The ecological assembly of bacterial communities in Antarctic wetlands varies across levels of phylogenetic resolution

Quiroga, María V.; Valverde, Angel; Mataloni, Gabriela; Casa, Valeria; Stegen, James C.; Cowan, Don

doi:10.1111/1462-2920.15912

Title: The ecological assembly of bacterial communities in Antarctic wetlands varies across levels of phylogenetic resolution

Journal Article · 27 January 2022 · Environmental Microbiology

DOI: https://doi.org/10.1111/1462-2920.15912 · OSTI ID:1868396

^[1];

^[2]; Mataloni, Gabriela ^[3]; Casa, Valeria ^[3]; Stegen, James C. ^[4]; Cowan, Don ^[5]

Instituto Tecnológico de Chascomús (INTECH, UNSAM – CONICET) Chascomús Argentina
Instituto de Recursos Naturales y Agrobiología de Salamanca (IRNASA‐CSIC) Consejo Superior de Investigaciones Científicas Salamanca Spain
Instituto de Investigación e Ingeniería Ambiental (IIIA, UNSAM‐CONICET), San Martín Buenos Aires Argentina
Pacific Northwest National Laboratory Ecosystem Science Team Richland WA
Centre for Microbial Ecology and Genomics (CMEG), Department of Biochemistry, Genetics and Microbiology University of Pretoria Pretoria South Africa

Summary As functional traits are conserved at different phylogenetic depths, the ability to detect community assembly processes can be conditional on the phylogenetic resolution; yet most previous work quantifying their influence has focused on a single level of phylogenetic resolution. Here, we have studied the ecological assembly of bacterial communities from an Antarctic wetland complex, applying null models across different levels of phylogenetic resolution (i.e. clustering ASVs into OTUs with decreasing sequence identity thresholds). We found that the relative influence of the community assembly processes varies with phylogenetic resolution. More specifically, selection processes seem to impose stronger influence at finer (100% sequence similarity ASV) than at coarser (99%–97% sequence similarity OTUs) resolution. We identified environmental features related with the ecological processes and propose a conceptual model for the bacterial community assembly in this Antarctic ecosystem. Briefly, eco‐evolutionary processes appear to be leading to different but very closely related ASVs in lotic, lentic and terrestrial environments. In all, this study shows that assessing community assembly processes at different phylogenetic resolutions is key to improve our understanding of microbial ecology. More importantly, a failure to detect selection processes at coarser phylogenetic resolution does not imply the absence of such processes at finer resolutions.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1868396

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 8 Vol. 24; ISSN 1462-2912

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (63)

Short-term analysis of the phytoplankton structure and dynamics in two ponds with distinct trophic states from Cierva Point (maritime Antarctica) Allende, Luz; Mataloni, Gabriela Polar Biology, Vol. 36, Issue 5 https://doi.org/10.1007/s00300-013-1290-z	journal	February 2013
Potential Use of a Poultry Manure Digestate as a Biofertiliser: Evaluation of Soil Properties and Lactuca sativa Growth Mortola, Natalia; Romaniuk, Romina; Cosentino, Vanina Pedosphere, Vol. 29, Issue 1 https://doi.org/10.1016/S1002-0160(18)60057-8	journal	February 2019
Properties and processes of recently established soils from deglaciation of Cierva Point, Western Antarctic Peninsula Wilhelm, Kelly R.; Bockheim, James G.; Haus, Nicholas W. Geoderma, Vol. 277 https://doi.org/10.1016/j.geoderma.2016.05.001	journal	September 2016
What shapes edaphic communities in mineral and ornithogenic soils of Cierva Point, Antarctic Peninsula? Mataloni, G.; Garraza, G. González; Bölter, M. Polar Science, Vol. 4, Issue 2 https://doi.org/10.1016/j.polar.2010.04.005	journal	August 2010
Past and future species definitions for Bacteria and Archaea Rosselló-Móra, Ramon; Amann, Rudolf Systematic and Applied Microbiology, Vol. 38, Issue 4 https://doi.org/10.1016/j.syapm.2015.02.001	journal	June 2015
Does Intraspecific Variation in rDNA Copy Number Affect Analysis of Microbial Communities? Lavrinienko, Anton; Jernfors, Toni; Koskimäki, Janne J. Trends in Microbiology, Vol. 29, Issue 1 https://doi.org/10.1016/j.tim.2020.05.019	journal	January 2021
Abiotic characterization and epilithic communities of a naturally enriched stream at Cierva Point, Antarctic Peninsula Mataloni, Gabriela; Vinocur, Alicia; de TEZANOS PINTO, Paula Antarctic Science, Vol. 17, Issue 2 https://doi.org/10.1017/S0954102005002579	journal	June 2005
Stochastic and deterministic assembly processes in subsurface microbial communities Stegen, James C.; Lin, Xueju; Konopka, Allan E. The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.22	journal	March 2012
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Bacterial genome replication at subzero temperatures in permafrost Tuorto, Steven J.; Darias, Phillip; McGuinness, Lora R. The ISME Journal, Vol. 8, Issue 1 https://doi.org/10.1038/ismej.2013.140	journal	August 2013
Quantifying community assembly processes and identifying features that impose them Stegen, James C.; Lin, Xueju; Fredrickson, Jim K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.93	journal	June 2013
Evaluating community–environment relationships along fine to broad taxonomic resolutions reveals evolutionary forces underlying community assembly Lu, Hsiao-Pei; Yeh, Yi-Chun; Sastri, Akash R. The ISME Journal, Vol. 10, Issue 12 https://doi.org/10.1038/ismej.2016.78	journal	May 2016
Exact sequence variants should replace operational taxonomic units in marker-gene data analysis Callahan, Benjamin J.; McMurdie, Paul J.; Holmes, Susan P. The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.119	journal	July 2017
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Beyond biogeographic patterns: processes shaping the microbial landscape Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire Nature Reviews Microbiology, Vol. 10, Issue 7 https://doi.org/10.1038/nrmicro2795	journal	May 2012
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar Nature Reviews Microbiology, Vol. 12, Issue 9 https://doi.org/10.1038/nrmicro3330	journal	August 2014
Microbial ecology of Antarctic aquatic systems Cavicchioli, Ricardo Nature Reviews Microbiology, Vol. 13, Issue 11 https://doi.org/10.1038/nrmicro3549	journal	October 2015
Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions García-García, Natalia; Tamames, Javier; Linz, Alexandra M. The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0487-8	journal	August 2019
Environmental heterogeneity determines the ecological processes that govern bacterial metacommunity assembly in a floodplain river system Huber, Paula; Metz, Sebastian; Unrein, Fernando The ISME Journal, Vol. 14, Issue 12 https://doi.org/10.1038/s41396-020-0723-2	journal	July 2020
A large-scale assessment of lakes reveals a pervasive signal of land use on bacterial communities Kraemer, S. A.; Barbosa da Costa, N.; Shapiro, B. J. The ISME Journal, Vol. 14, Issue 12 https://doi.org/10.1038/s41396-020-0733-0	journal	August 2020
Microdiversity characterizes prevalent phylogenetic clades in the glacier-fed stream microbiome Fodelianakis, Stilianos; Washburne, Alex D.; Bourquin, Massimo The ISME Journal https://doi.org/10.1038/s41396-021-01106-6	journal	September 2021
A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming Ning, Daliang; Yuan, Mengting; Wu, Linwei Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18560-z	journal	September 2020
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Habitat heterogeneity and connectivity shape microbial communities in South American peatlands Oloo, Felix; Valverde, Angel; Quiroga, María Victoria Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25712	journal	May 2016
Phosphate acquisition genes in Prochlorococcus ecotypes: Evidence for genome-wide adaptation Martiny, A. C.; Coleman, M. L.; Chisholm, S. W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 33 https://doi.org/10.1073/pnas.0601301103	journal	August 2006
Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession Dini-Andreote, Francisco; Stegen, James C.; van Elsas, Jan Dirk Proceedings of the National Academy of Sciences, Vol. 112, Issue 11 https://doi.org/10.1073/pnas.1414261112	journal	March 2015
Adaptive differentiation and rapid evolution of a soil bacterium along a climate gradient Chase, Alexander B.; Weihe, Claudia; Martiny, Jennifer B. H. Proceedings of the National Academy of Sciences, Vol. 118, Issue 18 https://doi.org/10.1073/pnas.2101254118	journal	April 2021
Bacterial Species and Speciation Cohan, Frederick M. Systematic Biology, Vol. 50, Issue 4 https://doi.org/10.1080/10635150118398	journal	August 2001
Conceptual Synthesis in Community Ecology Vellend, Mark The Quarterly Review of Biology, Vol. 85, Issue 2 https://doi.org/10.1086/652373	journal	June 2010
Implications of Subzero Metabolic Activity on Long-Term Microbial Survival in Terrestrial and Extraterrestrial Permafrost Amato, Pierre; Doyle, Shawn M.; Battista, John R. Astrobiology, Vol. 10, Issue 8 https://doi.org/10.1089/ast.2010.0477	journal	October 2010
Picante: R tools for integrating phylogenies and ecology Kembel, S. W.; Cowan, P. D.; Helmus, M. R. Bioinformatics, Vol. 26, Issue 11 https://doi.org/10.1093/bioinformatics/btq166	journal	April 2010
Updating the 97% identity threshold for 16S ribosomal RNA OTUs Edgar, Robert C. Bioinformatics, Vol. 34, Issue 14 https://doi.org/10.1093/bioinformatics/bty113	journal	February 2018
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
Reconciliation between operational taxonomic units and species boundaries Mysara, Mohamed; Vandamme, Peter; Props, Ruben FEMS Microbiology Ecology, Vol. 93, Issue 4 https://doi.org/10.1093/femsec/fix029	journal	March 2017
Interplay between stochastic and deterministic processes in the maintenance of alternative community states in Verrucomicrobia-dominated shallow lakes Llames, Maria E.; Huber, Paula; Metz, Sebastián FEMS Microbiology Ecology, Vol. 93, Issue 7 https://doi.org/10.1093/femsec/fix077	journal	June 2017
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy Nucleic Acids Research, Vol. 41, Issue 1 https://doi.org/10.1093/nar/gks808	journal	August 2012
Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes Logares, Ramiro; Tesson, Sylvie V. M.; Canbäck, Björn Environmental Microbiology, Vol. 20, Issue 6 https://doi.org/10.1111/1462-2920.14265	journal	June 2018
Distinct assembly mechanisms underlie similar biogeographical patterns of rare and abundant bacteria in Tibetan Plateau grassland soils Ji, Mukan; Kong, Weidong; Stegen, James Environmental Microbiology, Vol. 22, Issue 6 https://doi.org/10.1111/1462-2920.14993	journal	April 2020
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY Anderson, Marti J. Austral Ecology, Vol. 26, Issue 1 https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x	journal	February 2001
The metacommunity concept: a framework for multi-scale community ecology: The metacommunity concept Leibold, M. A.; Holyoak, M.; Mouquet, N. Ecology Letters, Vol. 7, Issue 7 https://doi.org/10.1111/j.1461-0248.2004.00608.x	journal	June 2004
Distance-Based Tests for Homogeneity of Multivariate Dispersions Anderson, Marti J. Biometrics, Vol. 62, Issue 1 https://doi.org/10.1111/j.1541-0420.2005.00440.x	journal	October 2005
Local and regional factors influencing bacterial community assembly: Bacterial community assembly Lindström, Eva S.; Langenheder, Silke Environmental Microbiology Reports, Vol. 4, Issue 1 https://doi.org/10.1111/j.1758-2229.2011.00257.x	journal	April 2011
Homogeneous environmental selection dominates microbial community assembly in the oligotrophic South Pacific Gyre Allen, Ro; Hoffmann, Linn J.; Larcombe, Matthew J. Molecular Ecology, Vol. 29, Issue 23 https://doi.org/10.1111/mec.15651	journal	October 2020
The relative importance of ecological drivers of arbuscular mycorrhizal fungal distribution varies with taxon phylogenetic resolution Roy, Julien; Mazel, Florent; Sosa‐Hernández, Moisés A. New Phytologist, Vol. 224, Issue 2 https://doi.org/10.1111/nph.16080	journal	September 2019
Assessing the relative importance of neutral stochasticity in ecological communities Vellend, Mark; Srivastava, Diane S.; Anderson, Kathryn M. Oikos, Vol. 123, Issue 12 https://doi.org/10.1111/oik.01493	journal	September 2014
Microbiomes in light of traits: A phylogenetic perspective Martiny, J. B. H.; Jones, S. E.; Lennon, J. T. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aac9323	journal	November 2015
Stochastic Community Assembly: Does It Matter in Microbial Ecology? Zhou, Jizhong; Ning, Daliang Microbiology and Molecular Biology Reviews, Vol. 81, Issue 4 https://doi.org/10.1128/MMBR.00002-17	journal	October 2017
Patterns and Processes of Microbial Community Assembly Nemergut, D. R.; Schmidt, S. K.; Fukami, T. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3 https://doi.org/10.1128/MMBR.00051-12	journal	September 2013
Status of the Microbial Census Schloss, P. D.; Handelsman, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/MMBR.68.4.686-691.2004	journal	December 2004
Ecological Assembly Processes Are Coordinated between Bacterial and Viral Communities in Fractured Shale Ecosystems Danczak, R. E.; Daly, R. A.; Borton, M. A. mSystems, Vol. 5, Issue 2 https://doi.org/10.1128/mSystems.00098-20	journal	March 2020
Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems Paver, Sara F.; Muratore, Daniel; Newton, Ryan J. mSystems, Vol. 3, Issue 6 https://doi.org/10.1128/mSystems.00232-18	journal	October 2018
Disentangling the mechanisms shaping the surface ocean microbiota Logares, Ramiro; Deutschmann, Ina M.; Junger, Pedro C. Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00827-8	journal	April 2020
Microdiversity and phylogeographic diversification of bacterioplankton in pelagic freshwater systems revealed through long-read amplicon sequencing Okazaki, Yusuke; Fujinaga, Shohei; Salcher, Michaela M. Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00974-y	journal	January 2021
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
The Theory of Ecological Communities (MPB-57) Vellend, Mark https://doi.org/10.1515/9781400883790	book	September 2016
The Problem and Promise of Scale Dependency in Community Phylogenetics Swenson, Nathan G.; Enquist, Brian J.; Pither, Jason Ecology, Vol. 87, Issue 10 https://doi.org/10.1890/0012-9658(2006)87[2418:TPAPOS]2.0.CO;2	journal	October 2006
Defining Pathogenic Bacterial Species in the Genomic Era Georgiades, Kalliopi; Raoult, Didier Frontiers in Microbiology, Vol. 1 https://doi.org/10.3389/fmicb.2010.00151	journal	January 2011
Protection of Antarctic microbial communities â€“ â€˜out of sight, out of mindâ€™ Hughes, Kevin A.; Cowan, Don A.; Wilmotte, Annick Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00151	journal	February 2015
Estimating and mapping ecological processes influencing microbial community assembly Stegen, James C.; Lin, Xueju; Fredrickson, Jim K. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00370	journal	May 2015
Abundance and breeding distribution of seabirds in the northern part of the Danco Coast, Antarctic Peninsula González-Zevallos, Diego; Santos, MaríaM.; Rombolá, EmilceF. Polar Research, Vol. 32, Issue 1 https://doi.org/10.3402/polar.v32i0.11133	journal	January 2013
Pan-Antarctic map of near-surface permafrost temperatures at 1 km² scale Obu, Jaroslav; Westermann, Sebastian; Vieira, Gonçalo The Cryosphere, Vol. 14, Issue 2 https://doi.org/10.5194/tc-14-497-2020	journal	January 2020

Similar Records

Microdiverse bacterial clades prevail across Antarctic wetlands

Journal Article · 2023 · Molecular Ecology · OSTI ID:2328510

Quiroga, María Victoria; Stegen, James C.; Mataloni, Gabriela; +3 more

High-resolution phylogenetic microbial community profiling

Conference · 2014 · OSTI ID:1241181

Singer, Esther; Coleman-Derr, Devin; Bowman, Brett; +9 more

Long-term nitrogen addition affects the phylogenetic turnover of soil microbial community responding to moisture pulse

Journal Article · 2017 · Scientific Reports · OSTI ID:1430531

Liu, Chi; Yao, Minjie; Stegen, James C.; +3 more

Title: The ecological assembly of bacterial communities in Antarctic wetlands varies across levels of phylogenetic resolution

Citation Formats

References (63)

Similar Records

Related Subjects