Plant diversity and functional identity drive grassland rhizobacterial community responses after 15 years of CO 2 and nitrogen enrichment

Revillini, Daniel; Reich, Peter B.; Johnson, Nancy Collins

doi:10.1111/1365-2745.14271

Plant diversity and functional identity drive grassland rhizobacterial community responses after 15 years of CO ₂ and nitrogen enrichment

Journal Article · Thu Feb 01 00:00:00 EST 2024 · Journal of Ecology

DOI:https://doi.org/10.1111/1365-2745.14271· OSTI ID:2283790

^[1]; Reich, Peter B. ^[2]; Johnson, Nancy Collins ^[3]

Department of Biological Sciences Northern Arizona University Flagstaff Arizona USA, Instituto de Recursos Naturales y Agrobiologia de Sevilla (IRNAS‐CSIC) Sevilla Spain
Department of Forest Resources University of Minnesota St. Paul Minnesota USA, Hawkesbury Institute for the Environment Western Sydney University Penrith New South Wales Australia, School for Environment and Sustainability, Institute for Global Change Biology University of Michigan Ann Arbor Michigan USA
Department of Biological Sciences Northern Arizona University Flagstaff Arizona USA, School of Earth and Sustainability Northern Arizona University Flagstaff Arizona USA

Abstract

Improved understanding of bacterial community responses to multiple environmental filters over long time periods is a fundamental step to develop mechanistic explanations of plant–bacterial interactions as environmental change progresses.

This is the first study to examine responses of grassland root‐associated bacterial communities to 15 years of experimental manipulations of plant species richness, functional group and factorial enrichment of atmospheric CO ₂ (eCO ₂ ) and soil nitrogen (+N).

Across the experiment, plant species richness was the strongest predictor of rhizobacterial community composition, followed by +N, with no observed effect of eCO ₂ . Monocultures of C ₃ and C ₄ grasses and legumes all exhibited dissimilar rhizobacterial communities within and among those groups. Functional responses were also dependent on plant functional group, where N ₂ ‐fixation genes, NO ₃₋ ‐reducing genes and P‐solubilizing predicted gene abundances increased under resource‐enriched conditions for grasses, but generally declined for legumes. In diverse plots with 16 plant species, the interaction of eCO ₂ +N altered rhizobacterial composition, while +N increased the predicted abundance of nitrogenase‐encoding genes, and eCO ₂ +N increased the predicted abundance of bacterial P‐solubilizing genes.

Synthesis : Our findings suggest that rhizobacterial community structure and function will be affected by important global environmental change factors such as eCO ₂ , but these responses are primarily contingent on plant species richness and the selective influence of different plant functional groups.

View Journal Article

Sponsoring Organization:: USDOE

OSTI ID:: 2283790

Alternate ID(s):: OSTI ID: 2283792

Journal Information:: Journal of Ecology, Journal Name: Journal of Ecology Journal Issue: 4 Vol. 112; ISSN 0022-0477

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (47)

Metagenomic reconstruction of nitrogen cycling pathways in a CO2-enriched grassland ecosystem Tu, Qichao; He, Zhili; Wu, Liyou Soil Biology and Biochemistry, Vol. 106 https://doi.org/10.1016/j.soilbio.2016.12.017	journal	March 2017
Signaling in the Rhizosphere Venturi, Vittorio; Keel, Christoph Trends in Plant Science, Vol. 21, Issue 3 https://doi.org/10.1016/j.tplants.2016.01.005	journal	March 2016
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Trends in Plant Science, Vol. 23, Issue 1 https://doi.org/10.1016/j.tplants.2017.09.003	journal	January 2018
Mycorrhizal Markets, Firms, and Co-ops Noë, Ronald; Kiers, E. Toby Trends in Ecology & Evolution, Vol. 33, Issue 10 https://doi.org/10.1016/j.tree.2018.07.007	journal	October 2018
Nitrogen limitation of microbial decomposition in a grassland under elevated CO2 Hu, S.; Chapin, F. S.; Firestone, M. K. Nature, Vol. 409, Issue 6817 https://doi.org/10.1038/35051576	journal	January 2001
Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition Reich, Peter B.; Knops, Jean; Tilman, David Nature, Vol. 410, Issue 6830 https://doi.org/10.1038/35071062	journal	April 2001
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/NMETH.F.303	journal	April 2010
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide He, Zhili; Piceno, Yvette; Deng, Ye The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.99	journal	July 2011
Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass Reich, Peter B.; Hobbie, Sarah E. Nature Climate Change, Vol. 3, Issue 3 https://doi.org/10.1038/nclimate1694	journal	September 2012
Differential abundance analysis for microbial marker-gene surveys Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2658	journal	September 2013
Soil inoculation steers restoration of terrestrial ecosystems Wubs, E. R. Jasper; van der Putten, Wim H.; Bosch, Machiel Nature Plants, Vol. 2, Issue 8 https://doi.org/10.1038/nplants.2016.107	journal	July 2016
A trade-off between plant and soil carbon storage under elevated CO2 Terrer, C.; Phillips, R. P.; Hungate, B. A. Nature, Vol. 591, Issue 7851 https://doi.org/10.1038/s41586‐021‐03306‐8	journal	March 2021
Nitrate application or P deficiency induce a decline in Medicago truncatula N2-fixation by similar changes in the nodule transcriptome Liese, Rebecca; Schulze, Joachim; Cabeza, Ricardo A. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep46264	journal	April 2017
Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N Reich, P. B.; Tilman, D.; Naeem, S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 27 https://doi.org/10.1073/pnas.0306602101	journal	June 2004
Global patterns in bacterial diversity Lozupone, C. A.; Knight, R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 27 https://doi.org/10.1073/pnas.0611525104	journal	June 2007
Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity Isbell, F.; Reich, P. B.; Tilman, D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 29 https://doi.org/10.1073/pnas.1310880110	journal	July 2013
Root surface as a frontier for plant microbiome research: Fig. 1. van der Heijden, Marcel G. A.; Schlaeppi, Klaus Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1500709112	journal	February 2015
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1508382112	journal	August 2015
Assembly and ecological function of the root microbiome across angiosperm plant species Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1717617115	journal	January 2018
Population Marginal Means in the Linear Model: An Alternative to Least Squares Means Searle, S. R.; Speed, F. M.; Milliken, G. A. The American Statistician, Vol. 34, Issue 4 https://doi.org/10.1080/00031305.1980.10483031	journal	November 1980
Enhanced soybean (Glycine maxL.) plant growth and nodulation byBradyrhizobium japonicum-SB1 in presence ofBacillus thuringiensis-KR1 Mishra, Pankaj K.; Mishra, Smita; Selvakumar, G. Acta Agriculturae Scandinavica, Section B - Plant Soil Science, Vol. 59, Issue 2 https://doi.org/10.1080/09064710802040558	journal	March 2009
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
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
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
Predicting community and ecosystem outcomes of mycorrhizal responses to global change Johnson, Nancy C.; Angelard, Caroline; Sanders, Ian R. Ecology Letters, Vol. 16 https://doi.org/10.1111/ele.12085	journal	May 2013
Disentangling species and functional group richness effects on soil N cycling in a grassland ecosystem Wei, Xiaorong; Reich, Peter B.; Hobbie, Sarah E. Global Change Biology, Vol. 23, Issue 11 https://doi.org/10.1111/gcb.13757	journal	June 2017
Nitrogen fertilization weakens the linkage between soil carbon and microbial diversity: A global meta‐analysis Yang, Yang; Chen, Xinli; Liu, Liangxu Global Change Biology, Vol. 28, Issue 21 https://doi.org/10.1111/gcb.16361	journal	August 2022
Global projections of the soil microbiome in the Anthropocene Guerra, Carlos A.; Delgado‐Baquerizo, Manuel; Duarte, Eliana Global Ecology and Biogeography, Vol. 30, Issue 5 https://doi.org/10.1111/geb.13273	journal	February 2021
Mycorrhizal phenotypes and the Law of the Minimum Johnson, Nancy Collins; Wilson, Gail W. T.; Wilson, Jacqueline A. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13172	journal	November 2014
The importance of the microbiome of the plant holobiont Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13312	journal	February 2015
Host selection shapes crop microbiome assembly and network complexity Xiong, Chao; Zhu, Yong‐Guan; Wang, Jun‐Tao New Phytologist, Vol. 229, Issue 2 https://doi.org/10.1111/nph.16890	journal	September 2020
Functional diversity and identity of plant genotypes regulate rhizodeposition and soil microbial activity Semchenko, Marina; Xue, Piao; Leigh, Tomas New Phytologist, Vol. 232, Issue 2 https://doi.org/10.1111/nph.17604	journal	August 2021
Legume nodulation: The host controls the party Ferguson, Brett J.; Mens, Céline; Hastwell, April H. Plant, Cell & Environment, Vol. 42, Issue 1 https://doi.org/10.1111/pce.13348	journal	June 2018
Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis Kiers, E. T.; Duhamel, M.; Beesetty, Y. Science, Vol. 333, Issue 6044 https://doi.org/10.1126/science.1208473	journal	August 2011
How mycorrhizal associations drive plant population and community biology Tedersoo, Leho; Bahram, Mohammad; Zobel, Martin Science, Vol. 367, Issue 6480 https://doi.org/10.1126/science.aba1223	journal	February 2020
Resource Limitation in Plants-An Economic Analogy Bloom, A. J.; Chapin, F. S.; Mooney, H. A. Annual Review of Ecology and Systematics, Vol. 16, Issue 1 https://doi.org/10.1146/annurev.es.16.110185.002051	journal	November 1985
Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions Bonfante, Paola; Anca, Iulia-Andra Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073504	journal	October 2009
Plant-Growth-Promoting Rhizobacteria Lugtenberg, Ben; Kamilova, Faina Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.162918	journal	October 2009
Phylogenetic Diversity (PD) and Biodiversity Conservation: Some Bioinformatics Challenges Faith, Daniel P.; Baker, Andrew M. Evolutionary Bioinformatics, Vol. 2 https://doi.org/10.1177/117693430600200007	journal	January 2006
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z. Ecological Applications, Vol. 20, Issue 1 https://doi.org/10.1890/08-0127.1	journal	January 2010
Modeling the Carbon Cost of Plant Nitrogen and Phosphorus Uptake Across Temperate and Tropical Forests Allen, Kara; Fisher, Joshua B.; Phillips, Richard P. Frontiers in Forests and Global Change, Vol. 3 https://doi.org/10.3389/ffgc.2020.00043	journal	May 2020
Unraveling the plant microbiome: looking back and future perspectives Berg, Gabriele; Grube, Martin; Schloter, Michael Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00148	journal	June 2014
Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks Revillini, Daniel; Wilson, Gail W. T.; Miller, R. Michael Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01018	journal	August 2019
Legumes Modulate Allocation to Rhizobial Nitrogen Fixation in Response to Factorial Light and Nitrogen Manipulation Friel, Colleen A.; Friesen, Maren L. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01316	journal	November 2019
Swarm: robust and fast clustering method for amplicon-based studies Mahé, Frédéric; Rognes, Torbjørn; Quince, Christopher PeerJ, Vol. 2 https://doi.org/10.7717/peerj.593	journal	January 2014

Similar Records

Strong photosynthetic acclimation and enhanced water‐use efficiency in grassland functional groups persist over 21 years of CO ₂ enrichment, independent of nitrogen supply

Journal Article · Sun Jun 23 20:00:00 EDT 2019 · Global Change Biology · OSTI ID:1560216

Plant diversity and functional identity drive grassland rhizobacterial community responses after 15 years of CO 2 and nitrogen enrichment

Citation Formats

References (47)

Similar Records

Related Subjects

Plant diversity and functional identity drive grassland rhizobacterial community responses after 15 years of CO ₂ and nitrogen enrichment