Differential Functional Constraints Cause Strain-Level Endemism in Polynucleobacter Populations

Sangwan, Naseer; Zarraonaindia, Iratxe; Hampton-Marcell, Jarrad T.; Ssegane, Herbert; Eshoo, Tifani W.; Rijal, Geeta; Negri, M. Cristina; Gilbert, Jack A.

doi:10.1128/msystems.00003-16

Title: Differential Functional Constraints Cause Strain-Level Endemism in Polynucleobacter Populations

Journal Article · Tue May 24 00:00:00 EDT 2016 · mSystems

DOI:https://doi.org/10.1128/msystems.00003-16· OSTI ID:1626163

Sangwan, Naseer ^[1]; Zarraonaindia, Iratxe ^[2]; Hampton-Marcell, Jarrad T. ^[1]; Ssegane, Herbert ^[3]; Eshoo, Tifani W. ^[2]; Rijal, Geeta ^[4]; Negri, M. Cristina ^[3]; Gilbert, Jack A. ^[1]

Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division; Univ. of Chicago, Chicago, Illinois (United States). Dept. of Surgery and Dept. of Ecology and Evolution
Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
Argonne National Lab. (ANL), Argonne, IL (United States). Energy Systems Division
Metropolitan Water Reclamation District of Greater Chicago, Cicero, IL (United States)

The adaptation of bacterial lineages to local environmental conditions creates the potential for broader genotypic diversity within a species, which can enable a species to dominate across ecological gradients because of niche flexibility. The genus Polynucleobacter maintains both free-living and symbiotic ecotypes and maintains an apparently ubiquitous distribution in freshwater ecosystems. Subspecies-level resolution supplemented with metagenome-derived genotype analysis revealed that differential functional constraints, not geographic distance, produce and maintain strain-level genetic conservation in Polynucleobacter populations across three geographically proximal riverine environments. Genes associated with cofactor biosynthesis and one-carbon metabolism showed habitat specificity, and protein-coding genes of unknown function and membrane transport proteins were under positive selection across each habitat. Characterized by different median ratios of nonsynonymous to synonymous evolutionary changes (dN/dS ratios) and a limited but statistically significant negative correlation between the dN/dS ratio and codon usage bias between habitats, the free-living and core genotypes were observed to be evolving under strong purifying selection pressure. Highlighting the potential role of genetic adaptation to the local environment, the two-component system protein-coding genes were highly stable (dN/dS ratio, < 0.03). These results suggest that despite the impact of the habitat on genetic diversity, and hence niche partition, strong environmental selection pressure maintains a conserved core genome for Polynucleobacter populations.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

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

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1626163

Journal Information:: mSystems, Vol. 1, Issue 3; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

The GAAS Metagenomic Tool and Its Estimations of Viral and Microbial Average Genome Size in Four Major Biomes Angly, Florent E.; Willner, Dana; Prieto-Davó, Alejandra PLoS Computational Biology, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pcbi.1000593	journal	December 2009
Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data Eren, A. Murat; Maignien, Loïs; Sul, Woo Jun Methods in Ecology and Evolution, Vol. 4, Issue 12 https://doi.org/10.1111/2041-210X.12114	journal	October 2013
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt584	journal	October 2013
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments Suyama, M.; Torrents, D.; Bork, P. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl315	journal	July 2006
Bacterial competition: surviving and thriving in the microbial jungle Hibbing, Michael E.; Fuqua, Clay; Parsek, Matthew R. Nature Reviews Microbiology, Vol. 8, Issue 1 https://doi.org/10.1038/nrmicro2259	journal	November 2009
Metagenome Fragment Classification Using -Mer Frequency Profiles Rosen, Gail; Garbarine, Elaine; Caseiro, Diamantino Advances in Bioinformatics, Vol. 2008 https://doi.org/10.1155/2008/205969	journal	January 2008
Microevolutionary Genomics of Bacteria Jordan, I. King; Rogozin, Igor B.; Wolf, Yuri I. Theoretical Population Biology, Vol. 61, Issue 4 https://doi.org/10.1006/tpbi.2002.1588	journal	June 2002
FragGeneScan: predicting genes in short and error-prone reads Rho, Mina; Tang, Haixu; Ye, Yuzhen Nucleic Acids Research, Vol. 38, Issue 20 https://doi.org/10.1093/nar/gkq747	journal	August 2010
PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq) Kofler, R.; Pandey, R. V.; Schlotterer, C. Bioinformatics, Vol. 27, Issue 24 https://doi.org/10.1093/bioinformatics/btr589	journal	October 2011
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Average genome size estimation improves comparative metagenomics and sheds light on the functional ecology of the human microbiome Nayfach, Stephen; Pollard, Katherine S. Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0611-7	journal	March 2015
Recovering complete and draft population genomes from metagenome datasets Sangwan, Naseer; Xia, Fangfang; Gilbert, Jack A. Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0154-5	journal	March 2016
Ubiquity of Polynucleobacter necessarius subspecies asymbioticus results from ecological diversification: Ecological diversification in Polynucleobacter Jezbera, Jan; Jezberová, Jitka; Brandt, Ulrike Environmental Microbiology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1462-2920.2010.02396.x	journal	January 2011
Genome Sequence of a Freshwater Low-Nucleic-Acid-Content Bacterium, Betaproteobacterium Strain CB Hao, Z.; Li, L.; Liu, J. Genome Announcements, Vol. 1, Issue 2 https://doi.org/10.1128/genomeA.00135-13	journal	February 2013
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
PNAS Plus: From the Cover: Oligotyping analysis of the human oral microbiome Eren, A. M.; Borisy, G. G.; Huse, S. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 28 https://doi.org/10.1073/pnas.1409644111	journal	June 2014
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
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
Pan-genome dynamics of Pseudomonas gene complements enriched across hexachlorocyclohexane dumpsite Sharma, Anukriti; Sangwan, Naseer; Negi, Vivek BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1488-2	journal	April 2015
Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogenous 2000 km ² area Jezberová, Jitka; Jezbera, Jan; Brandt, Ulrike Environmental Microbiology, Vol. 12, Issue 3 https://doi.org/10.1111/j.1462-2920.2009.02106.x	journal	March 2010
AmphoraNet: The webserver implementation of the AMPHORA2 metagenomic workflow suite Kerepesi, Csaba; Bánky, Dániel; Grolmusz, Vince Gene, Vol. 533, Issue 2 https://doi.org/10.1016/j.gene.2013.10.015	journal	January 2014
Omikron , ein essentieller Endosymbiont von Euplotes aediculatus *† Heckmann, Klaus The Journal of Protozoology, Vol. 22, Issue 1 https://doi.org/10.1111/j.1550-7408.1975.tb00949.x	journal	February 1975
The Passive Yet Successful Way of Planktonic Life: Genomic and Experimental Analysis of the Ecology of a Free-Living Polynucleobacter Population Hahn, Martin W.; Scheuerl, Thomas; Jezberová, Jitka PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0032772	journal	March 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
Unsupervised discovery of microbial population structure within metagenomes using nucleotide base composition Saeed, Isaam; Tang, Sen-Lin; Halgamuge, Saman K. Nucleic Acids Research, Vol. 40, Issue 5 https://doi.org/10.1093/nar/gkr1204	journal	December 2011
Detecting putative orthologs Wall, D. P.; Fraser, H. B.; Hirsh, A. E. Bioinformatics, Vol. 19, Issue 13 https://doi.org/10.1093/bioinformatics/btg213	journal	September 2003
Ecological Succession and Viability of Human-Associated Microbiota on Restroom Surfaces Gibbons, Sean M.; Schwartz, Tara; Fouquier, Jennifer Applied and Environmental Microbiology, Vol. 81, Issue 2 https://doi.org/10.1128/AEM.03117-14	journal	November 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
Coupling Between Protein Level Selection and Codon Usage Optimization in the Evolution of Bacteria and Archaea Ran, Wenqi; Kristensen, David M.; Koonin, Eugene V. mBio, Vol. 5, Issue 2 https://doi.org/10.1128/mBio.00956-14	journal	March 2014
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
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
Metagenomic microbial community profiling using unique clade-specific marker genes Segata, Nicola; Waldron, Levi; Ballarini, Annalisa Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2066	journal	June 2012
Complete genome sequence of Polynucleobacter necessarius subsp. asymbioticus type strain (QLW-P1DMWA-1T) Meincke, Linda; Copeland, Alex; Lapidus, Alla Standards in Genomic Sciences, Vol. 6, Issue 1 https://doi.org/10.4056/sigs.2395367	journal	March 2012
Codon Deviation Coefficient: a novel measure for estimating codon usage bias and its statistical significance Zhang, Zhang; Li, Jun; Cui, Peng BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-43	journal	January 2012
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes Pati, Amrita; Ivanova, Natalia N.; Mikhailova, Natalia Nature Methods, Vol. 7, Issue 6 https://doi.org/10.1038/nmeth.1457	journal	May 2010
Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria Boscaro, V.; Felletti, M.; Vannini, C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 46 https://doi.org/10.1073/pnas.1316687110	journal	October 2013
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Metagenomic insights into microbial diversity in a groundwater basin impacted by a variety of anthropogenic activities Sonthiphand, Prinpida; Ruangroengkulrith, Siwat; Mhuantong, Wuttichai Environmental Science and Pollution Research, Vol. 26, Issue 26 https://doi.org/10.1007/s11356-019-05905-5	journal	July 2019
Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms Shalev, Or; Ashkenazy, Haim; Neumann, Manuela The ISME Journal, Vol. 16, Issue 5 https://doi.org/10.1038/s41396-021-01168-6	journal	December 2021
Infant gut microbiota characteristics generally do not modify effects of lipid-based nutrient supplementation on growth or inflammation: secondary analysis of a randomized controlled trial in Malawi Hughes, Riley L.; Arnold, Charles D.; Young, Rebecca R. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-71922-x	journal	September 2020

Cited By (2)

Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions Props, Ruben; Monsieurs, Pieter; Vandamme, Peter mSphere, Vol. 4, Issue 1 https://doi.org/10.1128/mspheredirect.00011-19	journal	February 2019
Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions García-García, Natalia; Tamames, Javier; Linz, Alexandra M. The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0487-8	journal	August 2019

Similar Records

Complete genome sequence of Polynucleobacter necessarius subsp. asymbioticus type strain (QLW-P1DMWA-1T)

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Standards in Genomic Sciences · OSTI ID:1626163

Meincke, Linda; Copeland, A; Lapidus, Alla L; +26 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:1626163

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

Genomic Features and Pervasive Negative Selection in Rhodanobacter Strains Isolated from Nitrate and Heavy Metal Contaminated Aquifer

Journal Article · Wed Feb 23 00:00:00 EST 2022 · Microbiology Spectrum · OSTI ID:1626163

Peng, Mu; Wang, Dongyu; Lui, Lauren M.; +15 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Microbiology

Title: Differential Functional Constraints Cause Strain-Level Endemism in Polynucleobacter Populations

Citation Formats

References (44)

Cited By (2)

Similar Records

Related Subjects