Lysogenic virus–host interactions predominate at deep-sea diffuse-flow hydrothermal vents

Williamson, Shannon J.; Cary, S. Craig; Williamson, Kurt E.; Helton, Rebekah R.; Bench, Shellie R.; Winget, Danielle M.; Wommack, K. Eric

doi:10.1038/ismej.2008.73

Cited by 116 publications

(116 citation statements)

References 49 publications

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“…In addition, viral production in the mud volcanoes investigated was significantly higher (up to one order of magnitude) than that of the control sediments. Recent studies have indicated that lysogenic infection can prevail on the lytic strategy both in shallow and deep hydrothermal vent ecosystems (Williamson et al, 2008;Maugeri et al, 2010). However, our results suggest that the environmental conditions of mud volcanoes promote high rates of viral replication through lytic infection, which indicates that these ecosystems represent hot spots of viral activity.…”

Section: Discussioncontrasting

confidence: 54%

Viral infections stimulate the metabolism and shape prokaryotic assemblages in submarine mud volcanoes

2011

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Mud volcanoes are geological structures in the oceans that have key roles in the functioning of the global ecosystem. Information on the dynamics of benthic viruses and their interactions with prokaryotes in mud volcano ecosystems is still completely lacking. We investigated the impact of viral infection on the mortality and assemblage structure of benthic prokaryotes of five mud volcanoes in the Mediterranean Sea. Mud volcano sediments promote high rates of viral production (1.65-7.89 Â 10 9 viruses g À1 d À1 ), viral-induced prokaryotic mortality (VIPM) (33% cells killed per day) and heterotrophic prokaryotic production (3.0-8.3 lgC g À1 d À1 ) when compared with sediments outside the mud volcano area. The viral shunt (that is, the microbial biomass converted into dissolved organic matter as a result of viral infection, and thus diverted away from higher trophic levels) provides 49 mgC m À2 d À1 , thus fuelling the metabolism of uninfected prokaryotes and contributing to the total C budget. Bacteria are the dominant components of prokaryotic assemblages in surface sediments of mud volcanoes, whereas archaea dominate the subsurface sediment layers. Multivariate multiple regression analyses show that prokaryotic assemblage composition is not only dependant on the geochemical features and processes of mud volcano ecosystems but also on synergistic interactions between bottom-up (that is, trophic resources) and top-down (that is, VIPM) controlling factors. Overall, these findings highlight the significant role of the viral shunt in sustaining the metabolism of prokaryotes and shaping their assemblage structure in mud volcano sediments, and they provide new clues for our understanding of the functioning of cold-seep ecosystems.

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Section: Discussioncontrasting

confidence: 54%

Viral infections stimulate the metabolism and shape prokaryotic assemblages in submarine mud volcanoes

2011

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“…As prokaryotes living in the marine deep subsurface are mainly prone to starvation (Jørgensen and D'Hondt, 2006), our study demonstrates the link between lysogeny and extreme environments such as the energy-poor marine subsurface. Other extreme habitats like energy-rich deep-sea hydrothermal vents can even be dominated by lysogens (Williamson et al, 2008). Previously, we found prophages in a variety of different phylogenetic groups isolated from the marine deep subsurface (Engelhardt et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments

et al. 2012

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Bacteriophages might be the main 'predators' in the marine deep subsurface and probably have a major impact on indigenous microbial communities. To identify their function within this habitat, we have determined their abundance and distribution along the sediment columns of two continental margin and two open ocean sites that were recovered during Leg 201 of the Ocean Drilling Program. For all investigated sites, viral abundance followed the total cell numbers with a virus-to-cell ratio between 1 and 10 in the upper 100 mbsf (meters below seafloor). An increasing ratio of about 20 in deeper layers indicated an ongoing viral production in up to 11 Ma old sediments. We have used Rhizobium radiobacter as the most frequently isolated organism from the deep subsurface with a high in situ abundance to identify the frequency of associated rhizobiophages. In this study, 16S rRNA gene copies of R. radiobacter accounted for up to 5.6% of total bacterial 16S rRNA genes (average: 0.75%) as detected by quantitative PCR. A distinctive distribution was identified for R. radiobacter as indicated by a site-specific arrangement of genetically similar populations. Whole genome information of rhizobiophage RR1-A was used to generate a primer system for quantitative PCR specifically targeting the prophage antirepressor gene, indicative for temperate phages. The quantification of this gene within various sediment horizons showed a contribution of temperate phages of up to 14.3% to the total viral abundance. Thus, the high amount of temperate phages within the sediments and among all investigated isolates indicates that lysogeny is the main viral proliferation mode in deep subsurface populations.

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“…The amount of virus-induced prokaryotic mortality increases with water column depth, to 80% in open ocean sediments, indicating that the release of carbon from microbial cells through viral lysis is very important in deep-sea sediments. This means that lytic viruses are prevalent in deep-sea sediments, in contrast to other marine environments, such as hydrothermal plumes (see below) (266,430,609,615). The viral shunt is estimated to account for ϳ0.37 to 0.63 Gt C year Ϫ1 in the deep sea, providing organic carbon to fuel 35% of benthic metabolism.…”

Section: General Physical and Chemical Characteristicsmentioning

confidence: 99%

Microbial Ecology of the Dark Ocean above, at, and below the Seafloor

Orcutt

Sylvan

Knab

et al. 2011

Microbiol Mol Biol Rev

603

499

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SUMMARY The majority of life on Earth—notably, microbial life—occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean—the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.—has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.

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Lysogenic virus–host interactions predominate at deep-sea diffuse-flow hydrothermal vents

Cited by 116 publications

References 49 publications

Viral infections stimulate the metabolism and shape prokaryotic assemblages in submarine mud volcanoes

Viral infections stimulate the metabolism and shape prokaryotic assemblages in submarine mud volcanoes

Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments

Microbial Ecology of the Dark Ocean above, at, and below the Seafloor

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