Photosynthesis genes in marine viruses yield proteins during host infection

Lindell, Debbie; Jaffe, Jacob D.; Johnson, Zackary I.; Church, George M.; Chisholm, Sallie W.

doi:10.1038/nature04111

Cited by 449 publications

(471 citation statements)

References 29 publications

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“…One such example of channelization may be photosynthesis genes transferred by phages in Prochlorococcus. These genes are carried by phage and have been suggested to increase their fitness during infection by increasing gene dosage for proteins with extremely high turnover in the host cell (Lindell et al 2005). However, the phage may also act as a highly efficient gene transfer agent, which may spread alleles within or among populations that are adaptive from the host's point of view.…”

Section: Towards Bacterial Population Genomics In the Oceanmentioning

confidence: 99%

Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Polz

Hunt

Preheim

et al. 2006

Phil. Trans. R. Soc. B

173

156

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Microbes in the ocean dominate biogeochemical processes and are far more diverse than anticipated. Thus, in order to understand the ocean system, we need to delineate microbial populations with predictable ecological functions. Recent observations suggest that ocean communities comprise diverse groups of bacteria organized into genotypic (and phenotypic) clusters of closely related organisms. Although such patterns are similar to metazoan communities, the underlying mechanisms for microbial communities may differ substantially. Indeed, the potential among ocean microbes for vast population sizes, extensive migration and both homologous and illegitimate genetic recombinations, which are uncoupled from reproduction, challenges classical population models primarily developed for sexually reproducing animals. We examine possible mechanisms leading to the formation of genotypic clusters and consider alternative population genetic models for differentiation at individual loci as well as gene content at the level of whole genomes. We further suggest that ocean bacteria follow at least two different adaptive strategies, which constrain rates and bounds of evolutionary processes: the 'opportuni-troph', exploiting spatially and temporally variable resources; and the passive oligotroph, efficiently using low nutrient concentrations. These ecological lifestyle differences may represent a fundamental divide with major consequences for growth and predation rates, genome evolution and population diversity, as emergent properties driving the division of labour within microbial communities.

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Section: Towards Bacterial Population Genomics In the Oceanmentioning

confidence: 99%

Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Polz

Hunt

Preheim

et al. 2006

Phil. Trans. R. Soc. B

173

156

View full text Add to dashboard Cite

show abstract

“…An emerging paradigm is that viruses also possess auxiliary metabolic genes (AMGs; Breitbart et al, 2007)-'host' genes that may be expressed to augment viral-infected host metabolism and facilitate production of new viruses (reviewed in Breitbart (2012) and Rohwer and Thurber (2009)). Due to the availability of cultures and genomes, AMGs are most extensively explored in marine cyanophages (viruses that infect cyanobacteria) and include genes involved in photosynthesis, carbon metabolism, phosphate metabolism and stress response (Mann et al, 2003;Lindell et al, 2004Lindell et al, , 2005Sullivan et al, 2005;Clokie et al, 2006;Sullivan et al, 2006;Weigele et al, 2007;Dammeyer et al, 2008;Millard et al, 2009;Thompson et al, 2011;Zeng and Chisholm, 2012;Frank et al, 2013). AMGs have also been observed in other cultivated viral isolates including genes for sugar metabolism, lipid-fatty acid metabolism and signalling (Derelle et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…This might best be exemplified by cyanophages and 'phage photosynthesis' (Mann et al, 2003). Briefly, cyanophage genomes nearly universally contain the core photosystem II gene psbA (Sullivan et al, 2006) that is expressed during infection (Lindell et al, 2005;Clokie et al, 2006). This gene has been shown to increase cyanophage fitness (Bragg and Chisholm, 2008), and commonly constitutes a large fraction of total psbA genes in marine microbial metagenomes (Sharon et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome

2014

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Microbes drive myriad ecosystem processes, and their viruses modulate microbial-driven processes through mortality, horizontal gene transfer, and metabolic reprogramming by viral-encoded auxiliary metabolic genes (AMGs). However, our knowledge of viral roles in the oceans is primarily limited to surface waters. Here we assess the depth distribution of protein clusters (PCs) in the first large-scale quantitative viral metagenomic data set that spans much of the pelagic depth continuum (the Pacific Ocean Virome; POV). This established ‘core’ (180 PCs; one-third new to science) and ‘flexible’ (423K PCs) community gene sets, including niche-defining genes in the latter (385 and 170 PCs are exclusive and core to the photic and aphotic zones, respectively). Taxonomic annotation suggested that tailed phages are ubiquitous, but not abundant (<5% of PCs) and revealed depth-related taxonomic patterns. Functional annotation, coupled with extensive analyses to document non-viral DNA contamination, uncovered 32 new AMGs (9 core, 20 photic and 3 aphotic) that introduce ways in which viruses manipulate infected host metabolism, and parallel depth-stratified host adaptations (for example, photic zone genes for iron–sulphur cluster modulation for phage production, and aphotic zone genes for high-pressure deep-sea survival). Finally, significant vertical flux of photic zone viruses to the deep sea was detected, which is critical for interpreting depth-related patterns in nature. Beyond the ecological advances outlined here, this catalog of viral core, flexible and niche-defining genes provides a resource for future investigation into the organization, function and evolution of microbial molecular networks to mechanistically understand and model viral roles in the biosphere.

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“…The wastewater studies are particularly revealing about the ability of phages to carry host genes, as these studies identify diverse bacterial 16S ribosomal DNA sequences in the viral component of the waste water 111,112 . Some phages are thought to carry cellular genes because of a selective advantage that is accrued by the phage host, as exemplified by the photosynthesis genes that are carried by cyanophages 113 . Many viral metagenomes contain a large proportion of sequences with homologues that are classified as cellular in GenBank 86 , but it is uncertain what proportion of these are homologues of prophage genes in bacterial genomes rather than homologues of cellular genes that are packaged by the phages.…”

mentioning

confidence: 99%

Gene transfer agents: phage-like elements of genetic exchange

2012

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Horizontal gene transfer is important in the evolution of bacterial and archaeal genomes. An interesting genetic exchange process is carried out by diverse phage-like gene transfer agents (GTAs) that are found in a wide range of prokaryotes. Although GTAs resemble phages, they lack the hallmark capabilities that define typical phages, and they package random pieces of the producing cell's genome. In this Review, we discuss the defining characteristics of the GTAs that have been identified to date, along with potential functions for these agents and the possible evolutionary forces that act on the genes involved in their production.The prevalence of horizontal gene transfer (HGT), in which DNA is exchanged between closely or distantly related lineages, has altered the way we think about evolution 1,2 , having profound effects on our views of the evolutionary relationships among living organisms. It has caused a shift from a bifurcating 'tree of life' view to a 'net of life' or 'web of life' view [3][4][5] , in which "highways of gene sharing" (REF. 6) represent major connections, with genes (or DNA segments) viewed as "public goods, available for all organisms to integrate into their genomes" (REF. 7). HGT occurs within and between all three domains of life, and it has been estimated that 0.05-80% of genes in bacterial and archaeal genomes have been affected by HGT, depending on the analytical method used and the genome analysed [8][9][10] . Although HGT is widespread, it is not random: patterns of preferential gene exchange among specific groups of organisms that share ancestry or habitat have been * Present address. aslang@mun.ca; olgazh@dartmouth.edu; j.beatty@mail.ubc.ca Competing interests statementThe authors declare no competing financial interests. 6,9,11,12 . Such patterns are probably a consequence of existing barriers to HGT, which have been reviewed in detail elsewhere 13,14 . FURTHER INFORMATIONAlthough we have known about some HGT mechanisms for decades, novel processes that expand the existing repertoire of gene exchange methods are continually being identified. Transformation was the first mechanism of gene exchange to be discovered 15 , wherein DNA is taken up directly from the environment (reviewed elsewhere 16,17 ). In transduction, DNA transfer is mediated by viral particles (BOX 1). In conjugation, which was discovered in the 1940s 18 , DNA is transferred from a donor to a recipient cell during cell-to-cell contact; conjugation is used in the transfer of plasmids, transposons, integrons, and integrative and conjugative elements (ICEs) [19][20][21] . There are other modes of gene exchange that do not fit well into any of these three canonical mechanisms, including temporary cell fusion followed by chromosomal recombination and plasmid exchange 22 , intercellular connection through nanotubes 23 , and the release of membrane vesicles containing chromosomal, plasmid and phage DNA that can then merge with nearby cells 24 . In addition, a novel mechanism of gene transfer that has feature...

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Photosynthesis genes in marine viruses yield proteins during host infection

Cited by 449 publications

References 29 publications

Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome

Gene transfer agents: phage-like elements of genetic exchange

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