Contrasting patterns of genome-level diversity across distinct co-occurring bacterial populations

Garcia, Sarahi L.; Stevens, Sarah L. R.; Crary, Benjamin; Martinez-Garcia, Manuel; Stepanauskas, Ramunas; Woyke, Tanja; Tringe, Susannah G.; Andersson, Siv G. E.; Bertilsson, Stefan; Malmstrom, Rex R.; McMahon, Katherine D.

doi:10.1038/s41396-017-0001-0

Title: Contrasting patterns of genome-level diversity across distinct co-occurring bacterial populations

Journal Article · Fri Dec 08 00:00:00 EST 2017 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-017-0001-0· OSTI ID:1459402

Garcia, Sarahi L. ^[1];

^[2]; Crary, Benjamin ^[2]; Martinez-Garcia, Manuel ^[3];

^[4]; Woyke, Tanja ^[5];

^[5]; Andersson, Siv G. E. ^[6]; Bertilsson, Stefan ^[6]; Malmstrom, Rex R. ^[5];

^[2]

Univ. of Wisconsin-Madison, Madison, WI (United States); Uppsala Univ., Uppsala (Sweden)
Univ. of Wisconsin-Madison, Madison, WI (United States)
Univ. of Alicante, Alicante (Spain)
Bigelow Lab for Ocean Sciences, East Boothbay, ME (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Uppsala Univ., Uppsala (Sweden)

To understand the forces driving differentiation and diversification in wild bacterial populations, we must be able to delineate and track ecologically relevant units through space and time. Mapping metagenomic sequences to reference genomes derived from the same environment can reveal genetic heterogeneity within populations, and in some cases, be used to identify boundaries between genetically similar, but ecologically distinct, populations. Here we examine population-level heterogeneity within abundant and ubiquitous freshwater bacterial groups such as the acI Actinobacteria and LD12 Alphaproteobacteria (the freshwater sister clade to the marine SAR11) using 33 single-cell genomes and a 5-year metagenomic time series. The single-cell genomes grouped into 15 monophyletic clusters (termed "tribes") that share at least 97.9% 16S rRNA identity. Distinct populations were identified within most tribes based on the patterns of metagenomic read recruitments to single-cell genomes representing these tribes. Genetically distinct populations within tribes of the acI Actinobacterial lineage living in the same lake had different seasonal abundance patterns, suggesting these populations were also ecologically distinct. In contrast, sympatric LD12 populations were less genetically differentiated. This suggests that within one lake, some freshwater lineages harbor genetically discrete (but still closely related) and ecologically distinct populations, while other lineages are composed of less differentiated populations with overlapping niches. Our results point at an interplay of evolutionary and ecological forces acting on these communities that can be observed in real time.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1459402

Journal Information:: The ISME Journal, Vol. 12, Issue 3; Related Information: © 2017 The Author(s) 2017, under exclusive licence to Macmillan Publishers Limited, part of Springer Nature.; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 41 works

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References (47)

The first complete genome sequences of the acI lineage, the most abundant freshwater Actinobacteria, obtained by whole-genome-amplification of dilution-to-extinction cultures Kang, Ilnam; Kim, Suhyun; Islam, Md. Rashedul Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42252	journal	February 2017
Diversity and Seasonal Dynamics of Actinobacteria Populations in Four Lakes in Northeastern Germany Allgaier, M.; Grossart, H. -P. Applied and Environmental Microbiology, Vol. 72, Issue 5 https://doi.org/10.1128/AEM.72.5.3489-3497.2006	journal	May 2006
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
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
Infrequent Transitions between Saline and Fresh Waters in One of the Most Abundant Microbial Lineages (SAR11) Logares, R.; Brate, J.; Heinrich, F. Molecular Biology and Evolution, Vol. 27, Issue 2 https://doi.org/10.1093/molbev/msp239	journal	October 2009
Single-cell genomics reveal low recombination frequencies in freshwater bacteria of the SAR11 clade Zaremba-Niedzwiedzka, Katarzyna; Viklund, Johan; Zhao, Weizhou Genome Biology, Vol. 14, Issue 11 https://doi.org/10.1186/gb-2013-14-11-r130	journal	January 2013
Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment Kaeberlein, T. Science, Vol. 296, Issue 5570 https://doi.org/10.1126/science.1070633	journal	May 2002
Single cell genomics: an individual look at microbes Stepanauskas, Ramunas Current Opinion in Microbiology, Vol. 15, Issue 5 https://doi.org/10.1016/j.mib.2012.09.001	journal	October 2012
Abundances, Identity, and Growth State of Actinobacteria in Mountain Lakes of Different UV Transparency Warnecke, F.; Sommaruga, R.; Sekar, R. Applied and Environmental Microbiology, Vol. 71, Issue 9 https://doi.org/10.1128/AEM.71.9.5551-5559.2005	journal	September 2005
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus Kashtan, N.; Roggensack, S. E.; Rodrigue, S. Science, Vol. 344, Issue 6182 https://doi.org/10.1126/science.1248575	journal	April 2014
Interannual dynamics and phenology of bacterial communities in a eutrophic lake Shade, Ashley; Kent, Angela D.; Jones, Stuart E. Limnology and Oceanography, Vol. 52, Issue 2 https://doi.org/10.4319/lo.2007.52.2.0487	journal	March 2007
Comparative 16S rRNA Analysis of Lake Bacterioplankton Reveals Globally Distributed Phylogenetic Clusters Including an Abundant Group of Actinobacteria Glockner, F. O.; Zaichikov, E.; Belkova, N. Applied and Environmental Microbiology, Vol. 66, Issue 11 https://doi.org/10.1128/AEM.66.11.5053-5065.2000	journal	November 2000
Marine microbial community dynamics and their ecological interpretation Fuhrman, Jed A.; Cram, Jacob A.; Needham, David M. Nature Reviews Microbiology, Vol. 13, Issue 3 https://doi.org/10.1038/nrmicro3417	journal	February 2015
Genomic patterns of recombination, clonal divergence and environment in marine microbial populations Konstantinidis, Konstantinos T.; DeLong, Edward F. The ISME Journal, Vol. 2, Issue 10 https://doi.org/10.1038/ismej.2008.62	journal	June 2008
Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas Limnology and Oceanography, Vol. 55, Issue 2 https://doi.org/10.4319/lo.2010.55.2.0846	journal	February 2010
A Guide to the Natural History of Freshwater Lake Bacteria Newton, R. J.; Jones, S. E.; Eiler, A. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1 https://doi.org/10.1128/MMBR.00028-10	journal	March 2011
In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake Salcher, Michaela M.; Posch, Thomas; Pernthaler, Jakob The ISME Journal, Vol. 7, Issue 5 https://doi.org/10.1038/ismej.2012.162	journal	December 2012
Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers Zwart, G.; Crump, Bc; Kamst-van Agterveld, Mp Aquatic Microbial Ecology, Vol. 28 https://doi.org/10.3354/ame028141	journal	January 2002
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12) Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.8	journal	March 2011
PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes Segata, Nicola; Börnigen, Daniela; Morgan, Xochitl C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3304	journal	August 2013
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria Eiler, Alexander; Mondav, Rhiannon; Sinclair, Lucas The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2015.260	journal	January 2016
Metagenomic Insights into the Evolution, Function, and Complexity of the Planktonic Microbial Community of Lake Lanier, a Temperate Freshwater Ecosystem Oh, Seungdae; Caro-Quintero, Alejandro; Tsementzi, Despina Applied and Environmental Microbiology, Vol. 77, Issue 17 https://doi.org/10.1128/AEM.00107-11	journal	July 2011
Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species Luo, C.; Walk, S. T.; Gordon, D. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1015622108	journal	April 2011
Rules of Engagement: Interspecies Interactions that Regulate Microbial Communities Little, Ainslie E. F.; Robinson, Courtney J.; Peterson, S. Brook Annual Review of Microbiology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev.micro.030608.101423	journal	October 2008
Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden) Heinrich, F.; Eiler, A.; Bertilsson, S. Aquatic Microbial Ecology, Vol. 70, Issue 1 https://doi.org/10.3354/ame01637	journal	August 2013
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
The future is now: single-cell genomics of bacteria and archaea Blainey, Paul C. FEMS Microbiology Reviews, Vol. 37, Issue 3 https://doi.org/10.1111/1574-6976.12015	journal	May 2013
A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA Kara, Emily L.; Hanson, Paul C.; Hu, Yu Hen The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.118	journal	October 2012
Coherent dynamics and association networks among lake bacterioplankton taxa Eiler, Alexander; Heinrich, Friederike; Bertilsson, Stefan The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.113	journal	September 2011
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton Garcia, Sarahi L.; McMahon, Katherine D.; Martinez-Garcia, Manuel The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.86	journal	July 2012
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
Phylogenetic Ecology of the Freshwater Actinobacteria acI Lineage Newton, R. J.; Jones, S. E.; Helmus, M. R. Applied and Environmental Microbiology, Vol. 73, Issue 22 https://doi.org/10.1128/AEM.00794-07	journal	September 2007
Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage Ghylin, Trevor W.; Garcia, Sarahi L.; Moya, Francisco The ISME Journal, Vol. 8, Issue 12 https://doi.org/10.1038/ismej.2014.135	journal	August 2014
Genomic insights that advance the species definition for prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409727102	journal	February 2005
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas Limnology and Oceanography, Vol. 55, Issue 2 https://doi.org/10.4319/lo.2009.55.2.0846	journal	January 2010
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
Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing Ghai, Rohit; Mizuno, Carolina Megumi; Picazo, Antonio Molecular Ecology, Vol. 23, Issue 24 https://doi.org/10.1111/mec.12985	journal	November 2014
High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.84	journal	June 2011
Bacterial species may exist, metagenomics reveal: Bacterial species may exist Caro-Quintero, Alejandro; Konstantinidis, Konstantinos T. Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02668.x	journal	December 2011
Long-Term Characterization of Free-Living and Particle-Associated Bacterial Communities in Lake Tiefwaren Reveals Distinct Seasonal Patterns Rösel, Stefan; Allgaier, Martin; Grossart, Hans-Peter Microbial Ecology, Vol. 64, Issue 3 https://doi.org/10.1007/s00248-012-0049-3	journal	April 2012
Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Amann, R. I.; Ludwig, W.; Schleifer, K. H. Microbiological reviews, Vol. 59, Issue 1 https://doi.org/10.1128/MMBR.59.1.143-169.1995	journal	January 1995

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Wide Distribution of Phage That Infect Freshwater SAR11 Bacteria Chen, Lin-Xing; Zhao, Yanlin; McMahon, Katherine D. mSystems, Vol. 4, Issue 5 https://doi.org/10.1128/msystems.00410-19	journal	October 2019
Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade Delmont, Tom O.; Kiefl, Evan; Kilinc, Ozsel eLife, Vol. 8 https://doi.org/10.7554/elife.46497	journal	September 2019
Accurate and complete genomes from metagenomes Chen, Lin-Xing; Anantharaman, Karthik; Shaiber, Alon Genome Research, Vol. 30, Issue 3 https://doi.org/10.1101/gr.258640.119	journal	March 2020
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