Abstract
Recent diversity studies have revealed that microbial communities of natural environments are dominated by species-like, sequence-discrete populations. However, how stable the sequence and gene-content diversity are within these populations and especially in highly dynamic lotic habitats remain unclear. Here we quantified the dynamics of intra-population diversity in samples spanning two years and five sites in the Kalamas River (Northwest Greece). A significant positive correlation was observed between higher intra-population sequence diversity and longer persistence over time, revealing that more diverse populations tended to represent more autochthonous (vs. allochthonous) community members. Assessment of intra-population gene-content changes caused by strain replacement or gene loss over time revealed different profiles with the majority of populations exhibiting gene-content changes close to 10% of the total genes, while one population exhibited ~21% change. The variable genes were enriched in hypothetical proteins and mobile elements, and thus, were probably functionally neutral or attributable to phage predation. A few notable exceptions to this pattern were also noted such as phototrophy-related proteins in summer vs. winter populations. Taken together, these results revealed that some freshwater genomes are remarkably dynamic, even across short time and spatial scales, and have implications for the bacterial species concept and microbial source tracking.
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References
Ghai R, Rodriguez-Valera F, McMahon KD, Toyama D, Rinke R, Cristina Souza de Oliveira T, et al. Metagenomics of the water column in the pristine upper course of the Amazon river. PLoS ONE. 2011;6:e23785.
Read DS, Gweon HS, Bowes MJ, Newbold LK, Field D, Bailey MJ, et al. Catchment-scale biogeography of riverine bacterioplankton. ISME J. 2015;9:516–26.
Portillo MC, Anderson SP, Fierer N. Temporal variability in the diversity and composition of stream bacterioplankton communities. Environ Microbiol. 2012;14:2417–28.
Savio D, Sinclair L, Ijaz UZ, Parajka J, Reischer GH, Stadler P. et al. Bacterial diversity along a 2600 km river continuum. Environ Microbiol. 2015;17:4994–5007.
Van Rossum T, Peabody MA, Uyaguari-Diaz MI, Cronin KI, Chan M, Slobodan JR. et al. Year-long metagenomic study of river microbiomes across land use and water quality. Front Microbiol. 2015;16:1405
Meziti A, Tsementzi D, Ar. Kormas K, Karayanni H, Konstantinidis KT. Anthropogenic effects on bacterial diversity and function along a river-to-estuary gradient in Northwest Greece revealed by metagenomics. Environ Microbiol. 2016;18:4640–52.
Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, et al. Opinion: re-evaluating prokaryotic species. Nat Rev Microbiol. 2005;3:733–9.
Rodriguez RLM, Castro JC, Kyrpides NC, Cole JR, Tiedje JM, Konstantinidis KT. How much do rRNA gene surveys underestimate extant bacterial diversity?. Appl Environ Microbiol. 2018;84:e00014–8.
Konstantinidis KT, DeLong EF. Genomic patterns of recombination, clonal divergence and environment in marine microbial populations. ISME J. 2008;2:1052–65.
Caro-Quintero A, Konstantinidis KT. Bacterial species may exist, metagenomics reveal. Environ Microbiol. 2012;14:347–55.
Schneider D, Duperchy E, Depeyrot J, Coursange E, Lenski RE, Blot M. Genomic comparisons among Escherichia coli strains B, K-12, and O157:H7 using IS elements as molecular markers. BMC Microbiol. 2002;2:18.
Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, et al. Population genomics of early events in the ecological differentiation of bacteria. Science. 2012;336:48–51.
Oh S, Caro-Quintero A, Tsementzi D, DeLeon-Rodriguez N, Luo C, Poretsky R, et al. Metagenomic insights into the evolution, function, and complexity of the planktonic microbial community of Lake Lanier, a temperate freshwater ecosystem. Appl Environ Microbiol. 2011;77:6000–11.
Tsementzi D, Poretsky R, Rodriguez-R LM, Luo C, Konstantinidis KT. Evaluation of metatranscriptomic protocols and application to the study of freshwater microbial communities. Environ Microbiol Rep. 2014;6:640–55.
Johnston ER, Rodriguez-R LM, Luo C, Yuan MM, Wu L, He Z, et al. Metagenomics reveals pervasive bacterial populations and reduced community diversity across the Alaska Tundra ecosystem. Front Microbiol. 2016;7:579.
Bendall ML, Stevens SL, Chan L-K, Malfatti S, Schwientek P, Tremblay J, et al. Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. ISME J. 2016;10:1589–601.
Cox MP, Peterson DA, Biggs PJ. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinforma. 2010;11:485.
Peng Y, Leung HCM, Yiu SM, Chin FYL. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics. 2012;28:1420–8.
Zhu W, Lomsadze A, Borodovsky M. Ab initio gene identification in metagenomic sequences. Nucl Acids Res. 2010;38:e132.
Wu Y-W, Tang Y-H, Tringe SG, Simmons BA, Singer SW. MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbiome. 2014;2:26.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, et al. The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res. 2018;46:W282–8.
Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr. 2016;4:e1900v1.
Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res. 2014;42:e73.
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.
Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12:656–64.
Luo C, Tsementzi D, Kyrpides NC, Konstantinidis KT. Individual genome assembly from complex community short-read metagenomic datasets. ISME J. 2012;6:898–901.
Rodriguez-R LM, Konstantinidis KT. Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets. Bioinformatics. 2014;30:629–35.
Tsementzi D, Wu J, Deutsch S, Nath S, Rodriguez-R LM, Burns AS, et al. SAR11 bacteria linked to ocean anoxia and nitrogen loss. Nature. 2016;536:179–83.
Crump BC, Amaral-Zettler LA, Kling GW. Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J. 2012;6:1629–39.
Zeglin LH. Stream microbial diversity in response to environmental changes: review and synthesis of existing research. Front Microbiol. 2015;18:454
Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA. 2005;102:2567–72.
Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K, Kyrpides NC, et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res. 2015;43:6761–71.
Garcia SL, Stevens SLR, Crary B, Martinez-Garcia M, Stepanauskas R, Woyke T, et al. Contrasting patterns of genome-level diversity across distinct co-occurring bacterial populations. ISME J. 2018;12:742–55.
Spero MA, Aylward FO, Currie CR, Donohue TJ. Phylogenomic analysis and predicted physiological role of the proton-translocating NADH:quinone oxidoreductase (Complex I) across bacteria. mBio. 2015;6:e00389–15.
Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, et al. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotech. 2004;22:55–61.
Nagashima KVP, Hiraishi A, Shimada K, Matsuura K. Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol. 1997;45:131–6.
Zheng Q, Lin W, Liu Y, Chen C, Jiao N. A comparison of 14 erythrobacter genomes provides insights into the genomic divergence and scattered distribution of phototrophs. Front Microbiol. 2016;7:984
Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 2006;4:e234.
Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci. 2006;361:1929–40.
Akhter S, Aziz RK, Edwards RA. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res. 2012;40:e126.
Acknowledgements
This research was supported, in part, by the US National Science Foundation (award DEB 1241046 to KTK), the European Union (European Regional Development Fund- ERDF), and Greek national funds through the Operational Program “THESSALY- MAINLAND GREECE AND EPIRUS-2007-2013” of the National Strategic Reference Framework (NSRF 2007–2013) (2012–2015). We are grateful to the Management Body of Straits and Estuaries of the Rivers Acheron and Kalamas and to Theofilos Vanikiotis for providing helpful information on the sampling area as well as sampling facilities, and to an anonymous reviewer for providing useful suggestions regarding the manuscript.
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Meziti, A., Tsementzi, D., Rodriguez-R, L.M. et al. Quantifying the changes in genetic diversity within sequence-discrete bacterial populations across a spatial and temporal riverine gradient. ISME J 13, 767–779 (2019). https://doi.org/10.1038/s41396-018-0307-6
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DOI: https://doi.org/10.1038/s41396-018-0307-6
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