Patterns of local, intercontinental and interseasonal variation of soil bacterial and eukaryotic microbial communities

[en] Although ongoing research has revealed some of the main drivers behind global spatial patterns of microbial communities, spatio-temporal dynamics of these communities still remain largely unexplored. Here, we investigate spatio-temporal variability of both bacterial and eukaryotic soil microbial communities at local and intercontinental scales. We compare how temporal variation in community composition scales with spatial variation in community composition, and explore the extent to which bacteria, protists, fungi and metazoa have similar patterns of temporal community dynamics. All soil microbial groups displayed a strong correlation between spatial distance and community dissimilarity, which was related to the ratio of organism to sample size. Temporal changes were variable, ranging from equal to local between-sample variation, to as large as that between communities several thousand kilometers apart. Moreover, significant correlations were found between bacterial and protist communities, as well as between protist and fungal communities, indicating that these microbial groups change in tandem, potentially driven by interactions between them. We conclude that temporal variation can be considerable in soil microbial communities, and that future studies need to consider temporal variation in order to reliably capture all drivers of soil microbiome changes.

Disciplines :

Microbiology
Biochemistry, biophysics & molecular biology

Author, co-author :

De Gruyter, Johan

Weedon, James

Bazot, Stéphane

Dauwe, Steven

Fernandez-Garberi, Pere-Roc

Geisen, Stephan

Gourlez de la Motte, Louis ; Université de Liège - ULiège > Département GxABT > Plant Sciences

Heinesch, Bernard ; Université de Liège - ULiège > Département GxABT > Biosystems Dynamics and Exchanges

Janssens, Ivan

Leblanc, Niki

More authors (7 more)

Language :

English

Title :

Patterns of local, intercontinental and interseasonal variation of soil bacterial and eukaryotic microbial communities

Publication date :

January 2020

Journal title :

FEMS Microbiology Ecology

ISSN :

0168-6496

eISSN :

1574-6941

Publisher :

Oxford University Press, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 23 March 2020

Statistics

Number of views

91 (2 by ULiège)

Number of downloads

223 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Adl MS, Gupta VVSR. Protists in soil ecology and forest nutrient cycling. Can J Forest Res 2006;36:1805-17.
Bahram M, Hildebrand F, Forslund SK et al. Structure and function of the global topsoilmicrobiome. Nature 2018;560:233-7.
Bates ST, Clemente JC, Flores GE et al. Global biogeography of highly diverse protistan communities in soil. ISME J 2013;7:652-9.
Bernhard JM, Kormas K, Pachiadaki MG et al. Benthic protists and fungi of Mediterranean deep hypsersaline anoxic basin redoxcline sediments. Front Microbiol 2014;5:1-13.
Bittinger K. usedist: DistanceMatrix Utilities. R package version 0.1.0. URL: https://CRAN.R-project.org/package=usedist. 2017.
Bŕechet LM, Lopez-Sangil L, George C et al. Distinct responses of soil respiration to experimental litter manipulation in temperatewoodland and tropical forest. Ecol Evol 2018;8:3787-96.
Buscardo E, Geml J, Schmidt SK et al. Spatio-temporal dynamics of soil bacterial communities as a function of Amazon forest phenology. Sci Rep 2018;8:1-13.
Caporaso JG, Kuczynski J, Stombaugh J et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
Caron DA, Countway PD, Jones AC et al. Marine protistan diversity. Ann Rev Mar Sci 2011;4:467-93.
Chemidlin Prevost-Boure N, Maron PA, Ranjard L et al. Seasonal dynamics of the bacterial community in forest soils under different quantities of leaf litter. Appl Soil Ecol 2011;47: 14-23.
Clarholm M. Protozoan grazing of bacteria in soil-impact and importance. Microb Ecol 1981;7:343-50.
Couteaux MM, Bottner P. Biological Interactions Between Fauna and the Microbial Community in Soils. Chichester: John Wiley &Sons, 1994.
Crowther TW, Boddy L, Jones TH. Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 2011;167:535-45.
Delgado-Baquerizo M, Oliverio AM, Brewer TE et al. A global atlas of the dominant bacteria found in soil. Science 2018a;359: 320-5.
Delgado-Baquerizo M, Reith F, Dennis PG et al. Ecological drivers of soil microbial diversity and soil biological networks in the Southern Hemisphere. Ecology 2018b;99:583-96.
de Ruiter PC, Neutel A-M,Moore JC. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 1995;269:1257-60.
Dunthorn M, Kauserud H, Bass D et al. Yeasts dominate soil fungal communities in three lowland Neotropical rainforests. Environ Microbiol Rep 2017;9:668-75.
Dupont AOC, Griffiths RI, Bell T et al. Differences in soil micro-eukaryotic communities over soil pH gradients are strongly driven by parasites and saprotrophs. Environ Microbiol 2016;18:2010-24.
Edgar RC. Search and clustering orders ofmagnitude faster than BLAST. Bioinformatics 2010;26:2460-1.
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013;10:996.
Ekelund F, Rønn R. Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol Rev 1994;15:321-53.
Finlay BJ, Black HIJ, Brown S et al. Estimating the growth potential of the soil protozoan community. Protist 2000;151:69-80.
Foissner W. Protozoa as bioindicators in agroecosystems, with emphasis on farming practices, biocides, and biodiversity. Agric Ecosyst Environ 1997;62:93-103.
Geisen S, Koller R, Hünninghaus M et al. The soil food web revisited: diverse and widespread mycophagous soil protists. Soil Biol Biochem 2016;94:10-8.
Geisen S, Laros I, Vizcáino A et al. Not all are free-living: high-throughput DNA metabarcoding reveals a diverse community of protists parasitizing soil metazoa. Mol Ecol 2015a;24:4556-69.
Geisen S, Mitchell EAD, Wilkinson DM et al. Soil protistology rebooted: 30 fundamental questions to start with. Soil Biol Biochem 2017;111:94-103.
Geisen S, Rosengarten J, Koller R et al. Pack hunting by a common soil amoeba on nematodes. Environ Microbiol 2015b;17: 4538-46.
Gilbert JA, Steele JA, Caporaso JG et al. Defining seasonal marine microbial community dynamics. ISME J 2012;6:298-308.
Guillou L, Bachar D, Audic S et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res 2013;41:D597-604.
Hijmans RJ. geosphere: Spherical Trigonometry. R package version 1.5-URL: https://CRAN.R-project.org/package=geosphere. 2017.
Hillebrand H, Azovsky AI. Body size determines the strength of the latitudinal diversity gradient. Ecography 2001;24:251-6.
Hillebrand H, Watermann F, Karez R et al. Differences in species richness patterns between unicellular and multicellular organisms. Oecologia 2001;126:114-24.
Jassey VEJ, Shimano S, Dupuy C et al. Characterizing the feeding habits of the testate amoebae Hyalosphenia papilio and Nebela tincta along a narrow "Fen-Bog" gradient using digestive vacuole content and13C and15N isotopic analyses. Protist 2012;163:451-64.
Kennedy K, Hall MW, Lynch MDJ et al. Evaluating bias of Illumina-based bacterial 16S rRNA gene profiles. Appl Environ Microb 2014;80:5717-22.
Klindworth A, Pruesse E, Schweer T et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and nextgeneration sequencing-based diversity studies. Nucleic Acids Res 2013;41:1-11.
Lan G, Li Y, Lesueurd D et al. Seasonal changes impact soil bacterial communities in a rubber plantation on Hainan Island, China. Sci Total Environ 2018;626:826-34.
Lauber CL, Hamady M, Knight R et al. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl EnvironMicrob 2009;75:5111-20.
Lauber CL, Ramirez KS, Aanderud Z et al. Temporal variability in soil microbial communities across land-use types. ISME J 2013;7:1641-50.
Lazzaro A, Hilfiker D, Zeyer J. Structures of microbial communities in alpine soils: seasonal and elevational effects. Front Microbiol 2015;6:1-13.
Leff JW, Jones SE, Prober SM et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci 2015;112: 10967-72.
Lenoir L, Persson T, Bengtsson J et al. Bottom-up or top-down control in forest soil microcosms? Effects of soil fauna on fungal biomass and C/N mineralisation. Biol Fertil Soils 2007;43:281-94.
Lie AAY, Liu Z, Hu SK et al. Investigating microbial eukaryotic diversity from a global census: insights from a comparison of pyrotag and full-length sequences of 18S rRNA genes. Appl Environ Microb 2014;80:4363-73.
Logares R, Haverkamp THA, Kumar S et al. Environmental microbiology through the lens of high-throughput DNA sequencing: synopsis of current platforms and bioinformatics approaches. J Microbiol Methods 2012;91: 106-13.
López-Escardó D, Paps J, De Vargas C et al. Metabarcoding analysis on European coastal samples reveals new molecular metazoan diversity. Sci Rep 2018;8:1-14.
Maestre FT, Delgado-Baquerizo M, Jeffries TC et al. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Natl Acad Sci 2015;112:201516684.
Mahé F, Mayor J, Bunge J et al. Comparing high-throughput platforms for sequencing the V4 region of SSU-rDNA in environmental microbial eukaryotic diversity surveys. J Eukaryot Microbiol 2015;62:338-45.
Mahé F, De Vargas C, Bass D et al. Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests. Nat Ecol Evol 2017;1:1-8.
Meyer KM, Memiaghe H, Korte L et al. Why do microbes exhibit weak biogeographic patterns? ISME J 2018;12:1404-13.
Mikola J, Seẗalä H. No evidence of trophic cascades in an experimentalmicrobial-based soil food web. Ecology 1998;79: 153-64.
Mitchell EAD. Pack hunting by minute soil testate amoebae: nematode hell is a naturalist's paradise. Environ Microbiol 2015;17:4145-7.
Monroy F, van der Putten WH, Yergeau E et al. Community patterns of soil bacteria and nematodes in relation to geographic distance. Soil Biol Biochem 2012;45:1-7.
Oberholster T, Vikram S, Cowan D et al. Keymicrobial taxa in the rhizosphere of sorghum and sunflower grown in crop rotation. Sci Total Environ 2018;624:530-9.
Oksanen J, Blanchet FG, FriendlyMet al. vegan: Community Ecology Package. R package version 2.5-5. URL: https://CRAN.R-project.o rg/package=vegan 2019.
Pawlowski J, Esling P, Lejzerowicz F et al. Environmental monitoring through protist next-generation sequencing metabarcoding: assessing the impact of fish farming on benthic foraminifera communities. Mol Ecol Resour 2014;14: 1129-40.
Prober SM, Leff JW, Bates ST et al. Plant diversity predicts beta but not alpha diversity of soilmicrobes across grasslands worldwide. Ecol Lett 2015;18:85-95.
Quast C, Pruesse E, Yilmaz P et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590-6.
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/ 2019.
Ramirez KS, Leff JW, Barber án A et al. Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally. Proc Biol Sci 2014;281:20141988.
Ratcliffe S, Bosman B, Carnol M. Spatial and temporal variability of biological indicators of soil quality in two forest catchments in Belgium. Appl Soil Ecol 2018;126: 148-59.
Rognes T, Flouri T, Nichols B et al. VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016;4:e2584.
Rösel S, Allgaier M, Grossart HP. Long-term characterization of free-living and particle-associated bacterial communities in lake tiefwaren reveals distinct seasonal patterns. Microb Ecol 2012;64:571-83.
Rousk J, Baath E, Brookes PC et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 2010;4:1340.
Shen C, Liang W, Shi Y et al. Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 2014;95:3190-202.
Shi Y, Xiang X, Shen C et al. Vegetation-associated impacts on Arctic tundra bacterial and microeukaryotic communities. Appl Environ Microb 2015;81:492-501.
Stoeck T, Bass D, Nebel M et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 2010;19:21-31.
Talbot JM, Bruns TD, Taylor JW et al. Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci 2014;111:6341-6.
Tedersoo L, Bahram M, Cajthaml T et al. Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 2016;10:346-62.
Tedersoo L, Bahram M, Polme S et al. Global diversity and geography of soil fungi. Science 2014;346:1256688.
Treseder KK, Maltz MR, Hawkins BA et al. Evolutionary histories of soil fungi are reflected in their large-scale biogeography. Ecol Lett 2014;17:1086-93.
Vedder B, Kampichler C, Bachmann G et al. Impact of faunal complexity on microbial biomass and N turnover in field mesocosms from a spruce forest soil. Biol Fertil Soils 1996;22: 22-30.
Yang F, Wu J, Zhang D et al. Soil bacterial community composition and diversity in relation to edaphic properties and plant traits in grasslands of southern China. Appl Soil Ecol 2018;128:43-53.
Yao H, Bowman D, Shi W. Seasonal variations of soil microbial biomass and activity inwarm-and cool-season turfgrass systems. Soil Biol Biochem 2011;43:1536-43.
Zhang J, Li M, Jia K et al. Seasonal variation rather than stand age determines bacterial diversity in the rhizosphere of wolfberry (Lycium barbarum L.) associated with soil degradation. J Soils Sediments 2018;18: 1518-29.
Zhou J, Deng Y, Shen L et al. Temperature mediates continentalscale diversity of microbes in forest soils. Nat Commun 2016;7:1-10.
Zhou J, Kang S, Schadt CW et al. Spatial scaling of functional gene diversity across various microbial taxa. Proc Natl Acad Sci 2008;105:7768-73.
Zinger L, Taberlet P, Schimann H et al. Body size determines soil community assembly in a tropical forest. Mol Ecol 2019;28:528-43.