Nitrogen enrichment suppresses other environmental drivers and homogenizes salt marsh leaf microbiome

Daleo, Pedro; Alberti, Juan; Jumpponen, Ari; Veach, Allison M.; Ialonardi, Florencia; Iribarne, Oscar; Silliman, Brian

doi:10.1002/ecy.2240

Title: Nitrogen enrichment suppresses other environmental drivers and homogenizes salt marsh leaf microbiome

Journal Article · Thu Apr 12 00:00:00 EDT 2018 · Ecology

DOI:https://doi.org/10.1002/ecy.2240· OSTI ID:1456792

^[1]; Alberti, Juan ^[1]; Jumpponen, Ari ^[2];

^[3]; Ialonardi, Florencia ^[1]; Iribarne, Oscar ^[1]; Silliman, Brian ^[4]

Instituto de Investigaciones Marinas y Costeras (Argentina)
Kansas State Univ., Manhattan, KS (United States)
Kansas State Univ., Manhattan, KS (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Duke Univ., Beaufort, NC (United States)

Microbial community assembly is affected by a combination of forces that act simultaneously, but the mechanisms underpinning their relative influences remain elusive. This gap strongly limits our ability to predict human impacts on microbial communities and the processes they regulate. Here, we experimentally demonstrate that increased salinity stress, food web alteration and nutrient loading interact to drive outcomes in salt marsh fungal leaf communities. Both salinity stress and food web alterations drove communities to deterministically diverge, resulting in distinct fungal communities. Increased nutrient loads, nevertheless, partially suppressed the influence of other factors as determinants of fungal assembly. Using a null model approach, we found that increased nutrient loads enhanced the relative importance of stochastic over deterministic divergent processes; without increased nutrient loads, samples from different treatments showed a relatively (deterministic) divergent community assembly whereas increased nutrient loads drove the system to more stochastic assemblies, suppressing the effect of other treatments. These results demonstrate that common anthropogenic modifications can interact to control fungal community assembly. As a result, our results suggest that when the environmental conditions are spatially heterogeneous (as in our case, caused by specific combinations of experimental treatments), increased stochasticity caused by greater nutrient inputs can reduce the importance of deterministic filters that otherwise caused divergence, thus driving to microbial community homogenization.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1456792

Journal Information:: Ecology, Vol. 99, Issue 6; ISSN 0012-9658

Publisher:: Ecological Society of America (ESA)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 8 works

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References (68)

Stochastic Assembly Leads to Alternative Communities with Distinct Functions in a Bioreactor Microbial Community Zhou, Jizhong; Liu, Wenzong; Deng, Ye mBio, Vol. 4, Issue 2 https://doi.org/10.1128/mBio.00584-12	journal	March 2013
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
Microbial diversity in the deep sea and the underexplored "rare biosphere" Sogin, M. L.; Morrison, H. G.; Huber, J. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 32 https://doi.org/10.1073/pnas.0605127103	journal	July 2006
Using null models to disentangle variation in community dissimilarity from variation in α-diversity Chase, Jonathan M.; Kraft, Nathan J. B.; Smith, Kevin G. Ecosphere, Vol. 2, Issue 2 https://doi.org/10.1890/ES10-00117.1	journal	February 2011
Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation Browne, Hilary P.; Forster, Samuel C.; Anonye, Blessing O. Nature, Vol. 533, Issue 7604 https://doi.org/10.1038/nature17645	journal	May 2016
Coexistence of the Niche and Neutral Perspectives in Community Ecology Leibold, Mathew A.; McPeek, Mark A. Ecology, Vol. 87, Issue 6 https://doi.org/10.1890/0012-9658(2006)87[1399:COTNAN]2.0.CO;2	journal	June 2006
Physical stress modifies top-down and bottom-up forcing on plant growth and reproduction in a coastal ecosystem Daleo, Pedro; Alberti, Juan; Bruschetti, Carlos Martín Ecology, Vol. 96, Issue 8 https://doi.org/10.1890/14-1776.1	journal	August 2015
The Ubiquity of Small Species: Patterns of Local and Global Diversity Fenchel, Tom; Finlay, Bland J. BioScience, Vol. 54, Issue 8 https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2	journal	January 2004
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
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Herbivore exclusion promotes a more stochastic plant community assembly in a natural grassland Alberti, Juan; Bakker, Elisabeth S.; van Klink, Roel Ecology, Vol. 98, Issue 4 https://doi.org/10.1002/ecy.1741	journal	March 2017
Patterns of fungal diversity and composition along a salinity gradient Mohamed, Devon J.; Martiny, Jennifer BH The ISME Journal, Vol. 5, Issue 3 https://doi.org/10.1038/ismej.2010.137	journal	September 2010
Ironing out the wrinkles in the rare biosphere through improved OTU clustering: Ironing out the wrinkles in the rare biosphere Huse, Susan M.; Welch, David Mark; Morrison, Hilary G. Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02193.x	journal	March 2010
Resistance, resilience, and redundancy in microbial communities Allison, S. D.; Martiny, J. B. H. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0801925105	journal	August 2008
The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters Abarenkov, Kessy; Henrik Nilsson, R.; Larsson, Karl-Henrik New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03160.x	journal	March 2010
Competition, Not Cooperation, Dominates Interactions among Culturable Microbial Species Foster, Kevin R.; Bell, Thomas Current Biology, Vol. 22, Issue 19 https://doi.org/10.1016/j.cub.2012.08.005	journal	October 2012
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
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
Pyrosequencing enumerates and contrasts soil microbial diversity Roesch, Luiz F. W.; Fulthorpe, Roberta R.; Riva, Alberto The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.53	journal	July 2007
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
Herbivores and nutrients control grassland plant diversity via light limitation Borer, Elizabeth T.; Seabloom, Eric W.; Gruner, Daniel S. Nature, Vol. 508, Issue 7497 https://doi.org/10.1038/nature13144	journal	March 2014
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn FEMS Microbiology Ecology, Vol. 82, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01437.x	journal	July 2012
Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning Maherali, H.; Klironomos, J. N. Science, Vol. 316, Issue 5832 https://doi.org/10.1126/science.1143082	journal	June 2007
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
Analysis of Internal Transcribed Spacer (ITS) Regions of rRNA Genes in Fungal Communities in a Southeastern U.S. Salt Marsh Buchan, A.; Newell, S. Y.; Moreta, J. I. L. Microbial Ecology, Vol. 43, Issue 3 https://doi.org/10.1007/s00248-001-1062-0	journal	May 2002
Multivariate dispersion as a measure of beta diversity Anderson, Marti J.; Ellingsen, Kari E.; McArdle, Brian H. Ecology Letters, Vol. 9, Issue 6 https://doi.org/10.1111/j.1461-0248.2006.00926.x	journal	June 2006
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
Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities Siciliano, Steven D.; Palmer, Anne S.; Winsley, Tristrom Soil Biology and Biochemistry, Vol. 78 https://doi.org/10.1016/j.soilbio.2014.07.005	journal	November 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
Stochastic Community Assembly Causes Higher Biodiversity in More Productive Environments Chase, J. M. Science, Vol. 328, Issue 5984 https://doi.org/10.1126/science.1187820	journal	May 2010
Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally Ramirez, Kelly S.; Leff, Jonathan W.; Barberán, Albert Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1795 https://doi.org/10.1098/rspb.2014.1988	journal	November 2014
A Comparison of some methods for analysing changes in benthic community structure Warwick, R. M.; Clarke, K. R. Journal of the Marine Biological Association of the United Kingdom, Vol. 71, Issue 1 https://doi.org/10.1017/S0025315400037528	journal	February 1991
Combined niche and neutral effects in a microbial wastewater treatment community Ofiteru, I. D.; Lunn, M.; Curtis, T. P. Proceedings of the National Academy of Sciences, Vol. 107, Issue 35 https://doi.org/10.1073/pnas.1000604107	journal	August 2010
The role of ecological theory in microbial ecology Prosser, James I.; Bohannan, Brendan J. M.; Curtis, Tom P. Nature Reviews Microbiology, Vol. 5, Issue 5 https://doi.org/10.1038/nrmicro1643	journal	May 2007
Neutral assembly of bacterial communities: Neutral assembly of bacterial communities Woodcock, Stephen; Van Der Gast, Christopher J.; Bell, Thomas FEMS Microbiology Ecology, Vol. 62, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00379.x	journal	November 2007
Effects of nutrient enrichment and crab herbivory on a SW Atlantic salt marsh productivity Alberti, Juan; Cebrian, Just; Casariego, Agustina Méndez Journal of Experimental Marine Biology and Ecology, Vol. 405, Issue 1-2 https://doi.org/10.1016/j.jembe.2011.05.023	journal	August 2011
Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments Jumpponen, A.; Jones, K. L. New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03197.x	journal	February 2010
Increasing aridity reduces soil microbial diversity and abundance in global drylands Maestre, Fernando T.; Delgado-Baquerizo, Manuel; Jeffries, Thomas C. Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1516684112	journal	December 2015
The ecology of the microbiome: Networks, competition, and stability Coyte, K. Z.; Schluter, J.; Foster, K. R. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aad2602	journal	November 2015
Competition for Light Causes Plant Biodiversity Loss After Eutrophication Hautier, Y.; Niklaus, P. A.; Hector, A. Science, Vol. 324, Issue 5927 https://doi.org/10.1126/science.1169640	journal	April 2009
Stochastic assembly produces heterogeneous communities in the Caenorhabditis elegans intestine Vega, Nicole M.; Gore, Jeff PLOS Biology, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pbio.2000633	journal	March 2017
Dispersal enhances beta diversity in nectar microbes Vannette, Rachel L.; Fukami, Tadashi Ecology Letters, Vol. 20, Issue 7 https://doi.org/10.1111/ele.12787	journal	June 2017
'Everything is everywhere, but, the environment selects'; what did Baas Becking and Beijerinck really say? de Wit, Rutger; Bouvier, Thierry Environmental Microbiology, Vol. 8, Issue 4 https://doi.org/10.1111/j.1462-2920.2006.01017.x	journal	April 2006
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
Bacterial diversity and community composition from seasurface to subseafloor Walsh, Emily A.; Kirkpatrick, John B.; Rutherford, Scott D. The ISME Journal, Vol. 10, Issue 4 https://doi.org/10.1038/ismej.2015.175	journal	October 2015
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
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
Challenges in microbial ecology: building predictive understanding of community function and dynamics Widder, Stefanie; Allen, Rosalind J.; Pfeiffer, Thomas The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.45	journal	March 2016
Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi Schoch, C. L.; Seifert, K. A.; Huhndorf, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1117018109	journal	March 2012
454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases Tedersoo, Leho; Nilsson, R. Henrik; Abarenkov, Kessy New Phytologist, Vol. 188, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03373.x	journal	July 2010
Dispersal alters bacterial diversity and composition in a natural community Albright, Michaeline B. N.; Martiny, Jennifer B. H. The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.161	journal	October 2017
ENSO episodes modify plant/terrestrial–herbivore interactions in a southwestern Atlantic salt marsh Canepuccia, Alejandro D.; Alberti, Juan; Pascual, Jesus Journal of Experimental Marine Biology and Ecology, Vol. 396, Issue 1 https://doi.org/10.1016/j.jembe.2010.09.013	journal	December 2010
Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh Alberti, Juan; Méndez Casariego, Agustina; Daleo, Pedro Oecologia, Vol. 163, Issue 1 https://doi.org/10.1007/s00442-009-1504-9	journal	November 2009
Grazer facilitation of fungal infection and the control of plant growth in south-western Atlantic salt marshes Daleo, Pedro; Silliman, Brian; Alberti, Juan Journal of Ecology, Vol. 97, Issue 4 https://doi.org/10.1111/j.1365-2745.2009.01508.x	journal	July 2009
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
Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere Jumpponen, A.; Jones, K. L. New Phytologist, Vol. 184, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02990.x	journal	October 2009
Null model approaches to evaluating the relative role of different assembly processes in shaping ecological communities Mori, Akira S.; Fujii, Saori; Kitagawa, Ryo Oecologia, Vol. 178, Issue 1 https://doi.org/10.1007/s00442-014-3170-9	journal	December 2014
Spatial and Resource Factors Influencing High Microbial Diversity in Soil Zhou, J.; Xia, B.; Treves, D. S. Applied and Environmental Microbiology, Vol. 68, Issue 1 https://doi.org/10.1128/AEM.68.1.326-334.2002	journal	January 2002
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
Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies Schloss, Patrick D.; Gevers, Dirk; Westcott, Sarah L. PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0027310	journal	December 2011
A new record of Limnognathia maerski Kristensen & Funch, 2000 (Micrognathozoa) from the subantarctic Crozet Islands, with redescription of the trophi De Smet, Willem H. Journal of Zoology, Vol. 258, Issue 3 https://doi.org/10.1017/S095283690200153X	journal	November 2002
Bacterial community response to changes in a tri-trophic cascade during a whole-lake fish manipulation Saarenheimo, Jatta; Aalto, Sanni L.; Syväranta, Jari Ecology https://doi.org/10.1890/15-1052.1	journal	October 2015
Biogeographic Patterns of Arbuscular Mycorrhizal Fungal Communities Along a Land-Use Intensification Gradient in the Subtropical Atlantic Forest Biome Ceola, Gessiane; Goss-Souza, Dennis; Alves, Joana Microbial Ecology https://doi.org/10.1007/s00248-021-01721-y	journal	March 2021
Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake Liu, Yang; Ren, Ze; Qu, Xiaodong Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61569-z	journal	March 2020
Challenges in microbial ecology: Building predictive understanding of community function and dynamics Unknown, (:Unkn) My University https://doi.org/10.34944/dspace/5051	text	January 2016
Competition for light causes plant biodiversity loss after eutrophication Hautier, Y.; Niklaus, P. A.; Hector, A. American Association for the Advancement of Science (AAAS) https://doi.org/10.5167/uzh-18666	text	January 2009
Challenges in microbial ecology: building predictive understanding of community function and dynamics. Widder, Stefanie; Allen, Rosalind J.; Allen, Rosalind J. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.10735	text	January 2016

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Title: Nitrogen enrichment suppresses other environmental drivers and homogenizes salt marsh leaf microbiome

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