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Title: Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer

Abstract

Genetic recombination is a driving force in genome evolution. Among viruses it has a dual role. For genomes with higher fitness, it maintains genome integrity in the face of high mutation rates. Conversely, for genomes with lower fitness, it provides immediate access to sequence space that cannot be reached by mutation alone. Understanding how recombination impacts the cohesion and dissolution of individual whole genomes within viral sequence space is poorly understood across double-stranded DNA bacteriophages (a.k.a phages) due to the challenges of obtaining appropriately scaled genomic datasets. Here in this study we explore the role of recombination in both maintaining and differentiating whole genomes of 142 wild double-stranded DNA marine cyanophages. Phylogenomic analysis across the 51 core genes revealed ten lineages, six of which were well represented. These phylogenomic lineages represent discrete genotypic populations based on comparisons of intra- and inter- lineage shared gene content, genome-wide average nucleotide identity, as well as detected gaps in the distribution of pairwise differences between genomes. McDonald-Kreitman selection tests identified putative niche-differentiating genes under positive selection that differed across the six well-represented genotypic populations and that may have driven initial divergence. Concurrent with patterns of recombination of discrete populations, recombination analyses of both genicmore » and intergenic regions largely revealed decreased genetic exchange across individual genomes between relative to within populations. Lastly, these findings suggest that discrete double-stranded DNA marine cyanophage populations occur in nature and are maintained by patterns of recombination akin to those observed in bacteria, archaea and in sexual eukaryotes.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [6];  [6];  [6];  [7];  [8];  [4];  [9]
  1. Univ. of Arizona, Tucson, AZ (United States). Dept. of Soil, Water and Environmental Science; The Ohio State Univ., Columbus, OH (United States). Dept. Microbiology
  2. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; The Ohio State Univ., Columbus, OH (United States). Dept. of Evolution, Ecology, and Organismal Biology
  3. Univ. of Arizona, Tucson, AZ (United States). Dept. of Molecular & Cellular Biology; Univ. of Southern California, Los Angeles, CA (United States). Dept. of Biological Sciences
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
  6. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  7. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biological Sciences; Georgia Inst. of Technology, Atlanta, GA (United States). School of Physics
  8. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States); Canadian Inst. for Advanced Research, Toronto (Canada). Integrated Microbial Biodiversity Program
  9. Univ. of Arizona, Tucson, AZ (United States). Dept. of Soil, Water and Environmental Science; Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Univ. of Arizona, Tucson, AZ (United States). Dept. of Molecular & Cellular Biology; The Ohio State Univ., Columbus, OH (United States). Dept. Microbiology; The Ohio State Univ., Columbus, OH (United States). Dept. of Evolution, Ecology, and Organismal Biology; The Ohio State Univ., Columbus, OH (United States). Dept. of Civil, Environmental and Geodetic Engineering
Publication Date:
Research Org.:
Argonne National Laboratory, Argonne, IL (United States). Advanced Photon Source (APS); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
Gordon and Betty Moore Foundation (GBMF); National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1373380
Alternate Identifier(s):
OSTI ID: 1377592
Grant/Contract Number:  
SC0004765; AC02-06CH11357; AC02-05CH11231; GBMF3788; OCE0940390
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 17; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacteriophage; Phage; Cyanophage; Virus; Evolution; Species; Double-stranded DNA

Citation Formats

Gregory, Ann C., Solonenko, Sergei A., Ignacio-Espinoza, J. Cesar, LaButti, Kurt, Copeland, Alex, Sudek, Sebastian, Maitland, Ashley, Chittick, Lauren, dos Santos, Filipa, Weitz, Joshua S., Worden, Alexandra Z., Woyke, Tanja, and Sullivan, Matthew B. Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. United States: N. p., 2016. Web. doi:10.1186/s12864-016-3286-x.
Gregory, Ann C., Solonenko, Sergei A., Ignacio-Espinoza, J. Cesar, LaButti, Kurt, Copeland, Alex, Sudek, Sebastian, Maitland, Ashley, Chittick, Lauren, dos Santos, Filipa, Weitz, Joshua S., Worden, Alexandra Z., Woyke, Tanja, & Sullivan, Matthew B. Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. United States. doi:10.1186/s12864-016-3286-x.
Gregory, Ann C., Solonenko, Sergei A., Ignacio-Espinoza, J. Cesar, LaButti, Kurt, Copeland, Alex, Sudek, Sebastian, Maitland, Ashley, Chittick, Lauren, dos Santos, Filipa, Weitz, Joshua S., Worden, Alexandra Z., Woyke, Tanja, and Sullivan, Matthew B. Wed . "Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer". United States. doi:10.1186/s12864-016-3286-x. https://www.osti.gov/servlets/purl/1373380.
@article{osti_1373380,
title = {Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer},
author = {Gregory, Ann C. and Solonenko, Sergei A. and Ignacio-Espinoza, J. Cesar and LaButti, Kurt and Copeland, Alex and Sudek, Sebastian and Maitland, Ashley and Chittick, Lauren and dos Santos, Filipa and Weitz, Joshua S. and Worden, Alexandra Z. and Woyke, Tanja and Sullivan, Matthew B.},
abstractNote = {Genetic recombination is a driving force in genome evolution. Among viruses it has a dual role. For genomes with higher fitness, it maintains genome integrity in the face of high mutation rates. Conversely, for genomes with lower fitness, it provides immediate access to sequence space that cannot be reached by mutation alone. Understanding how recombination impacts the cohesion and dissolution of individual whole genomes within viral sequence space is poorly understood across double-stranded DNA bacteriophages (a.k.a phages) due to the challenges of obtaining appropriately scaled genomic datasets. Here in this study we explore the role of recombination in both maintaining and differentiating whole genomes of 142 wild double-stranded DNA marine cyanophages. Phylogenomic analysis across the 51 core genes revealed ten lineages, six of which were well represented. These phylogenomic lineages represent discrete genotypic populations based on comparisons of intra- and inter- lineage shared gene content, genome-wide average nucleotide identity, as well as detected gaps in the distribution of pairwise differences between genomes. McDonald-Kreitman selection tests identified putative niche-differentiating genes under positive selection that differed across the six well-represented genotypic populations and that may have driven initial divergence. Concurrent with patterns of recombination of discrete populations, recombination analyses of both genic and intergenic regions largely revealed decreased genetic exchange across individual genomes between relative to within populations. Lastly, these findings suggest that discrete double-stranded DNA marine cyanophage populations occur in nature and are maintained by patterns of recombination akin to those observed in bacteria, archaea and in sexual eukaryotes.},
doi = {10.1186/s12864-016-3286-x},
journal = {BMC Genomics},
number = 1,
volume = 17,
place = {United States},
year = {Wed Nov 16 00:00:00 EST 2016},
month = {Wed Nov 16 00:00:00 EST 2016}
}

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Works referenced in this record:

Recombination in HIV-1
journal, March 1995

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