Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities
Abstract
ABSTRACT Biotic factors that influence the temporal stability of microbial community functioning are an emerging research focus for the control of natural and engineered systems. The discovery of common features within community ensembles that differ in functional stability over time is a starting point to explore biotic factors. We serially propagated a suite of soil microbial communities through five generations of 28-day microcosm incubations to examine microbial community compositional and functional stability during plant litter decomposition. Using dissolved organic carbon (DOC) abundance as a target function, we hypothesized that microbial diversity, compositional stability, and associated changes in interactions would explain the relative stability of the ecosystem function between generations. Communities with initially high DOC abundance tended to converge towards a “low DOC” phenotype within two generations, but across all microcosms, functional stability between generations was highly variable. By splitting communities into two cohorts based on their relative DOC functional stability, we found that compositional shifts, diversity, and interaction network complexity were associated with the stability of DOC abundance between generations. Further, our results showed that legacy effects were important in determining compositional and functional outcomes, and we identified taxa associated with high DOC abundance. In the context of litter decomposition,more »
- Authors:
-
[1];
[1];
[1];
- Bioscience Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USA
- Earth and Environmental Sciences Division, Los Alamos National Laboratory , Los Alamos, New Mexico, USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1987731
- Resource Type:
- Published Article
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Name: mSystems Journal Volume: 8 Journal Issue: 3; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Moore, Eric R., Suazo, Dennis, Babilonia, Joany, Montoya, Kyana N., Gallegos-Graves, La Verne, Sevanto, Sanna, Dunbar, John, Albright, Michaeline B. N., and Graham, ed., Emily B. Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities. United States: N. p., 2023.
Web. doi:10.1128/msystems.01220-22.
Moore, Eric R., Suazo, Dennis, Babilonia, Joany, Montoya, Kyana N., Gallegos-Graves, La Verne, Sevanto, Sanna, Dunbar, John, Albright, Michaeline B. N., & Graham, ed., Emily B. Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities. United States. https://doi.org/10.1128/msystems.01220-22
Moore, Eric R., Suazo, Dennis, Babilonia, Joany, Montoya, Kyana N., Gallegos-Graves, La Verne, Sevanto, Sanna, Dunbar, John, Albright, Michaeline B. N., and Graham, ed., Emily B. Thu .
"Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities". United States. https://doi.org/10.1128/msystems.01220-22.
@article{osti_1987731,
title = {Drivers of stability and transience in composition-functioning links during serial propagation of litter-decomposing microbial communities},
author = {Moore, Eric R. and Suazo, Dennis and Babilonia, Joany and Montoya, Kyana N. and Gallegos-Graves, La Verne and Sevanto, Sanna and Dunbar, John and Albright, Michaeline B. N. and Graham, ed., Emily B.},
abstractNote = {ABSTRACT Biotic factors that influence the temporal stability of microbial community functioning are an emerging research focus for the control of natural and engineered systems. The discovery of common features within community ensembles that differ in functional stability over time is a starting point to explore biotic factors. We serially propagated a suite of soil microbial communities through five generations of 28-day microcosm incubations to examine microbial community compositional and functional stability during plant litter decomposition. Using dissolved organic carbon (DOC) abundance as a target function, we hypothesized that microbial diversity, compositional stability, and associated changes in interactions would explain the relative stability of the ecosystem function between generations. Communities with initially high DOC abundance tended to converge towards a “low DOC” phenotype within two generations, but across all microcosms, functional stability between generations was highly variable. By splitting communities into two cohorts based on their relative DOC functional stability, we found that compositional shifts, diversity, and interaction network complexity were associated with the stability of DOC abundance between generations. Further, our results showed that legacy effects were important in determining compositional and functional outcomes, and we identified taxa associated with high DOC abundance. In the context of litter decomposition, achieving functionally stable communities is required to utilize soil microbiomes to increase DOC abundance and long-term terrestrial DOC sequestration as one solution to reduce atmospheric carbon dioxide concentrations. Identifying factors that stabilize function for a community of interest may improve the success of microbiome engineering applications. IMPORTANCE Microbial community functioning can be highly dynamic over time. Identifying and understanding biotic factors that control functional stability is of significant interest for natural and engineered communities alike. Using plant litter–decomposing communities as a model system, this study examined the stability of ecosystem function over time following repeated community transfers. By identifying microbial community features that are associated with stable ecosystem functions, microbial communities can be manipulated in ways that promote the consistency and reliability of the desired function, improving outcomes and increasing the utility of microorganisms.},
doi = {10.1128/msystems.01220-22},
journal = {mSystems},
number = 3,
volume = 8,
place = {United States},
year = {Thu Jun 29 00:00:00 EDT 2023},
month = {Thu Jun 29 00:00:00 EDT 2023}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/msystems.01220-22
https://doi.org/10.1128/msystems.01220-22
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The importance of anabolism in microbial control over soil carbon storage
journal, July 2017
- Liang, Chao; Schimel, Joshua P.; Jastrow, Julie D.
- Nature Microbiology, Vol. 2, Issue 8
Alternative stable states in ecology
journal, September 2003
- Beisner, Be; Haydon, Dt; Cuddington, K.
- Frontiers in Ecology and the Environment, Vol. 1, Issue 7
Enterotypes of the human gut microbiome
journal, April 2011
- Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric
- Nature, Vol. 473, Issue 7346
Return to Neverland: Shifting Baselines Affect Eutrophication Restoration Targets
journal, October 2008
- Duarte, Carlos M.; Conley, Daniel J.; Carstensen, Jacob
- Estuaries and Coasts, Vol. 32, Issue 1
Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011
- Martin, Marcel
- EMBnet.journal, Vol. 17, Issue 1
Death and cannibalism in a seasonal environment facilitate bacterial coexistence
journal, January 2009
- Rozen, Daniel E.; Philippe, Nadège; Arjan de Visser, J.
- Ecology Letters, Vol. 12, Issue 1
New insights into bacterial adaptation through in vivo and in silico experimental evolution
journal, March 2012
- Hindré, Thomas; Knibbe, Carole; Beslon, Guillaume
- Nature Reviews Microbiology, Vol. 10, Issue 5
Will a Large Complex System be Stable?
journal, August 1972
- May, Robert M.
- Nature, Vol. 238, Issue 5364
New frontiers in agriculture productivity: Optimised microbial inoculants and in situ microbiome engineering
journal, November 2019
- Qiu, Zhiguang; Egidi, Eleonora; Liu, Hongwei
- Biotechnology Advances, Vol. 37, Issue 6
The Inherent Conflicts in Developing Soil Microbial Inoculants
journal, February 2019
- Kaminsky, Laura M.; Trexler, Ryan V.; Malik, Rondy J.
- Trends in Biotechnology, Vol. 37, Issue 2
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?
journal, February 2016
- Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas
- Frontiers in Microbiology, Vol. 7
Catastrophic shifts in ecosystems
journal, October 2001
- Scheffer, Marten; Carpenter, Steve; Foley, Jonathan A.
- Nature, Vol. 413, Issue 6856
The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications
journal, October 2018
- Nilsson, Rolf Henrik; Larsson, Karl-Henrik; Taylor, Andy F. S.
- Nucleic Acids Research, Vol. 47, Issue D1
Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli
journal, January 2003
- Cooper, T. F.; Rozen, D. E.; Lenski, R. E.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward
journal, May 2019
- Kallenbach, Cynthia M.; Wallenstein, Matthew D.; Schipanksi, Meagan E.
- Frontiers in Microbiology, Vol. 10
Experimental Design and Data Analysis for Biologists
book, January 2012
- Quinn, Gerry P.; Keough, Michael J.
- Cambridge University Press
Common principles and best practices for engineering microbiomes
journal, September 2019
- Lawson, Christopher E.; Harcombe, William R.; Hatzenpichler, Roland
- Nature Reviews Microbiology, Vol. 17, Issue 12
Engineering microbial consortia for controllable outputs
journal, March 2016
- Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob
- The ISME Journal, Vol. 10, Issue 9
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
Multiple states in river and lake ecosystems
journal, May 2002
- Dent, C. Lisa; Cumming, Graeme S.; Carpenter, Stephen R.
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 357, Issue 1421
The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks
journal, November 2013
- Yilmaz, Pelin; Parfrey, Laura Wegener; Yarza, Pablo
- Nucleic Acids Research, Vol. 42, Issue D1
Machine learning to predict microbial community functions: An analysis of dissolved organic carbon from litter decomposition
journal, July 2019
- Thompson, Jaron; Johansen, Renee; Dunbar, John
- PLOS ONE, Vol. 14, Issue 7
Reactor performances and microbial communities of biogas reactors: effects of inoculum sources
journal, October 2015
- Han, Sheng; Liu, Yafeng; Zhang, Shicheng
- Applied Microbiology and Biotechnology, Vol. 100, Issue 2
Community history affects the predictability of microbial ecosystem development
journal, August 2013
- Pagaling, Eulyn; Strathdee, Fiona; Spears, Bryan M.
- The ISME Journal, Vol. 8, Issue 1
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Stability criteria for complex microbial communities
journal, July 2018
- Butler, Stacey; O’Dwyer, James P.
- Nature Communications, Vol. 9, Issue 1
Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae
journal, November 2002
- Dunham, M. J.; Badrane, H.; Ferea, T.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 25
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
Succession of Microbial Decomposers Is Determined by Litter Type, but Site Conditions Drive Decomposition Rates
journal, December 2019
- Buresova, A.; Kopecky, J.; Hrdinkova, V.
- Applied and Environmental Microbiology, Vol. 85, Issue 24
Vaginal microbiome of reproductive-age women
journal, June 2010
- Ravel, J.; Gajer, P.; Abdo, Z.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
Long‐Term Experimental Evolution in Escherichia coli . VIII. Dynamics of a Balanced Polymorphism
journal, January 2000
- Rozen, Daniel E.; Lenski, Richard E.
- The American Naturalist, Vol. 155, Issue 1
Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning
journal, October 2019
- Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran
- Nature Communications, Vol. 10, Issue 1
Persistence of soil organic carbon caused by functional complexity
journal, July 2020
- Lehmann, Johannes; Hansel, Colleen M.; Kaiser, Christina
- Nature Geoscience, Vol. 13, Issue 8
Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils?
journal, April 2010
- Prescott, Cindy E.
- Biogeochemistry, Vol. 101, Issue 1-3
Abiotic conditions outweigh microbial origin during bacterial assembly in soils
journal, November 2020
- Kaminsky, Laura M.; Esker, Paul D.; Bell, Terrence H.
- Environmental Microbiology, Vol. 23, Issue 1
The ecology of the microbiome: Networks, competition, and stability
journal, November 2015
- Coyte, K. Z.; Schluter, J.; Foster, K. R.
- Science, Vol. 350, Issue 6261
Trophic Downgrading of Planet Earth
journal, July 2011
- Estes, James A.; Terborgh, John; Brashares, Justin S.
- Science, Vol. 333, Issue 6040
Trusting the hand that feeds: microbes evolve to anticipate a serial transfer protocol as individuals or collectives
journal, November 2019
- van Dijk, Bram; Meijer, Jeroen; Cuypers, Thomas D.
- BMC Evolutionary Biology, Vol. 19, Issue 1
Context-dependent dynamics lead to the assembly of functionally distinct microbial communities
journal, March 2020
- Bittleston, Leonora S.; Gralka, Matti; Leventhal, Gabriel E.
- Nature Communications, Vol. 11, Issue 1
Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome
journal, June 2016
- de Souza, Rafael Soares Correa; Okura, Vagner Katsumi; Armanhi, Jaderson Silveira Leite
- Scientific Reports, Vol. 6, Issue 1
Contribution of dissolved organic matter to carbon storage in forest mineral soils
journal, February 2008
- Kalbitz, Karsten; Kaiser, Klaus
- Journal of Plant Nutrition and Soil Science, Vol. 171, Issue 1
Bacterial succession on decomposing leaf litter exhibits a specific occurrence pattern of cellulolytic taxa and potential decomposers of fungal mycelia
journal, August 2016
- Tláskal, Vojtěch; Voříšková, Jana; Baldrian, Petr
- FEMS Microbiology Ecology, Vol. 92, Issue 11
Differences in substrate use linked to divergent carbon flow during litter decomposition
journal, July 2020
- Albright, Michaeline B. N.; Thompson, Jaron; Kroeger, Marie E.
- FEMS Microbiology Ecology, Vol. 96, Issue 8
Food Web Complexity and Species Diversity
journal, January 1966
- Paine, Robert T.
- The American Naturalist, Vol. 100, Issue 910
Microbial legacies alter decomposition in response to simulated global change
journal, October 2016
- Martiny, Jennifer BH; Martiny, Adam C.; Weihe, Claudia
- The ISME Journal, Vol. 11, Issue 2
Successional dynamics and alternative stable states in a saline activated sludge microbial community over 9 years
journal, October 2021
- Wang, Yulin; Ye, Jun; Ju, Feng
- Microbiome, Vol. 9, Issue 1
Comparison of factors limiting bacterial growth in different soils
journal, October 2007
- Demoling, Fredrik; Figueroa, Daniela; Bååth, Erland
- Soil Biology and Biochemistry, Vol. 39, Issue 10
Testing the functional significance of microbial composition in natural communities: Functional significance of microbial composition
journal, November 2007
- Reed, Heather E.; Martiny, Jennifer B. H.
- FEMS Microbiology Ecology, Vol. 62, Issue 2
Soil Bacterial and Fungal Richness Forecast Patterns of Early Pine Litter Decomposition
journal, November 2020
- Albright, Michaeline B. N.; Johansen, Renee; Thompson, Jaron
- Frontiers in Microbiology, Vol. 11
Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency
journal, September 2018
- Chen, Leiyi; Liu, Li; Mao, Chao
- Nature Communications, Vol. 9, Issue 1
Population-level analysis of gut microbiome variation
journal, April 2016
- Falony, Gwen; Joossens, Marie; Vieira-Silva, Sara
- Science, Vol. 352, Issue 6285
Structure and Function of Bacterial Communities Emerging from Different Sources under Identical Conditions
journal, January 2006
- Langenheder, S.; Lindstrom, E. S.; Tranvik, L. J.
- Applied and Environmental Microbiology, Vol. 72, Issue 1
Complexity–stability trade-off in empirical microbial ecosystems
journal, April 2022
- Yonatan, Yogev; Amit, Guy; Friedman, Jonathan
- Nature Ecology & Evolution, Vol. 6, Issue 6
Disturbed subsurface microbial communities follow equivalent trajectories despite different structural starting points: Microbial community succession and disturbance
journal, April 2014
- Handley, Kim M.; Wrighton, Kelly C.; Miller, Christopher S.
- Environmental Microbiology, Vol. 17, Issue 3
The legacy of the past: effects of historical processes on microbial metacommunities
journal, March 2017
- Vass, M.; Langenheder, S.
- Aquatic Microbial Ecology, Vol. 79, Issue 1