Soil pH mediates the balance between stochastic and deterministic assembly of bacteria

Tripathi, Binu M.; Stegen, James C.; Kim, Mincheol; Dong, Ke; Adams, Jonathan M.; Lee, Yoo Kyung

doi:10.1038/s41396-018-0082-4

Title: Soil pH mediates the balance between stochastic and deterministic assembly of bacteria

Journal Article · Wed Mar 07 00:00:00 EST 2018 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-018-0082-4· OSTI ID:1439021

Tripathi, Binu M.;

; Kim, Mincheol; Dong, Ke; Adams, Jonathan M.; Lee, Yoo Kyung

Little is known about the factors affecting the relative influence of stochastic and deterministic processes that governs the assembly of microbial communities in successional soils. Here, we conducted a meta-analysis of bacterial communities using six different successional soils data sets, scattered across different regions, with different pH conditions in early and late successional soils. We found that soil pH was the best predictor of bacterial community assembly and the relative importance of stochastic and deterministic processes along successional soils. Extreme acidic or alkaline pH conditions lead to assembly of phylogenetically more clustered bacterial communities through deterministic processes, whereas pH conditions close to neutral lead to phylogenetically less clustered bacterial communities with more stochasticity. We suggest that the influence of pH, rather than successional age, is the main driving force in producing trends in phylogenetic assembly of bacteria, and that pH also influences the relative balance of stochastic and deterministic processes along successional soils. Given that pH had a much stronger association with community assembly than did successional age, we evaluated whether the inferred influence of pH was maintained when studying globally-distributed samples collected without regard for successional age. This dataset confirmed the strong influence of pH, suggesting that the influence of soil pH on community assembly processes occurs globally. Extreme pH conditions likely exert more stringent limits on survival and fitness, imposing strong selective pressures through ecological and evolutionary time. Taken together, these findings suggest that the degree to which stochastic vs. deterministic processes shape soil bacterial community assembly is a consequence of soil pH rather than successional age.

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Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1439021

Report Number(s):: PNNL-SA-129633

Journal Information:: The ISME Journal, Vol. 12, Issue none; ISSN 1751-7362

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

References (54)

Species sorting and neutral processes are both important during the initial assembly of bacterial communities Langenheder, Silke; Székely, Anna J. The ISME Journal, Vol. 5, Issue 7 https://doi.org/10.1038/ismej.2010.207	journal	January 2011
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
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
Bacterial diversity in a glacier foreland of the high Arctic SchÜTte, Ursel M. E.; Abdo, Zaid; Foster, James Molecular Ecology, Vol. 19 https://doi.org/10.1111/j.1365-294X.2009.04479.x	journal	March 2010
The ecodist Package for Dissimilarity-based Analysis of Ecological Data Goslee, Sarah C.; Urban, Dean L. Journal of Statistical Software, Vol. 22, Issue 7 https://doi.org/10.18637/jss.v022.i07	journal	January 2007
Seed arrival and ecological filters interact to assemble high-diversity plant communities Myers, Jonathan A.; Harms, Kyle E. Ecology, Vol. 92, Issue 3 https://doi.org/10.1890/10-1001.1	journal	March 2011
PANDAseq: paired-end assembler for illumina sequences Masella, Andre P.; Bartram, Andrea K.; Truszkowski, Jakub M. BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-31	journal	January 2012
The merging of community ecology and phylogenetic biology Cavender-Bares, Jeannine; Kozak, Kenneth H.; Fine, Paul V. A. Ecology Letters, Vol. 12, Issue 7 https://doi.org/10.1111/j.1461-0248.2009.01314.x	journal	July 2009
Nitrogen fixation in different biogeochemical niches along a 120 000-year chronosequence in New Zealand Menge, Duncan N. L.; Hedin, Lars O. Ecology, Vol. 90, Issue 8 https://doi.org/10.1890/08-0877.1	journal	August 2009
Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons Williams, Mark A.; Jangid, Kamlesh; Shanmugam, Shankar G. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.08.023	journal	February 2013
Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes Wang, Jianjun; Shen, Ji; Wu, Yucheng The ISME Journal, Vol. 7, Issue 7 https://doi.org/10.1038/ismej.2013.30	journal	February 2013
Mechanisms of Maintenance of Species Diversity Chesson, Peter Annual Review of Ecology and Systematics, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.ecolsys.31.1.343	journal	November 2000
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
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale Lauber, C. L.; Hamady, M.; Knight, R. Applied and Environmental Microbiology, Vol. 75, Issue 15 https://doi.org/10.1128/AEM.00335-09	journal	June 2009
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Biogeochemical drivers of microbial community convergence across actively retreating glaciers Castle, Sarah C.; Nemergut, Diana R.; Grandy, A. Stuart Soil Biology and Biochemistry, Vol. 101 https://doi.org/10.1016/j.soilbio.2016.07.010	journal	October 2016
Phylogenies and Community Ecology Webb, Campbell O.; Ackerly, David D.; McPeek, Mark A. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.010802.150448	journal	November 2002
Testing the spatial phylogenetic structure of local communities: statistical performances of different null models and test statistics on a locally neutral community: Testing spatial community phylogenetic structure Hardy, Olivier J. Journal of Ecology, Vol. 96, Issue 5 https://doi.org/10.1111/j.1365-2745.2008.01421.x	journal	August 2008
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
Neutral theory and community ecology: Neutral theory and community ecology Chave, J. Ecology Letters, Vol. 7, Issue 3 https://doi.org/10.1111/j.1461-0248.2003.00566.x	journal	February 2004
Phylogenetic Clustering and Overdispersion in Bacterial Communities Horner-Devine, M. Claire; Bohannan, Brendan J. M. Ecology, Vol. 87, Issue sp7 https://doi.org/10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2	journal	July 2006
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
Disentangling the importance of ecological niches from stochastic processes across scales Chase, Jonathan M.; Myers, Jonathan A. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1576 https://doi.org/10.1098/rstb.2011.0063	journal	August 2011
Soil bacterial community succession during long-term ecosystem development Jangid, Kamlesh; Whitman, William B.; Condron, Leo M. Molecular Ecology, Vol. 22, Issue 12 https://doi.org/10.1111/mec.12325	journal	June 2013
Contrasting assembly processes in a bacterial metacommunity along a desiccation gradient Valverde, Angel; Makhalanyane, Thulani P.; Cowan, Don A. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00668	journal	December 2014
Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils Brown, Shawn P.; Jumpponen, Ari Molecular Ecology, Vol. 23, Issue 2 https://doi.org/10.1111/mec.12487	journal	September 2013
Drought mediates the importance of stochastic community assembly Chase, J. M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 44 https://doi.org/10.1073/pnas.0704350104	journal	October 2007
How to model species responses along ecological gradients - Huisman-Olff-Fresco models revisited Jansen, Florian; Oksanen, Jari Journal of Vegetation Science, Vol. 24, Issue 6 https://doi.org/10.1111/jvs.12050	journal	February 2013
Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning Dini-Andreote, Francisco; de Cássia Pereira e. Silva, Michele; Triadó-Margarit, Xavier The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.54	journal	April 2014
Stochasticity, succession, and environmental perturbations in a fluidic ecosystem Zhou, Jizhong; Deng, Ye; Zhang, Ping Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1324044111	journal	February 2014
Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform Schirmer, Melanie; Ijaz, Umer Z.; D'Amore, Rosalinda Nucleic Acids Research, Vol. 43, Issue 6 https://doi.org/10.1093/nar/gku1341	journal	January 2015
Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities Fine, Paul V. A.; Kembel, Steven W. Ecography, Vol. 34, Issue 4 https://doi.org/10.1111/j.1600-0587.2010.06548.x	journal	August 2011
Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield Rime, Thomas; Hartmann, Martin; Brunner, Ivano Molecular Ecology, Vol. 24, Issue 5 https://doi.org/10.1111/mec.13051	journal	January 2015
Soil bacterial and fungal communities across a pH gradient in an arable soil Rousk, Johannes; Bååth, Erland; Brookes, Philip C. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.58	journal	May 2010
Theory predicts a rapid transition from niche-structured to neutral biodiversity patterns across a speciation-rate gradient Chisholm, Ryan A.; Pacala, Stephen W. Theoretical Ecology, Vol. 4, Issue 2 https://doi.org/10.1007/s12080-011-0113-5	journal	February 2011
The bacterial biogeography of British soils: Mapping soil bacteria Griffiths, Robert I.; Thomson, Bruce C.; James, Phillip Environmental Microbiology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1462-2920.2011.02480.x	journal	April 2011
A hierarchical set of models for species response analysis Huisman, J.; Olff, H.; Fresco, L. F. M. Journal of Vegetation Science, Vol. 4, Issue 1 https://doi.org/10.2307/3235732	journal	February 1993
Evolution of carbon fluxes during initial soil formation along the forefield of Damma glacier, Switzerland Guelland, K.; Hagedorn, F.; Smittenberg, R. H. Biogeochemistry, Vol. 113, Issue 1-3 https://doi.org/10.1007/s10533-012-9785-1	journal	September 2012
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
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
Changes in assembly processes in soil bacterial communities following a wildfire disturbance Ferrenberg, Scott; O'Neill, Sean P.; Knelman, Joseph E. The ISME Journal, Vol. 7, Issue 6 https://doi.org/10.1038/ismej.2013.11	journal	February 2013
Spatial Scaling Effects on Soil Bacterial Communities in Malaysian Tropical Forests Tripathi, Binu M.; Lee-Cruz, Larisa; Kim, Mincheol Microbial Ecology, Vol. 68, Issue 2 https://doi.org/10.1007/s00248-014-0404-7	journal	March 2014
Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes: Bacterial biogeography in arctic soils Chu, Haiyan; Fierer, Noah; Lauber, Christian L. Environmental Microbiology, Vol. 12, Issue 11 https://doi.org/10.1111/j.1462-2920.2010.02277.x	journal	November 2010
Tropical Soil Bacterial Communities in Malaysia: pH Dominates in the Equatorial Tropics Too Tripathi, Binu M.; Kim, Mincheol; Singh, Dharmesh Microbial Ecology, Vol. 64, Issue 2 https://doi.org/10.1007/s00248-012-0028-8	journal	February 2012
Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Losos, Jonathan B. Ecology Letters, Vol. 11, Issue 10 https://doi.org/10.1111/j.1461-0248.2008.01229.x	journal	October 2008
Soil Organic Phosphorus Transformations During Pedogenesis Turner, Benjamin L.; Condron, Leo M.; Richardson, Sarah J. Ecosystems, Vol. 10, Issue 7 https://doi.org/10.1007/s10021-007-9086-z	journal	October 2007
Communities contain closely related species during ecosystem disturbance Helmus, Matthew R.; Keller, Wendel (Bill); Paterson, Michael J. Ecology Letters, Vol. 13, Issue 2 https://doi.org/10.1111/j.1461-0248.2009.01411.x	journal	February 2010
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Shifts in bacterial community structure during succession in a glacier foreland of the High Arctic Kim, Mincheol; Jung, Ji Young; Laffly, Dominique FEMS Microbiology Ecology, Vol. 93, Issue 1 https://doi.org/10.1093/femsec/fiw213	journal	October 2016
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
Community assembly and invasion: An experimental test of neutral versus niche processes Fargione, J.; Brown, C. S.; Tilman, D. Proceedings of the National Academy of Sciences, Vol. 100, Issue 15 https://doi.org/10.1073/pnas.1033107100	journal	July 2003
Phylogenetic diversity analyses reveal disparity between fungal and bacterial communities during microbial primary succession Brown, Shawn P.; Jumpponen, Ari Soil Biology and Biochemistry, Vol. 89 https://doi.org/10.1016/j.soilbio.2015.06.025	journal	October 2015
Effects of dispersal and selection on stochastic assembly in microbial communities Evans, Sarah; Martiny, Jennifer B. H.; Allison, Steven D. The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.96	journal	August 2016
Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea Herlemann, Daniel PR; Labrenz, Matthias; Jürgens, Klaus The ISME Journal, Vol. 5, Issue 10 https://doi.org/10.1038/ismej.2011.41	journal	April 2011

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