Schmitt, M., Bahn, M., Wohlfahrt, G., Tappeiner, U. & Cernusca, A. Land use affects the net ecosystem CO2 exchange and its components in mountain grasslands. Biogeosciences 7, 2297 (2010).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 76.

    Estiarte, M. et al. Few multiyear precipitation–reduction experiments find a shift in the productivity–precipitation relationship. Glob. Chang. Biol. 22, 2570–2581 (2016).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 77.

    Spohn, M., Klaus, K., Wanek, W. & Richter, A. Microbial carbon use efficiency and biomass turnover times depending on soil depth—Implications for carbon cycling. Soil Biol. Biochem. 96, 74–81 (2016).

    CAS 
    Article 

    Google Scholar 

  • 78.

    Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Ågren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 79.

    Schinner, F., Öhlinger, R., Kandeler, E., Margesin, R. & Kaiser, P. Methods in soil biology. Bull. Inst. Pasteur 4, 311–312 (1996).

    Google Scholar 

  • 80.

    Kuo, S. Phosphorus. In Methods of Soil Analysis, Part 3 (eds. Sparks, D. L. et al.) Ch. 32, 869–919 (SSSA, 1996).

  • 81.

    Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).

    CAS 
    Article 

    Google Scholar 

  • 82.

    Brookes, P. C., Landman, A., Pruden, G. & Jenkinson, D. S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842 (1985).

    CAS 
    Article 

    Google Scholar 

  • 83.

    Doyle, A., Weintraub, M. N. & Schimel, J. P. Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci. Soc. Am. J. 68, 669–676 (2004).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 84.

    Kandeler, E. & Gerber, H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68–72 (1988).

    CAS 
    Article 

    Google Scholar 

  • 85.

    Hood-Nowotny, R., Umana, N. H.-N., Inselbacher, E., Oswald- Lachouani, P. & Wanek, W. Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci. Soc. Am. J. 74, 1018–1027 (2010).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 86.

    Jones, D. L., Owen, A. G. & Farrar, J. F. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol. Biochem. 34, 1893–1902 (2002).

    CAS 
    Article 

    Google Scholar 

  • 87.

    Prommer, J. et al. Biochar decelerates soil organic nitrogen cycling but stimulates soil nitrification in a temperate arable field trial. PLoS ONE 9, e86388 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 88.

    Kaiser, C., Frank, A., Wild, B., Koranda, M. & Richter, A. Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol. Biochem. 42, 1650–1652 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 89.

    Kaiser, C. et al. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol. 187, 843–858 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 90.

    Olsson, P. A. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 29, 303–310 (1999).

    CAS 
    Article 

    Google Scholar 

  • 91.

    Ngosong, C., Gabriel, E. & Ruess, L. Use of the signature fatty acid 16:1ω5 as a tool to determine the distribution of arbuscular mycorrhizal fungi in soil. J. Lipids 2012, 236807 (2012).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 92.

    Quideau, S. A. et al. Extraction and analysis of microbial phospholipid fatty acids in soils. J. Vis. Exp. 2016, 54360 (2016).

  • 93.

    García-Orenes, F., Morugán-Coronado, A., Zornoza, R., Cerdà, A. & Scow, K. Changes in soil microbial community structure influenced by agricultural management practices in a mediterranean agro-ecosystem. PLoS ONE 8, e80522–e80522 (2013).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 94.

    Herbold, C. et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front. Microbiol. 6, 731 (2015).

  • 95.

    Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).

    Article 

    Google Scholar 

  • 96.

    Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 97.

    White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 315–322 (Academic Press, 1990).

  • 98.

    Paymaneh, Z., Sarcheshmehpour, M., Bukovská, P. & Jansa, J. Could indigenous arbuscular mycorrhizal communities be used to improve tolerance of pistachio to salinity and/or drought? Symbiosis 79, 269–283 (2019).

  • 99.

    Smith, D. P. & Peay, K. G. Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS ONE 9, e90234 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 100.

    Tedersoo, L. & Lindahl, B. Fungal identification biases in microbiome projects. Environ. Microbiol. Rep. 8, 774–779 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 101.

    Krüger, M., Stockinger, H., Krüger, C. & Schüßler, A. DNA‐based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol. 183, 212–223 (2009).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 102.

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

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 103.

    Bengtsson‐Palme, J. et al. Improved software detection and extraction of ITS1 and ITS 2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).

    Google Scholar 

  • 104.

    Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 105.

    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 106.

    Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 107.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 108.

    Deshpande, V. et al. Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 109.

    R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2017).

  • 110.

    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 
    Article 

    Google Scholar 

  • 111.

    Chen, L. et al. GMPR: a robust normalization method for zero-inflated count data with application to microbiome sequencing data. PeerJ 6, e4600–e4600 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 112.

    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 
    Article 
    CAS 

    Google Scholar 

  • 113.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

  • 114.

    Kozak, M. & Piepho, H. What’s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions. J. Agron. Crop Sci. 204, 86–98 (2018).

    Article 

    Google Scholar 

  • 115.

    Ben-Shachar, M. S., Lüdecke, D. & Makowski, D. effectsize: Estimation of effect size indices and standardized parameters. J. Open Source Softw. 5, 2815 (2020).

    ADS 
    Article 

    Google Scholar 

  • 116.

    Oksanen, J. et al. Package ‘vegan’. Community Ecol. Packag. 2, 1–295 (2013).

    Google Scholar 

  • 117.

    Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta‐analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).

    Article 

    Google Scholar 

  • 118.

    Barbera, P. et al. EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst. Biol. 68, 365–369 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 119.

    Czech, L. & Stamatakis, A. Scalable methods for analyzing and visualizing phylogenetic placement of metagenomic samples. PLoS ONE 14, e0217050–e0217050 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 120.

    Louca, S. & Doebeli, M. Efficient comparative phylogenetics on large trees. Bioinformatics 34, 1053–1055 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 121.

    McMurdie, P. J. & Paulson, J. N. biomformat: An interface package for the BIOM file format. R/Bioconductor Package, version 1.0.0. (Bioconductor, 2015).


  • Source: Ecology - nature.com

    Proteomic traits vary across taxa in a coastal Antarctic phytoplankton bloom

    Verrucomicrobiota are specialist consumers of sulfated methyl pentoses during diatom blooms