High potential for temperate viruses to drive carbon cycling in chemoautotrophy‐dominated shallow‐water hydrothermal vents

Rastelli, Eugenio; Corinaldesi, Cinzia; Dell’Anno, Antonio; Tangherlini, Michael; Martorelli, Eleonora; Ingrassia, Michela; Chiocci, Francesco Latino; Martire, Marco Lo; Danovaro, Roberto

doi:10.1111/1462-2920.13890

Cited by 21 publications

(14 citation statements)

References 98 publications

(147 reference statements)

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“…Lysogeny can favour transfer of viral genes between hosts by transduction [ 54 ]. Knowledge on biotic and abiotic factors in oxygen-limited environments that set the lysogeny-to-lytic switch will definitely shed new light on the role of temperate viruses in the microbial food web and energy transfer to higher trophic levels [ 62 ].…”

Section: Resultsmentioning

confidence: 99%

High Incidence of Lysogeny in the Oxygen Minimum Zones of the Arabian Sea (Southwest Coast of India)

Parvathi

Jasna

Aparna

et al. 2018

Viruses

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Though microbial processes in the oxygen minimum zones (OMZs) of the Arabian Sea (AS) are well documented, prokaryote-virus interactions are less known. The present study was carried out to determine the potential physico-chemical factors influencing viral abundances and their life strategies (lytic and lysogenic) along the vertical gradient in the OMZ of the AS (southwest coast of India). Water samples were collected during the southwest monsoon (SWM) season in two consecutive years (2015 and 2016) from different depths, namely, the surface layer, secondary chlorophyll a maxima (~30–40 m), oxycline (~70–80 m), and hypoxic/suboxic layers (~200–350 m). The high viral abundances observed in oxygenated surface waters (mean ± SD = 6.1 ± 3.4 × 106 viral-like particles (VLPs) mL−1), drastically decreased with depth in the oxycline region (1.2 ± 0.5 × 106 VLPs mL−1) and hypoxic/suboxic waters (0.3 ± 0.3 × 106 VLPs mL−1). Virus to prokaryote ratio fluctuated in the mixed layer (~10) and declined significantly (p < 0.001) to 1 in the hypoxic layer. Viral production (VP) and frequency of virus infected cells (FIC) were maximum in the surface and minimum in the oxycline layer, whereas the viral lysis was undetectable in the suboxic/hypoxic layer. The detection of a high percentage of lysogeny in suboxic (48%) and oxycline zones (9–24%), accompanied by undetectable rates of lytic viral infection support the hypothesis that lysogeny may represent the major survival strategy for viruses in unproductive or harsh nutrient/host conditions in deoxygenated waters.

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Section: Resultsmentioning

confidence: 99%

High Incidence of Lysogeny in the Oxygen Minimum Zones of the Arabian Sea (Southwest Coast of India)

Parvathi

Jasna

Aparna

et al. 2018

Viruses

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“…Our results observed the coupling of the viral lysis-lysogeny pattern and bacterial diversity, showing a high level of lysogeny accorded with dominance of active bacterial groups among the community with a lower bacterial Shannon index; in contrast, a higher bacterial Shannon index was found during the period with more viral lysis (Figure 2). The lysogen-dominant bacterial community would suffer a significant reduction in bacterial diversity, whereas the subsequent viral lysogeny to lysis switching due to prophage-induced direct killing of host bacteria would contribute to a dramatic increase in bacterial community diversity (Knowles et al, 2016; Pradeep Ram et al, 2016; Liu H. et al, 2017; Rastelli et al, 2017). During the experimental incubation, the succession of the bacterial community toward the initial status was observed after the lysogeny to lysis switching (Figure 3, 4), suggesting the importance of viruses in sustaining the bacterial community.…”

Section: Discussionmentioning

confidence: 99%

Viral Regulation on Bacterial Community Impacted by Lysis-Lysogeny Switch: A Microcosm Experiment in Eutrophic Coastal Waters

Chen

Yang

et al. 2019

Front. Microbiol.

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Marine viruses are major drivers of global biogeochemical cycles and energy fluxes, yet the importance of viral impacts on the succession and diversity of the bacterial community remains largely unexplored. Here, we explored viral life strategy and its potential effect on the bacterial community by experimental incubations of eutrophic coastal waters under lysogen-induced and non-induced treatments. The lysogen-induced treatment showed relatively constant viral and bacterial abundances, lytic and lysogenic viral production throughout the experimental period, together with the progressive declines in not only the relative abundances for SAR11, Rhodobacteraceae , Alteromonadaceae , and SAR86 but the bacterial community diversity. Conversely, the non-induced treatment observed the marked variation in the abundances of viruses, bacteria and cells with high nucleic acid content over the time course of incubation, which was congruent with the drastic shift in lytic and lysogenic viral production as well as the succession of bacterial community. Our results supported the hypotheses that a high level of lysogeny would occur with the increasing density of bacteria with rapid growth rate, which may contribute to a relatively lower host community diversity, whereas the lysogeny to lysis switching would fuel growth opportunities for less-active or initially rare bacterial taxa and generate a more diverse bacterial community. Altogether, the present study underscored the crucial regulatory role of the viral lysis-lysogeny pattern in bacterial community dynamics, composition and diversity, highlighting the viral impact on the microbial food web and biogeochemical processes.

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“…rRNA genes were predicted by cell wall/membrane/envelope biogenesis (6.33%); coenzyme transport and metabolism (5.97%); carbohydrate transport and metabolism (5.87%); and energy production and conversion (5.72%). [14,15]. In addition to acting as microbial predators, phages might confer an enhanced level of fitness to the microbial host, enhancing host survival in the extreme environment [16].…”

Section: Data Descriptionmentioning

confidence: 99%

Genome analysis of Crassaminicella sp. SY095, an anaerobic mesophilic marine bacterium isolated from a deep-sea hydrothermal vent on the Southwest Indian Ridge

Zhang

et al. 2020

Marine Genomics

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Crassaminicella sp. strain SY095 is an anaerobic mesophilic marine bacterium that was recently isolated from a deep-sea hydrothermal vent on the Southwest Indian Ridge. Here, we present the complete genome sequence of strain SY095. The genome consists of a chromosome of 3,046,753 bp (G+C content of 30.81%) and a plasmid of 36,627 bp (G+C content of 31.29%), encodes 2966 protein, 135 tRNA genes, and 34 rRNA genes. Numerous genes are related to peptide transport, amino acid metabolism, motility, and sporulation. This agrees with the observation that strain SY095 is a spore-forming, motile, and chemoheterotrophic bacterium. Further, the genome harbors multiple prophages that carry all the genes necessary for viral particle synthesis. Some prophages carry additional genes that may be involved in the regulation of sporulation. This is the first reported genome of a bacterium from the genus Crassaminicella, providing insights into the microbial adaptation strategies to the deep-sea hydrothermal vent environment.

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High potential for temperate viruses to drive carbon cycling in chemoautotrophy‐dominated shallow‐water hydrothermal vents

Cited by 21 publications

References 98 publications

High Incidence of Lysogeny in the Oxygen Minimum Zones of the Arabian Sea (Southwest Coast of India)

High Incidence of Lysogeny in the Oxygen Minimum Zones of the Arabian Sea (Southwest Coast of India)

Viral Regulation on Bacterial Community Impacted by Lysis-Lysogeny Switch: A Microcosm Experiment in Eutrophic Coastal Waters

Genome analysis of Crassaminicella sp. SY095, an anaerobic mesophilic marine bacterium isolated from a deep-sea hydrothermal vent on the Southwest Indian Ridge

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