Widespread genetic exchange among terrestrial bacteriophages

Bacteriophages are the most numerous entities in the biosphere. Despite this numerical dominance, the genetic structure of bacteriophage populations is poorly understood. Here, we present a biogeography study involving 25 previously undescribed bacteriophages from the Cystoviridae clade, a group cha...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 102; no. 52; pp. 19009 - 19014
Main Authors Silander, O.K, Weinreich, D.M, Wright, K.M, O'Keefe, K.J, Rang, C.U, Turner, P.E, Chao, L
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 27.12.2005
National Acad Sciences
Subjects
Alleles
Bacteria
Bacteriophages
Bacteriophages - genetics
Biogeography
Biological Sciences
Biological taxonomies
Cystoviridae
Cystoviridae - genetics
double-stranded RNA
evolution
Evolutionary biology
Genetic exchange
Genetic mutation
genetic reassortment
genetic recombination
Genetic Variation
Genome, Viral
intrasegment recombination
isolation
leaves
Linkage Disequilibrium
Medical genetics
Models, Genetic
Molecular Sequence Data
Mutation
nucleotide sequences
Nucleotides
Phaseolus vulgaris
Phylogeny
Polymerase Chain Reaction
population genetics
Recombination, Genetic
RNA - genetics
RNA, Double-Stranded - chemistry
Sequence Analysis, DNA
Species Specificity
Trifolium repens
Viruses
Viruses - genetics
Connecticut
California
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Summary:Bacteriophages are the most numerous entities in the biosphere. Despite this numerical dominance, the genetic structure of bacteriophage populations is poorly understood. Here, we present a biogeography study involving 25 previously undescribed bacteriophages from the Cystoviridae clade, a group characterized by a dsRNA genome divided into three segments. Previous laboratory manipulation has shown that, when multiple Cystoviruses infect a single host cell, they undergo (i) rare intrasegment recombination events and (ii) frequent genetic reassortment between segments. Analyzing linkage disequilibrium (LD) within segments, we find no significant evidence of intrasegment recombination in wild populations, consistent with (i). An extensive analysis of LD between segments supports frequent reassortment, on a time scale similar to the genomic mutation rate. The absence of LD within this group of phages is consistent with expectations for a completely sexual population, despite the fact that some segments have >50% nucleotide divergence at 4-fold degenerate sites. This extraordinary rate of genetic exchange between highly unrelated individuals is unprecedented in any taxa. We discuss our results in light of the biological species concept applied to viruses.
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Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ273591-DQ273662).
Edited by Peter Palese, Mount Sinai School of Medicine, New York, NY
Present address: Department of Biology, P.O. Box 90338, Duke University, Durham, NC 27708.
Author contributions: O.K.S., D.M.W., K.J.O., C.U.R., P.E.T., and L.C. designed research; O.K.S., D.M.W., K.M.W., K.J.O., and C.U.R. performed research; O.K.S. and D.M.W. analyzed data; and O.K.S., D.M.W., P.E.T., and L.C. wrote the paper.
To whom correspondence should be addressed. E-mail: olin.silander@env.ethz.ch.
Abbreviations: LD, linkage disequilibrium; Pp, Pseudomonas syringae pathovar phaseolicola.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office.
O.K.S. and D.M.W. contributed equally to this work.
Present address: Eidgenössische Technische Hochschule Zurich, Ecology and Evolution, ETH-Zentrum NW 8092, Zurich, Switzerland.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0503074102