Hierarchical phylogenetic community assembly of soil protists in a temperate agricultural field.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
27
06
2022
received:
12
01
2022
accepted:
09
07
2022
pubmed:
16
7
2022
medline:
19
11
2022
entrez:
15
7
2022
Statut:
ppublish
Résumé
Protists are abundant, diverse and perform essential functions in soils. Protistan community structure and its change across time or space are traditionally studied at the species level but the relative importance of the processes shaping these patterns depends on the taxon phylogenetic resolution. Using 18S rDNA amplicon data of the Cercozoa, a group of dominant soil protists, from an agricultural field in western Germany, we observed a turnover of relatively closely related taxa (from sequence variants to genus-level clades) across soil depth; while across soil habitats (rhizosphere, bulk soil, drilosphere), we observed turnover of relatively distantly related taxa, confirming Paracercomonadidae as a rhizosphere-associated clade. We extended our approach to show that closely related Cercozoa encounter divergent arbuscular mycorrhizal (AM) fungi across soil depth and that distantly related Cercozoa encounter closely related AM fungi across soil compartments. This study suggests that soil Cercozoa community assembly at the field scale is driven by niche-based processes shaped by evolutionary legacy of adaptation to conditions primarily related to the soil compartment, followed by the soil layer, giving a deeper understanding on the selection pressures that shaped their evolution.
Identifiants
pubmed: 35837871
doi: 10.1111/1462-2920.16134
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5498-5508Informations de copyright
© 2022 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Amend, A.S., Martiny, A.C., Allison, S.D., Berlemont, R., Goulden, M.L., Lu, Y. et al. (2016) Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. The ISME Journal, 10, 109-118.
Anderson, M.J. (2001) A new method for non parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
Bass, D., Howe, A.T., Mylnikov, A.P., Vickerman, K., Chao, E.E., Edwards Smallbone, J. et al. (2009) Phylogeny and classification of Cercomonadida (Protozoa, Cercozoa): Cercomonas, Eocercomonas, Paracercomonas, and Cavernomonas gen. nov. Protist, 160, 483-521.
Botnen, S.S., Davey, M.L., Halvorsen, R. & Kauserud, H. (2018) Sequence clustering threshold has little effect on the recovery of microbial community structure. Molecular Ecology Resources, 1, 13.
Burki, F., Roger, A.J., Brown, M.W. & Simpson, A.G.B. (2020) The new tree of eukaryotes. Trends in Ecology & Evolution, 35, 43-55.
Callahan, B.J., McMurdie, P.J. & Holmes, S.P. (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME Journal, 11, 2639-2643.
Callahan, B.J., Mcmurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J. & Holmes, S.P. (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581-583.
Caron, D.A. & Hu, S.K. (2018) Are we overestimating protistan diversity in nature ? Trends in Microbiology, 27, 197-205.
Cavender-Bares, J., Keen, A. & Miles, B. (2006) Phylogenetic structure of Floridian plant communities depends on taxonomic and spatial scale. Ecology, 87, S109-S122.
Chalmandrier, L., Münkemüller, T., Lavergne, S. & Thuiller, W. (2015) Effects of species' similarity and dominance on the functional and phylogenetic structure of a plant meta-community. Ecology, 96, 143-153.
Chalmandrier, L., Pansu, J., Zinger, L., Boyer, F., Coissac, E., Génin, A. et al. (2019) Environmental and biotic drivers of soil microbial β-diversity across spatial and phylogenetic scales. Ecography, 42, 1-13.
De Cáceres, M. & Legendre, P. (2009) Associations between species and groups of sites: indices and statistical inference. Ecology, 90, 3566-3574.
Degrune, F., Dumack, K., Fiore-Donno, A.M., Bonkowski, M., Sosa-Hernández, M.A., Schloter, M. et al. (2019) Distinct communities of Cercozoa at different soil depths in a temperate agricultural field. FEMS Microbiol Ecol, 95, 1-7.
Dumack, K., Fiore-Donno, A.M., Bass, D. & Bonkowski, M. (2020) Making sense of environmental sequencing data: ecologically important functional traits of the protistan groups Cercozoa and Endomyxa (Rhizaria). Molecular Ecology Resources, 20, 398-403.
Dumack, K., Pundta, J. & Bonkowski, M. (2018) Food choice experiments indicate selective Fungivorous predation in Fisculla terrestris (Thecofilosea, Cercozoa). J Eukaryot Microbiol E, 66, 525-527.
Fernández, L.D., Seppey, C.V.W., Singer, D., Fournier, B., Tatti, D., Mitchell, E.A.D. et al. (2022) Niche conservatism drives the Elevational diversity gradient in major groups of free-living soil unicellular eukaryotes. Microbial Ecology, 83, 459-469.
Fiore-Donno, A.M., Rixen, C., Rippin, M., Glaser, K., Samolov, E., Karsten, U. et al. (2018) New barcoded primers for efficient retrieval of cercozoan sequences in high-throughput environmental diversity surveys, with emphasis on worldwide biological soil crusts. Molecular Ecology Resources, 18, 229-239.
Flues, S., Blokker, M., Dumack, K. & Bonkowski, M. (2018) Diversity of Cercomonad species in the phyllosphere and rhizosphere of different plant species with a description of Neocercomonas epiphylla (Cercozoa, Rhizaria) a leaf-associated protist. The Journal of Eukaryotic Microbiology, 65, 587-599.
Geisen, S., Koller, R., Hünninghaus, M., Dumack, K., Urich, T. & Bonkowski, M. (2016) The soil food web revisited: diverse and widespread mycophagous soil protists. Soil Biology and Biochemistry, 94, 10-18.
Geisen, S., Mitchell, E.A.D., Adl, S., Bonkowski, M., Dunthorn, M., Ekelund, F. et al. (2018) Soil protists: a fertile frontier in soil biology research. FEMS Microbiology Reviews, 42, 293-323.
Geisen, S., Mitchell, E.A.D., Wilkinson, D.M., Adl, S., Bonkowski, M., Brown, M.W. et al. (2017) Soil protistology rebooted: 30 fundamental questions to start with. Soil Biology and Biochemistry, 111, 94-103.
Glassman, S.I. & Martiny, B.H. (2018) Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere, 3, 1-5.
Glücksman, E., Bell, T., Griffiths, R.I. & Bass, D. (2010) Closely related protist strains have different grazing impacts on natural bacterial communities. Environmental Microbiology, 12, 3105-3113.
Grossmann, L., Jensen, M., Heider, D., Jost, S., Glücksman, E., Hartikainen, H. et al. (2016) Protistan community analysis: key findings of a large-scale molecular sampling. The ISME Journal, 10, 2269-2279.
Groussin, M., Mazel, F., Sanders, J.G., Smillie, C.S., Lavergne, S., Thuiller, W. et al. (2017) Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nature Communications, 8, 1-12.
Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L. et al. (2013) The Protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Research, 41, 597-604.
Hart, M.M. & Reader, R.J. (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. The New Phytologist, 153, 335-344.
Henkes, G.J., Kandeler, E., Marhan, S., Scheu, S. & Bonkowski, M. (2018) Interactions of mycorrhiza and protists in the rhizosphere systemically alter microbial community composition, plant shoot-to-root ratio and within-root system nitrogen allocation. Front Environ Sci, 6, 117. https://doi.org/10.3389/fenvs.2018.00117
Howe, A.T., Bass, D., Scoble, J.M., Lewis, R., Vickerman, K., Arndt, H. et al. (2011) Novel cultured protists identify deep-branching environmental DNA clades of Cercozoa: new genera Tremula, Micrometopion, Minimassisteria, Nudifila, Peregrinia. Annals of Anatomy, 162, 332-372.
Hünninghaus, M., Dibbern, D., Kramer, S., Koller, R., Pausch, J., Schloter-Hai, B. et al. (2019) Disentangling carbon flow across microbial kingdoms in the rhizosphere of maize. Soil Biology and Biochemistry, 134, 122-130.
Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059-3066.
Legendre, P. & Legendre, L. (2012) Numerical ecology. Amsterdam: Elsevier Science BV.
Lekberg, Y., Gibbons, S.M. & Rosendahl, S. (2014) Will different OTU delineation methods change interpretation of arbuscular mycorrhizal fungal community patterns? New Phytology, 202, 1101-1104.
Lennon, J.T., Aanderud, Z.T., Lehmkuhl, B.K. & Schoolmaster, D.R. (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology, 93, 1867-1879.
Lentendu, G. & Dunthorn, M. (2021) Phylogenetic relatedness drives protist assembly in marine and terrestrial environments. Global Ecology and Biogeography, 30, 1532-1544.
Lu, H., Yeh, Y., Sastri, A.R., Shiah, F., Gong, G. & Hsieh, C. (2016) Evaluating community-environment relationships along fine to broad taxonomic resolutions reveals evolutionary forces underlying community assembly. The ISME Journal, 10, 2867-2878.
Martiny, A.C., Tai, A.P.K., Veneziano, D., Primeau, F. & Chisholm, S.W. (2009) Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environmental Microbiology, 11, 823-832.
Martiny, A.C., Treseder, K. & Pusch, G. (2013) Phylogenetic conservatism of functional traits in microorganisms. The ISME Journal, 7, 830-838.
Martiny, J.B.H., Jones, S.E., Lennon, J.T. & Martiny, A.C. (2015) Microbiomes in light of traits: a phylogenetic perspective. Science, 350, aac9323-1-aac9323-8.
Mazel, F., Malard, L., Niculita-Hirzel, H., Yashiro, E., Mod, H.K., Mitchell, E.A.D. et al. (2021) Soil protist function varies with elevation in the Swiss Alps. Environmental Microbiology, 24, 1689-1702. https://doi.org/10.1111/1462-2920.15686
Mazel, F., Wüest, R.O., Lessard, J.-P., Renaud, J., Ficetola, G.F., Lavergne, S. et al. (2017) Global patterns of β-diversity along the phylogenetic time-scale: the role of climate and plate tectonics. Global Ecology and Biogeography, 26, 1211-1221.
Mitchell, E.A.D., Lamentowicz, M., Payne, R.J. & Mazei, Y. (2014) Effect of taxonomic resolution on ecological and palaeoecological inference e a test using testate amoeba water table depth transfer functions. Quaternary Science Reviews, 91, 62-69.
Oksanen, J.F., Blanchet, G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D. et al. (2016) vegan: Community Ecology Package.
Oliverio, A.M., Geisen, S., Delgado-baquerizo, M., Maestre, F.T., Turner, B.L. & Fierer, N. (2020) The global-scale distributions of soil protists and their contributions to belowground systems. Science Advances, 6, 1-11.
Öztoprak, H., Walden, S., Heger, T., Bonkowski, M. & Dumack, K. (2020) What drives the diversity of the most abundant terrestrial Cercozoan family (Rhogostomidae, Cercozoa, Rhizaria)? Microorganisms, 8, 1-17.
Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290.
Pawlowski, J., Kelly-Quinn, M., Altermatt, F., Apothéloz-Perret-Gentil, L., Beja, P., Boggero, A. et al. (2018) The future of biotic indices in the ecogenomic era: integrating (e) DNA metabarcoding in biological assessment of aquatic ecosystems. Sci Total Environ, 637-638, 1295-1310.
Philippot, L., Andersson, S.G.E., Battin, T.J., Prosser, J.I., Schimel, J.P., Whitman, W.B. & Hallin, S. (2010) The ecological coherence of high bacterial taxonomic ranks. Nature Reviews Microbiology, 8, 523-529.
Pillon, Y., Alfonso, D., Herizo, G., Ii, P.P.L., Jaffré, T. & Merlot, S. (2019) Parallel ecological filtering of ultramafic soils in three distant Island floras. Journal of Biogeography, 46, 2457-2465.
Powell, J.R., Parrent, J.L., Hart, M.M., Klironomos, J.N., Rillig, M.C. & Maherali, H. (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc Biol Sci, 276, 4237-4245.
Powell, J.R. & Sikes, B.A. (2014) Method or madness: does OTU delineation bias our perceptions of fungal ecology? The New Phytologist, 202, 1095-1097.
Roy, J., Mazel, F., Sosa-Hernandez, A., Duenas, J.F., Hempel, S., Zinger, L. et al. (2019) The relative importance of ecological drivers of arbuscular mycorrhizal fungal distribution varies with taxon phylogenetic resolution. The New Phytologist, 224, 936-948.
Roy, J., van Duijnen, R., Leifheit, E.F., Mbedi, S., Temperton, V.M. & Rillig, M.C. (2021) Legacy effects of pre-crop plant functional group on fungal root symbionts of barley. Ecological Applications, 31, 1-16.
Rozmos, M., Bukovská, P., Hršelová, H., Kotianová, M., Dudáš, M., Gančarčíková, K. & Jansa, J. (2022) Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by speci fi c soil bacteria and a protist. ISME Journal, 16, 676-685.
Saladin, B., Thuiller, W., Graham, C.H., Lavergne, S., Maiorano, L., Salamin, N. et al. (2019) Environment and evolutionary history shape phylogenetic turnover in European tetrapods. Nature Communications, 10, 1-9.
Sapp, M., Ploch, S., Fiore-donno, A.M., Bonkowski, M. & Rose, L.E. (2018) Protists are an integral part of the Arabidopsis thaliana microbiome. Environmental Microbiology, 20, 30-43.
Simonin, M., Dasilva, C., Terzi, V., Ngonkeu, E.L.M., Diouf, D., Kane, A. et al. (2020) Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils. FEMS Microbiology Ecology, 96, 1-18.
Singer, D., Kosakyan, A., Seppey, C.V.W., Pillonel, A.M., Fernandez, L.D., Fontaneto, D. et al. (2018) Environmental filtering and phylogenetic clustering correlate with the distribution patterns of cryptic protist species. Ecology, 99, 904-914.
Sosa-Hernández, M.A., Roy, J., Hempel, S., Kautz, T., Köpke, U., Uksa, M. et al. (2018) Subsoil arbuscular mycorrhizal fungal communities in arable soil differ from those in topsoil. Soil Biology and Biochemistry, 117, 83-86.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313.
Uksa, M., Fischer, D., Welzl, G., Kautz, T., Köpke, U. & Schloter, M. (2018) Community structure of prokaryotes and their functional potential in subsoils is more affected by spatial heterogeneity than by temporal variations. Soil Biology and Biochemistry, 75, 197-201.
von Humboldt, A. & Bonpland, A. (1814) Voyage aux régions équinoxiales du nouveau monde. Paris: F. Schoell.
Wang, Q., Garrity, G.M., Tiedje, J.M. & Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 5261-5267.
Washburne, A.D., Silverman, J.D., Leff, J.W., Bennett, D.J., Darcy, J.L., Mukherjee, S. et al. (2017) Phylogenetic factorization of compositional data yields lineage-level associations in microbiome datasets. PeerJ, 5, e2969.