Adaptive differentiation and rapid evolution of a soil bacterium along a climate gradient

Chase, Alexander B.; Weihe, Claudia; Martiny, Jennifer B. H.

doi:10.1073/pnas.2101254118

Title: Adaptive differentiation and rapid evolution of a soil bacterium along a climate gradient

Journal Article · Tue Apr 27 00:00:00 EDT 2021 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2101254118· OSTI ID:1780508

^[1];

^[2];

^[2]

Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697,, Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, CA 92093
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697,

Microbial community responses to environmental change are largely associated with ecological processes; however, the potential for microbes to rapidly evolve and adapt remains relatively unexplored in natural environments. To assess how ecological and evolutionary processes simultaneously alter the genetic diversity of a microbiome, we conducted two concurrent experiments in the leaf litter layer of soil over 18 mo across a climate gradient in Southern California. In the first experiment, we reciprocally transplanted microbial communities from five sites to test whether ecological shifts in ecotypes of the abundant bacterium, Curtobacterium, corresponded to past adaptive differentiation. In the transplanted communities, ecotypes converged toward that of the native communities growing on a common litter substrate. Moreover, these shifts were correlated with community-weighted mean trait values of the Curtobacterium ecotypes, indicating that some of the trait variation among ecotypes could be explained by local adaptation to climate conditions. In the second experiment, we transplanted an isogenic Curtobacterium strain and tracked genomic mutations associated with the sites across the same climate gradient. Using a combination of genomic and metagenomic approaches, we identified a variety of nonrandom, parallel mutations associated with transplantation, including mutations in genes related to nutrient acquisition, stress response, and exopolysaccharide production. Together, the field experiments demonstrate how both demographic shifts of previously adapted ecotypes and contemporary evolution can alter the diversity of a soil microbiome on the same timescale.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of California, Irvine, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: PS02-09ER09-25; SC0016410; SC0020382

OSTI ID:: 1780508

Alternate ID(s):: OSTI ID: 1816727; OSTI ID: 2263364

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 118 Journal Issue: 18; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Mutation Rate Inferred From Synonymous Substitutions in a Long-Term Evolution Experiment With Escherichia coli Wielgoss, Sébastien; Barrick, Jeffrey E.; Tenaillon, Olivier G3: Genes\|Genomes\|Genetics, Vol. 1, Issue 3 https://doi.org/10.1534/g3.111.000406	journal	August 2011
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
Evolution of a Dominant Natural Isolate of Escherichia coli in the Human Gut over the Course of a Year Suggests a Neutral Evolution with Reduced Effective Population Size Ghalayini, Mohamed; Launay, Adrien; Bridier-Nahmias, Antoine Applied and Environmental Microbiology, Vol. 84, Issue 6 https://doi.org/10.1128/AEM.02377-17	journal	January 2018
Evolutionary dynamics of bacteria in the gut microbiome within and across hosts Garud, Nandita R.; Good, Benjamin H.; Hallatschek, Oskar PLOS Biology, Vol. 17, Issue 1 https://doi.org/10.1371/journal.pbio.3000102	journal	January 2019
Increased biofilm formation due to high-temperature adaptation in marine Roseobacter Kent, Alyssa G.; Garcia, Catherine A.; Martiny, Adam C. Nature Microbiology, Vol. 3, Issue 9 https://doi.org/10.1038/s41564-018-0213-8	journal	July 2018
Ordering microbial diversity into ecologically and genetically cohesive units Shapiro, B. Jesse; Polz, Martin F. Trends in Microbiology, Vol. 22, Issue 5 https://doi.org/10.1016/j.tim.2014.02.006	journal	May 2014
Decomposition responses to climate depend on microbial community composition Glassman, Sydney I.; Weihe, Claudia; Li, Junhui Proceedings of the National Academy of Sciences, Vol. 115, Issue 47 https://doi.org/10.1073/pnas.1811269115	journal	November 2018
Microbial diversity and soil functions Nannipieri, P.; Ascher, J.; Ceccherini, M. T. European Journal of Soil Science, Vol. 54, Issue 4 https://doi.org/10.1046/j.1351-0754.2003.0556.x	journal	December 2003
The importance of resolving biogeographic patterns of microbial microdiversity Chase, Alexander B.; Martiny, Jennifer BH Microbiology Australia, Vol. 39, Issue 1 https://doi.org/10.1071/MA18003	journal	January 2018
Ecology drives a global network of gene exchange connecting the human microbiome Smillie, Chris S.; Smith, Mark B.; Friedman, Jonathan Nature, Vol. 480, Issue 7376 https://doi.org/10.1038/nature10571	journal	October 2011
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher Current Protocols in Bioinformatics, Vol. 43, Issue 1 https://doi.org/10.1002/0471250953.bi1110s43	journal	October 2013
Fundamentals of Microbial Community Resistance and Resilience Shade, Ashley; Peter, Hannes; Allison, Steven D. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00417	journal	January 2012
Microdiversity shapes the traits, niche space, and biogeography of microbial taxa: The ecological function of microdiversity Larkin, Alyse A.; Martiny, Adam C. Environmental Microbiology Reports, Vol. 9, Issue 2 https://doi.org/10.1111/1758-2229.12523	journal	March 2017
Eco-evolutionary Dynamics Set the Tempo and Trajectory of Metabolic Evolution in Multispecies Communities Evans, Rachael; Beckerman, Andrew P.; Wright, Rosanna C. T. Current Biology, Vol. 30, Issue 24 https://doi.org/10.1016/j.cub.2020.09.028	journal	December 2020
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Microbial response to simulated global change is phylogenetically conserved and linked with functional potential Amend, Anthony S.; Martiny, Adam C.; Allison, Steven D. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.96	journal	June 2015
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
Population Genetics in the Human Microbiome Garud, Nandita R.; Pollard, Katherine S. Trends in Genetics, Vol. 36, Issue 1 https://doi.org/10.1016/j.tig.2019.10.010	journal	January 2020
Explaining microbial genomic diversity in light of evolutionary ecology Cordero, Otto X.; Polz, Martin F. Nature Reviews Microbiology, Vol. 12, Issue 4 https://doi.org/10.1038/nrmicro3218	journal	March 2014
Causes and evolutionary significance of genetic convergence Christin, Pascal-Antoine; Weinreich, Daniel M.; Besnard, Guillaume Trends in Genetics, Vol. 26, Issue 9 https://doi.org/10.1016/j.tig.2010.06.005	journal	September 2010
Temporal variation overshadows the response of leaf litter microbial communities to simulated global change Matulich, Kristin L.; Weihe, Claudia; Allison, Steven D. The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.58	journal	May 2015
Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range Ågren, Jon; Schemske, Douglas W. New Phytologist, Vol. 194, Issue 4 https://doi.org/10.1111/j.1469-8137.2012.04112.x	journal	March 2012
Bead-linked transposomes enable a normalization-free workflow for NGS library preparation Bruinsma, Stephen; Burgess, Joshua; Schlingman, Daniel BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-5096-9	journal	October 2018
A Reverse Ecology Approach Based on a Biological Definition of Microbial Populations Arevalo, Philip; VanInsberghe, David; Elsherbini, Joseph Cell, Vol. 178, Issue 4 https://doi.org/10.1016/j.cell.2019.06.033	journal	August 2019
Do community-weighted mean functional traits reflect optimal strategies? Muscarella, Robert; Uriarte, María Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1827 https://doi.org/10.1098/rspb.2015.2434	journal	March 2016
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
What genomic data can reveal about eco-evolutionary dynamics Rudman, Seth M.; Barbour, Matthew A.; Csilléry, Katalin Nature Ecology & Evolution, Vol. 2, Issue 1 https://doi.org/10.1038/s41559-017-0385-2	journal	November 2017
Adaptation from standing genetic variation Barrett, R.; Schluter, D. Trends in Ecology & Evolution, Vol. 23, Issue 1 https://doi.org/10.1016/j.tree.2007.09.008	journal	January 2008
Microbial abundance and composition influence litter decomposition response to environmental change Allison, Steven D.; Lu, Ying; Weihe, Claudia Ecology, Vol. 94, Issue 3 https://doi.org/10.1890/12-1243.1	journal	March 2013
Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes Moore, Lisa R.; Rocap, Gabrielle; Chisholm, Sallie W. Nature, Vol. 393, Issue 6684 https://doi.org/10.1038/30965	journal	June 1998
Growth dynamics of gut microbiota in health and disease inferred from single metagenomic samples Korem, T.; Zeevi, D.; Suez, J. Science, Vol. 349, Issue 6252 https://doi.org/10.1126/science.aac4812	journal	July 2015
Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton Hunt, D. E.; David, L. A.; Gevers, D. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1157890	journal	May 2008
Adaptation in Natural Microbial Populations Koskella, Britt; Vos, Michiel Annual Review of Ecology, Evolution, and Systematics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-ecolsys-112414-054458	journal	December 2015
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Evolutionary origins for ecological patterns in space Urban, Mark C.; Strauss, Sharon Y.; Pelletier, Fanie Proceedings of the National Academy of Sciences, Vol. 117, Issue 30 https://doi.org/10.1073/pnas.1918960117	journal	July 2020
Microbial decomposers not constrained by climate history along a Mediterranean climate gradient in southern California Baker, Nameer R.; Khalili, Banafshe; Martiny, Jennifer B. H. Ecology, Vol. 99, Issue 6 https://doi.org/10.1002/ecy.2345	journal	June 2018
The NCBI Taxonomy database Federhen, S. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1178	journal	December 2011
Extracellular enzyme kinetics and thermodynamics along a climate gradient in southern California Baker, Nameer R.; Allison, Steven D. Soil Biology and Biochemistry, Vol. 114 https://doi.org/10.1016/j.soilbio.2017.07.005	journal	November 2017
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Rapid evolution destabilizes species interactions in a fluctuating environment Rodríguez-Verdugo, Alejandra; Ackermann, Martin The ISME Journal, Vol. 15, Issue 2 https://doi.org/10.1038/s41396-020-00787-9	journal	October 2020
Niche Partitioning Among Prochlorococcus Ecotypes Along Ocean-Scale Environmental Gradients Johnson, Z. I. Science, Vol. 311, Issue 5768 https://doi.org/10.1126/science.1118052	journal	March 2006
Quantifying relationships between traits and explicitly measured gradients of stress and disturbance in early successional plant communities: Trait-environment linkages in early successional communities Sonnier, Grégory; Shipley, Bill; Navas, Marie-Laure Journal of Vegetation Science, Vol. 21, Issue 6 https://doi.org/10.1111/j.1654-1103.2010.01210.x	journal	August 2010
Measurement of bacterial replication rates in microbial communities Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C. Nature Biotechnology, Vol. 34, Issue 12 https://doi.org/10.1038/nbt.3704	journal	November 2016
The Molecular Diversity of Adaptive Convergence Tenaillon, O.; Rodriguez-Verdugo, A.; Gaut, R. L. Science, Vol. 335, Issue 6067, p. 457-461 https://doi.org/10.1126/science.1212986	journal	January 2012
Tempo and mode of genome evolution in a 50,000-generation experiment Tenaillon, Olivier; Barrick, Jeffrey E.; Ribeck, Noah Nature, Vol. 536, Issue 7615 https://doi.org/10.1038/nature18959	journal	August 2016
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
What are Bacterial Species? Cohan, Frederick M. Annual Review of Microbiology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev.micro.56.012302.160634	journal	October 2002
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits Chase, Alexander B.; Karaoz, Ulas; Brodie, Eoin L. mBio, Vol. 8, Issue 6 https://doi.org/10.1128/mBio.01809-17	journal	November 2017
In Situ Evolutionary Rate Measurements Show Ecological Success of Recently Emerged Bacterial Hybrids Denef, V. J.; Banfield, J. F. Science, Vol. 336, Issue 6080 https://doi.org/10.1126/science.1218389	journal	April 2012
Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq Deatherage, Daniel E.; Barrick, Jeffrey E. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0554-6_12	book	January 2014
PacBio Sequencing and Its Applications Rhoads, Anthony; Au, Kin Fai Genomics, Proteomics & Bioinformatics, Vol. 13, Issue 5 https://doi.org/10.1016/j.gpb.2015.08.002	journal	October 2015
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community Albright, Michaeline B. N.; Chase, Alexander B.; Martiny, Jennifer B. H. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mBio.00568-19	journal	April 2019
Calibrating bacterial evolution Ochman, H.; Elwyn, S.; Moran, N. A. Proceedings of the National Academy of Sciences, Vol. 96, Issue 22 https://doi.org/10.1073/pnas.96.22.12638	journal	October 1999
Community Assembly, Niche Conservatism, and Adaptive Evolution in Changing Environments Ackerly, David D. International Journal of Plant Sciences, Vol. 164, Issue S3 https://doi.org/10.1086/368401	journal	May 2003
Experimental manipulation of selfish genetic elements links genes to microbial community function Quistad, Steven D.; Doulcier, Guilhem; Rainey, Paul B. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798 https://doi.org/10.1098/rstb.2019.0681	journal	March 2020
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
The Reliability of Metagenome-Assembled Genomes (MAGs) in Representing Natural Populations: Insights from Comparing MAGs against Isolate Genomes Derived from the Same Fecal Sample Meziti, Alexandra; Rodriguez-R, Luis M.; Hatt, Janet K. Applied and Environmental Microbiology, Vol. 87, Issue 6 https://doi.org/10.1128/AEM.02593-20	journal	January 2021
Bacterial adaptation is constrained in complex communities Scheuerl, Thomas; Hopkins, Meirion; Nowell, Reuben W. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14570-z	journal	February 2020
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-538	journal	October 2010
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing Lee, H.; Popodi, E.; Tang, H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 41 https://doi.org/10.1073/pnas.1210309109	journal	September 2012
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement Walker, Bruce J.; Abeel, Thomas; Shea, Terrance PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112963	journal	November 2014
Rapid evolution and the convergence of ecological and evolutionary time: Rapid evolution and the convergence of ecological and evolutionary time Hairston, Nelson G.; Ellner, Stephen P.; Geber, Monica A. Ecology Letters, Vol. 8, Issue 10 https://doi.org/10.1111/j.1461-0248.2005.00812.x	journal	August 2005
Evidence for Ecological Flexibility in the Cosmopolitan Genus Curtobacterium Chase, Alexander B.; Arevalo, Philip; Polz, Martin F. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01874	journal	November 2016
Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria Chase, Alexander B.; Arevalo, Philip; Brodie, Eoin L. mBio, Vol. 10, Issue 5 https://doi.org/10.1128/mBio.02361-19	journal	October 2019
Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.241	journal	January 2016
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
Soil bacterial populations are shaped by recombination and gene-specific selection across a grassland meadow Crits-Christoph, Alexander; Olm, Matthew R.; Diamond, Spencer The ISME Journal, Vol. 14, Issue 7 https://doi.org/10.1038/s41396-020-0655-x	journal	April 2020
Emergence of soil bacterial ecotypes along a climate gradient: Soil ecotypes along a climate gradient Chase, Alexander B.; Gomez-Lunar, Zulema; Lopez, Alberto E. Environmental Microbiology, Vol. 20, Issue 11 https://doi.org/10.1111/1462-2920.14405	journal	October 2018

Similar Records

Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits

Journal Article · Fri Dec 29 00:00:00 EST 2017 · mBio · OSTI ID:1780508

Chase, Alexander B.; Karaoz, Ulas; Brodie, Eoin L.; +6 more

Emergence of soil bacterial ecotypes along a climate gradient: Soil ecotypes along a climate gradient

Journal Article · Fri Oct 05 00:00:00 EDT 2018 · Environmental Microbiology · OSTI ID:1780508

Chase, Alexander B.; Gomez-Lunar, Zulema; Lopez, Alberto E.; +4 more

Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria

Journal Article · Tue Oct 29 00:00:00 EDT 2019 · mBio (Online) · OSTI ID:1780508

Chase, Alexander B.; Arevalo, Philip; Brodie, Eoin L.; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
reciprocal transplant
Curtobacterium
adaptation
experimental evolution
ecotypes

Title: Adaptive differentiation and rapid evolution of a soil bacterium along a climate gradient

Citation Formats

References (71)

Similar Records

Related Subjects