Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria
Abstract
For free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several obstacles to the study of the processes contributing to microbial diversification. These obstacles are particularly high in soil, where high bacterial diversity inhibits the study of closely related genotypes and therefore the factors structuring microbial populations. Here, we isolated strains within a singleCurtobacteriumecotype from surface soil (leaf litter) across a regional climate gradient and investigated the phylogenetic structure, recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. Our results indicate that microbial populations are delineated by gene flow discontinuities, with distinct populations cooccurring at multiple sites. Bacterial population structure was further delineated by genomic features allowing for the identification of candidate genes possibly contributing to local adaptation. These results suggest that the genetic structure within this bacterium is maintained both by ecological specialization in localized microenvironments (isolation by environment) and by dispersal limitation between geographic locations (isolation by distance).
- Authors:
-
[1];
[2];
[2];
[4];
- Univ. of California, Irvine, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Irvine, CA (United States)
- Univ. of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1581756
- Grant/Contract Number:
- AC02-05CH11231; SC0016410
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 10; Journal Issue: 5; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; curtobacterium; population structure; gene flow; microbial ecology; ecotype
Citation Formats
Chase, Alexander B., Arevalo, Philip, Brodie, Eoin L., Polz, Martin F., Karaoz, Ulas, Martiny, Jennifer B. H., and Taylor, John W. Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria. United States: N. p., 2019.
Web. doi:10.1128/mBio.02361-19.
Chase, Alexander B., Arevalo, Philip, Brodie, Eoin L., Polz, Martin F., Karaoz, Ulas, Martiny, Jennifer B. H., & Taylor, John W. Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria. United States. https://doi.org/10.1128/mBio.02361-19
Chase, Alexander B., Arevalo, Philip, Brodie, Eoin L., Polz, Martin F., Karaoz, Ulas, Martiny, Jennifer B. H., and Taylor, John W. Tue .
"Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria". United States. https://doi.org/10.1128/mBio.02361-19. https://www.osti.gov/servlets/purl/1581756.
@article{osti_1581756,
title = {Maintenance of Sympatric and Allopatric Populations in Free-Living Terrestrial Bacteria},
author = {Chase, Alexander B. and Arevalo, Philip and Brodie, Eoin L. and Polz, Martin F. and Karaoz, Ulas and Martiny, Jennifer B. H. and Taylor, John W.},
abstractNote = {For free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several obstacles to the study of the processes contributing to microbial diversification. These obstacles are particularly high in soil, where high bacterial diversity inhibits the study of closely related genotypes and therefore the factors structuring microbial populations. Here, we isolated strains within a singleCurtobacteriumecotype from surface soil (leaf litter) across a regional climate gradient and investigated the phylogenetic structure, recombination, and flexible gene content of this genomic diversity to infer patterns of gene flow. Our results indicate that microbial populations are delineated by gene flow discontinuities, with distinct populations cooccurring at multiple sites. Bacterial population structure was further delineated by genomic features allowing for the identification of candidate genes possibly contributing to local adaptation. These results suggest that the genetic structure within this bacterium is maintained both by ecological specialization in localized microenvironments (isolation by environment) and by dispersal limitation between geographic locations (isolation by distance).},
doi = {10.1128/mBio.02361-19},
journal = {mBio (Online)},
number = 5,
volume = 10,
place = {United States},
year = {Tue Oct 29 00:00:00 EDT 2019},
month = {Tue Oct 29 00:00:00 EDT 2019}
}
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Works referenced in this record:
Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea
journal, August 2003
- Whitaker, R. J.
- Science, Vol. 301, Issue 5635
Population Genomics of Early Events in the Ecological Differentiation of Bacteria
journal, April 2012
- Shapiro, B. Jesse; Friedman, Jonathan; Cordero, Otto X.
- Science, Vol. 336, Issue 6077
Ordering microbial diversity into ecologically and genetically cohesive units
journal, May 2014
- Shapiro, B. Jesse; Polz, Martin F.
- Trends in Microbiology, Vol. 22, Issue 5
Roary: rapid large-scale prokaryote pan genome analysis
journal, July 2015
- Page, Andrew J.; Cummins, Carla A.; Hunt, Martin
- Bioinformatics, Vol. 31, Issue 22
Microbial diversity and soil functions
journal, December 2003
- Nannipieri, P.; Ascher, J.; Ceccherini, M. T.
- European Journal of Soil Science, Vol. 54, Issue 4
Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
journal, April 2014
- Yawata, Y.; Cordero, O. X.; Menolascina, F.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
High-throughput ANI Analysis of 90K Prokaryotic Genomes Reveals Clear Species Boundaries
posted_content, October 2017
- Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M.
ISfinder: the reference centre for bacterial insertion sequences
journal, January 2006
- Siguier, P.
- Nucleic Acids Research, Vol. 34, Issue 90001
Isolation by environment
journal, October 2014
- Wang, Ian J.; Bradburd, Gideon S.
- Molecular Ecology, Vol. 23, Issue 23
Is the pan-genome also a pan-selectome?
journal, January 2012
- Rodriguez-Valera, Francisco; Ussery, David W.
- F1000Research, Vol. 1
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus
journal, April 2014
- Kashtan, N.; Roggensack, S. E.; Rodrigue, S.
- Science, Vol. 344, Issue 6182
Fast and Efficient Estimation of Individual Ancestry Coefficients
journal, February 2014
- Frichot, Eric; Mathieu, François; Trouillon, Théo
- Genetics, Vol. 196, Issue 4
Horizontal gene transfer and the evolution of bacterial and archaeal population structure
journal, March 2013
- Polz, Martin F.; Alm, Eric J.; Hanage, William P.
- Trends in Genetics, Vol. 29, Issue 3
PopGenome: An Efficient Swiss Army Knife for Population Genomic Analyses in R
journal, April 2014
- Pfeifer, Bastian; Wittelsbürger, Ulrich; Ramos-Onsins, Sebastian E.
- Molecular Biology and Evolution, Vol. 31, Issue 7
Genomics, environmental genomics and the issue of microbial species
journal, June 2007
- Ward, D. M.; Cohan, F. M.; Bhaya, D.
- Heredity, Vol. 100, Issue 2
Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils
journal, April 2015
- VanInsberghe, David; Maas, Kendra R.; Cardenas, Erick
- The ISME Journal, Vol. 9, Issue 11
Explaining microbial genomic diversity in light of evolutionary ecology
journal, March 2014
- Cordero, Otto X.; Polz, Martin F.
- Nature Reviews Microbiology, Vol. 12, Issue 4
A Reverse Ecology Approach Based on a Biological Definition of Microbial Populations
journal, August 2019
- Arevalo, Philip; VanInsberghe, David; Elsherbini, Joseph
- Cell, Vol. 178, Issue 4
The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics
journal, January 2010
- Vieira-Silva, Sara; Rocha, Eduardo P. C.
- PLoS Genetics, Vol. 6, Issue 1
Genetic Isolation by Environment or Distance: Which Pattern of gene flow is most Common?: Special Section
journal, September 2013
- Sexton, Jason P.; Hangartner, Sandra B.; Hoffmann, Ary A.
- Evolution, Vol. 68, Issue 1
Bypassing Cultivation To Identify Bacterial Species: Culture-independent genomic approaches identify credibly distinct clusters, avoid cultivation bias, and provide true insights into microbial species
journal, March 2014
- Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
- Microbe Magazine, Vol. 9, Issue 3
Convergence of Campylobacter Species: Implications for Bacterial Evolution
journal, April 2008
- Sheppard, S. K.; McCarthy, N. D.; Falush, D.
- Science, Vol. 320, Issue 5873
What Is Speciation?
journal, March 2016
- Shapiro, B. Jesse; Leducq, Jean-Baptiste; Mallet, James
- PLOS Genetics, Vol. 12, Issue 3
A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus
journal, April 2016
- Wielgoss, Sébastien; Didelot, Xavier; Chaudhuri, Roy R.
- The ISME Journal, Vol. 10, Issue 10
Bacterial Species and Speciation
journal, August 2001
- Cohan, Frederick M.
- Systematic Biology, Vol. 50, Issue 4
Genetic isolation between two recently diverged populations of a symbiotic fungus
journal, April 2015
- Branco, Sara; Gladieux, Pierre; Ellison, Christopher E.
- Molecular Ecology, Vol. 24, Issue 11
Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton
journal, May 2008
- Hunt, D. E.; David, L. A.; Gevers, D.
- Science, Vol. 320, Issue 5879
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010
- Darling, Aaron E.; Mau, Bob; Perna, Nicole T.
- PLoS ONE, Vol. 5, Issue 6
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
A comparison of homologous recombination rates in bacteria and archaea
journal, October 2008
- Vos, Michiel; Didelot, Xavier
- The ISME Journal, Vol. 3, Issue 2
Inferring Horizontal Gene Transfer
journal, May 2015
- Ravenhall, Matt; Škunca, Nives; Lassalle, Florent
- PLOS Computational Biology, Vol. 11, Issue 5
PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies
journal, May 2012
- Akhter, Sajia; Aziz, Ramy K.; Edwards, Robert A.
- Nucleic Acids Research, Vol. 40, Issue 16
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
Nearly Neutrality and the Evolution of Codon Usage Bias in Eukaryotic Genomes: Figure 1.—
journal, April 2008
- Subramanian, Sankar
- Genetics, Vol. 178, Issue 4
Niche Partitioning Among Prochlorococcus Ecotypes Along Ocean-Scale Environmental Gradients
journal, March 2006
- Johnson, Z. I.
- Science, Vol. 311, Issue 5768
Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
journal, January 2014
- Doroghazi, James R.; Buckley, Daniel H.
- BMC Genomics, Vol. 15, Issue 1
Epidemic Clones, Oceanic Gene Pools, and Eco-LD in the Free Living Marine Pathogen Vibrio parahaemolyticus
journal, January 2015
- Cui, Yujun; Yang, Xianwei; Didelot, Xavier
- Molecular Biology and Evolution, Vol. 32, Issue 6
Latitude delineates patterns of biogeography in terrestrial Streptomyces: Biogeography of Streptomyces
journal, July 2016
- Choudoir, Mallory J.; Doroghazi, James R.; Buckley, Daniel H.
- Environmental Microbiology, Vol. 18, Issue 12
Neutral Theory, Microbial Practice: Challenges in Bacterial Population Genetics
journal, April 2018
- Rocha, Eduardo P. C.
- Molecular Biology and Evolution, Vol. 35, Issue 6
Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
journal, November 2017
- Chase, Alexander B.; Karaoz, Ulas; Brodie, Eoin L.
- mBio, Vol. 8, Issue 6
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Recombination Shapes the Natural Population Structure of the Hyperthermophilic Archaeon Sulfolobus islandicus
journal, August 2005
- Whitaker, Rachel J.; Grogan, Dennis W.; Taylor, John W.
- Molecular Biology and Evolution, Vol. 22, Issue 12
Patterns of Gene Flow Define Species of Thermophilic Archaea
journal, February 2012
- Cadillo-Quiroz, Hinsby; Didelot, Xavier; Held, Nicole L.
- PLoS Biology, Vol. 10, Issue 2
ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria
journal, October 2011
- Bi, Dexi; Xu, Zhen; Harrison, Ewan M.
- Nucleic Acids Research, Vol. 40, Issue D1
Isolation by landscape in populations of a prized edible mushroom Tricholoma matsutake
journal, March 2009
- Amend, Anthony; Garbelotto, Matteo; Fang, Zhendong
- Conservation Genetics, Vol. 11, Issue 3
A Latitudinal Diversity Gradient in Terrestrial Bacteria of the Genus Streptomyces
journal, April 2016
- Andam, Cheryl P.; Doroghazi, James R.; Campbell, Ashley N.
- mBio, Vol. 7, Issue 2
ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes
journal, February 2015
- Didelot, Xavier; Wilson, Daniel J.
- PLOS Computational Biology, Vol. 11, Issue 2
NCBI prokaryotic genome annotation pipeline
journal, June 2016
- Tatusova, Tatiana; DiCuccio, Michael; Badretdin, Azat
- Nucleic Acids Research, Vol. 44, Issue 14
CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins
journal, May 2018
- Couvin, David; Bernheim, Aude; Toffano-Nioche, Claire
- Nucleic Acids Research, Vol. 46, Issue W1
HMMER web server: interactive sequence similarity searching
journal, May 2011
- Finn, R. D.; Clements, J.; Eddy, S. R.
- Nucleic Acids Research, Vol. 39, Issue suppl
Phylogenetic conservatism of thermal traits explains dispersal limitation and genomic differentiation of Streptomyces sister-taxa
journal, June 2018
- Choudoir, Mallory J.; Buckley, Daniel H.
- The ISME Journal, Vol. 12, Issue 9
Evidence for Ecological Flexibility in the Cosmopolitan Genus Curtobacterium
journal, November 2016
- Chase, Alexander B.; Arevalo, Philip; Polz, Martin F.
- Frontiers in Microbiology, Vol. 7
LEA : An R package for landscape and ecological association studies
journal, May 2015
- Frichot, Eric; François, Olivier
- Methods in Ecology and Evolution, Vol. 6, Issue 8
Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes
journal, September 2007
- Zwirglmaier, Katrin; Jardillier, Ludwig; Ostrowski, Martin
- Environmental Microbiology, Vol. 0, Issue 0
A global map of genetic diversity in Babesia microti reveals strong population structure and identifies variants associated with clinical relapse
journal, June 2016
- Lemieux, Jacob E.; Tran, Alice D.; Freimark, Lisa
- Nature Microbiology, Vol. 1, Issue 7
Emergence of soil bacterial ecotypes along a climate gradient: Soil ecotypes along a climate gradient
journal, October 2018
- Chase, Alexander B.; Gomez-Lunar, Zulema; Lopez, Alberto E.
- Environmental Microbiology, Vol. 20, Issue 11
The ecology of transfer of mobile genetic elements
journal, November 2002
- Elsas, Jan Dirk; Bailey, Mark J.
- FEMS Microbiology Ecology, Vol. 42, Issue 2
The importance of resolving biogeographic patterns of microbial microdiversity
journal, January 2018
- Chase, Alexander B.; Martiny, Jennifer BH
- Microbiology Australia, Vol. 39, Issue 1
IND-enzymes: a repository for hydrolytic enzymes derived from thermophilic and psychrophilic bacterial species with potential industrial usage
journal, May 2021
- Sunny, Jithin S.; Nisha, Khairun; Natarajan, Anuradha
- Extremophiles, Vol. 25, Issue 4
The ecology of transfer of mobile genetic elements
journal, November 2002
- Vanelsas, J.; Bailey, M.
- FEMS Microbiology Ecology, Vol. 42, Issue 2
Genome-Wide SNP discovery and genomic characterization in avocado (Persea americana Mill.)
journal, December 2019
- Talavera, Alicia; Soorni, Aboozar; Bombarely, Aureliano
- Scientific Reports, Vol. 9, Issue 1
Microbial diversity and soil functions
journal, January 2017
- Nannipieri, P.; Ascher, J.; Ceccherini, M. T.
- European Journal of Soil Science, Vol. 68, Issue 1
Strain-Resolved Dynamics of the Lung Microbiome in Patients with Cystic Fibrosis
journal, April 2021
- Dmitrijeva, Marija; Kahlert, Christian R.; Feigelman, Rounak
- mBio, Vol. 12, Issue 2
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
text, January 2014
- Stamatakis, A.
- Karlsruhe
Inferring Horizontal Gene Transfer
text, January 2015
- Ravenhall, Matt; Škunca, Nives; Lassalle, Florent
- ETH Zurich
Works referencing / citing this record:
How can microbial population genomics inform community ecology?
journal, March 2020
- VanInsberghe, David; Arevalo, Philip; Chien, Diana
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798