Abstract
Several reports proposed that the extraordinary dominance of the SAR11 bacterial clade in ocean ecosystems could be a consequence of unusual mechanisms of resistance to bacteriophage infection, including 'cryptic escape' through reduced cell size and/or K-strategist defence specialism. Alternatively, the evolution of high surface-to-volume ratios coupled with minimal genomes containing high-affinity transporters enables unusually efficient metabolism for oxidizing dissolved organic matter in the world's oceans that could support vast population sizes despite phage susceptibility. These ideas are important for understanding plankton ecology because they emphasize the potentially important role of top-down mechanisms in predation, thus determining the size of SAR11 populations and their concomitant role in biogeochemical cycling. Here we report the isolation of diverse SAR11 viruses belonging to two virus families in culture, for which we propose the name 'pelagiphage', after their host. Notably, the pelagiphage genomes were highly represented in marine viral metagenomes, demonstrating their importance in nature. One of the new phages, HTVC010P, represents a new podovirus subfamily more abundant than any seen previously, in all data sets tested, and may represent one of the most abundant virus subfamilies in the biosphere. This discovery disproves the theory that SAR11 cells are immune to viral predation and is consistent with the interpretation that the success of this highly abundant microbial clade is the result of successfully evolved adaptation to resource competition.
MeSH Terms
Aquatic Organisms/genetics,isolation & purification
Bacteria/classification,isolation & purification,virology
Bacteriophages/classification,genetics,isolation & purification,physiology
Bermuda
Biota
Competitive Behavior
Food Chain
Genome, Viral/genetics
Metagenome/genetics
Models, Biological
Molecular Sequence Data
Oregon
Pacific Ocean
Plankton/physiology
Seawater/microbiology,virology
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zhao Yanlin
Department of Microbiology, Oregon State University, Corvallis, Oregon 97331, USA.
Temperton Ben
Thrash J Cameron
Schwalbach Michael S
Vergin Kevin L
Landry Zachary C
Ellisman Mark
Deerinck Tom
Sullivan Matthew B
Giovannoni Stephen J
References (27)
27 references, click to expand
-
Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea.
ISME J. 2012 Feb;6(2):273-84
PMID: 21833038
-
Streamlining and core genome conservation among highly divergent members of the SAR11 clade.
mBio. 2012 Sep 18;3(5):
PMID: 22991429
-
The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology.
PLoS One. 2013;8(2):e57355
PMID: 23468974
-
Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method.
Environ Microbiol. 2012 Sep;14(9):2526-37
PMID: 22713159
-
DNA phosphorothioation is widespread and quantized in bacterial genomes.
Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):2963-8
PMID: 21285367
-
Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.
PLoS Biol. 2005 May;3(5):e144
PMID: 15828858
-
Phylogenomics of T4 cyanophages: lateral gene transfer in the 'core' and origins of host genes.
Environ Microbiol. 2012 Aug;14(8):2113-26
PMID: 22348436
-
High intraspecific recombination rate in a native population of Candidatus pelagibacter ubique (SAR11).
Environ Microbiol. 2007 Oct;9(10):2430-40
PMID: 17803769
-
Rapid diversification of coevolving marine Synechococcus and a virus.
Proc Natl Acad Sci U S A. 2012 Mar 20;109(12):4544-9
PMID: 22388749
-
Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing.
ISME J. 2010 Sep;4(9):1154-66
PMID: 20393571
-
Viral influence on aquatic bacterial communities.
Biol Bull. 2003 Apr;204(2):192-5
PMID: 12700152
-
Explaining microbial population genomics through phage predation.
Nat Rev Microbiol. 2009 Nov;7(11):828-36
PMID: 19834481
-
Marine viruses--major players in the global ecosystem.
Nat Rev Microbiol. 2007 Oct;5(10):801-12
PMID: 17853907
-
The marine viromes of four oceanic regions.
PLoS Biol. 2006 Nov;4(11):e368
PMID: 17090214
-
Seasonality and monthly dynamics of marine myovirus communities.
Environ Microbiol. 2012 Aug;14(8):2171-83
PMID: 22507260
-
Genomic and functional adaptation in surface ocean planktonic prokaryotes.
Nature. 2010 Nov 4;468(7320):60-6
PMID: 21048761
-
Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean.
Appl Environ Microbiol. 2005 Jun;71(6):2979-86
PMID: 15932993
-
A comparison of homologous recombination rates in bacteria and archaea.
ISME J. 2009 Feb;3(2):199-208
PMID: 18830278
-
The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'.
Environ Microbiol. 2009 Nov;11(11):2935-51
PMID: 19840100
-
Genomic island variability facilitates Prochlorococcus-virus coexistence.
Nature. 2011 Jun 29;474(7353):604-8
PMID: 21720364
-
Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments.
Environ Microbiol. 2010 Nov;12(11):3035-56
PMID: 20662890
-
Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools.
Res Microbiol. 2008 Jun;159(5):406-14
PMID: 18555669
-
A bacterial metapopulation adapts locally to phage predation despite global dispersal.
Genome Res. 2008 Feb;18(2):293-7
PMID: 18077539
-
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus.
Nature. 2003 Aug 28;424(6952):1047-51
PMID: 12944965
-
Cultivation of the ubiquitous SAR11 marine bacterioplankton clade.
Nature. 2002 Aug 8;418(6898):630-3
PMID: 12167859
-
Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data.
Biol Direct. 2007 Nov 07;2:27
PMID: 17988398
-
High diversity of the viral community from an Antarctic lake.
Science. 2009 Nov 6;326(5954):858-61
PMID: 19892985