Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer
Abstract
Background: 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. Results: Here 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 andmore »
- Authors:
- Publication Date:
- Research Org.:
- Argonne National Laboratory, Argonne, IL (United States). Advanced Photon Source (APS); Lawrence Berkeley National Laboratory (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)
- OSTI Identifier:
- 1618552
- Alternate Identifier(s):
- OSTI ID: 1373380; OSTI ID: 1377592
- Grant/Contract Number:
- SC0004765; GBMF3788; AC02-06CH11357; AC02-05CH11231; OCE0940390
- Resource Type:
- Published Article
- Journal Name:
- BMC Genomics
- Additional Journal Information:
- Journal Name: BMC Genomics Journal Volume: 17 Journal Issue: 1; Journal ID: ISSN 1471-2164
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- 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 Kingdom: 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 Kingdom. https://doi.org/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 Kingdom. https://doi.org/10.1186/s12864-016-3286-x.
@article{osti_1618552,
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 = {Background: 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. Results: Here 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. Conclusions: 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 Kingdom},
year = {Wed Nov 16 00:00:00 EST 2016},
month = {Wed Nov 16 00:00:00 EST 2016}
}
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https://doi.org/10.1186/s12864-016-3286-x
https://doi.org/10.1186/s12864-016-3286-x
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Cited by: 66 works
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Figures / Tables:
Fig. 1: Phylogenomic analyses of 142 cyanophages. a Unrooted phylogenomic maximum likelihood tree of 51 concatenated core genes (see Additional file 2: Table S2) in 142 genome-sequenced isolates reveals 10 distinct cyanophage genomic lineages. Six lineages (designated I-VI) contain three or more representatives, while the remaining four are less well-representedmore »
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