Major viral impact on the functioning of benthic deep-sea ecosystems

Danovaro, Roberto; Dell’Anno, Antonio; Corinaldesi, Cinzia; Magagnini, Mirko; Noble, Rachel T.; Tamburini, Christian; Weinbauer, Markus G.

doi:10.1038/nature07268

Cited by 365 publications

(397 citation statements)

References 36 publications

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“…Viruses are increasingly considered as part of efforts to understand the factors controlling marine microbial mortality, productivity, and biogeochemical cycles [8,9,19,39,45,55]. Quantitative estimates of these viralinduced effects can be measured directly, but are often inferred indirectly, using the relative abundance of viruses to prokaryotes.…”

Section: Discussionmentioning

confidence: 99%

Re-examination of the relationship between marine virus and microbial cell abundances

et al. 2016

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Marine viruses are critical drivers of ocean biogeochemistry and their abundances vary spatiotemporally in the global oceans, with upper estimates exceeding 10 8 per ml. Over many years, a consensus has emerged that virus abundances are typically 10-fold higher than prokaryote abundances. The use of a fixed-ratio suggests that the relationship between virus and prokaryote abundances is both predictable and linear. However, the true explanatory power of a linear relationship and its robustness across diverse ocean environments is unclear. Here, we compile 5671 prokaryote and virus abundance estimates from 25 distinct marine surveys to characterize the relationship between virus and prokaryote abundances. We find that the median virus-to-prokaryote ratio (VPR) is 10:1 and 16:1 in the near-and sub-surface oceans, respectively. Nonetheless, we observe substantial variation in the VPR and find either no or limited explanatory power using fixed-ratio models. Instead, virus abundances are better described as nonlinear, power-law functions of prokaryote abundances -particularly when considering relationships within distinct marine surveys. Estimated power-laws have scaling exponents that are typically less than 1, signifying that the VPR decreases with prokaryote density, rather than remaining fixed. The emergence of power-law scaling presents a challenge for mechanistic models seeking to understand the ecological causes and consequences of marine virusmicrobe interactions. Such power-law scaling also implies that efforts to average viral effects on microbial mortality and biogeochemical cycles using "representative" abundances or abundanceratios need to be refined if they are to be utilized to make quantitative predictions at regional or global ocean scales.

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Section: Discussionmentioning

confidence: 99%

Re-examination of the relationship between marine virus and microbial cell abundances

et al. 2016

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“…Furthermore, viruses cause a short-cut (viral shunt) in the carbon and nutrient cycling within the pelagic food web (Wilhelm and Suttle, 1999;Suttle, 2005). A high viral turnover and the associated release of organic carbon was previously shown for surficial deep-sea sediments (Danovaro et al, 2008). For the marine deep biosphere, there are no comparable data available and the viral impact on microbial communities and the related carbon cycling in the marine deep biosphere is poorly constrained.…”

Section: Introductionmentioning

confidence: 95%

“…Cell and viral counts correlate over seven orders of magnitude (r 2 ¼ 0.941, n ¼ 89, Figure 3). At tidal flats (Beck et al, 2009) and the deep seafloor, intense microbial activity supports high viral production (Danovaro et al, 2008).…”

Section: Extraction Efficiency Of Viruses In Deep Subsurface Sedimentsmentioning

confidence: 99%

High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments

et al. 2014

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Marine sediments cover two-thirds of our planet and harbor huge numbers of living prokaryotes. Long-term survival of indigenous microorganisms within the deep subsurface is still enigmatic, as sources of organic carbon are vanishingly small. To better understand controlling factors of microbial life, we have analyzed viral abundance within a comprehensive set of globally distributed subsurface sediments. Phages were detected by electron microscopy in deep (320 m below seafloor), ancient (B14 Ma old) and the most oligotrophic subsurface sediments of the world's oceans (South Pacific Gyre (SPG)). The numbers of viruses (10 4 -10 9 cm À 3 , counted by epifluorescence microscopy) generally decreased with sediment depth, but always exceeded the total cell counts. The enormous numbers of viruses indicate their impact as a controlling factor for prokaryotic mortality in the marine deep biosphere. The virus-to-cell ratios increased in deeper and more oligotrophic layers, exhibiting values of up to 225 in the deep subsurface of the SPG. High numbers of phages might be due to absorption onto the sediment matrix and a diminished degradation by exoenzymes. However, even in the oldest sediments, microbial communities are capable of maintaining viral populations, indicating an ongoing viral production and thus, viruses provide an independent indicator for microbial life in the marine deep biosphere.

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“…The finding that the total cell counts began to drop after 5 days might be explained by cell lysis by phages, as the viral counts and the activity in aquatic ecosystems (Weinbauer and Hö fle, 1998) and sediments (Danovaro et al, 2008;Engelhardt et al, 2011) are high. Owing to the anoxic conditions, we did not expect eukaryotic grazers and they were not detected by microscopy.…”

Section: Process Assessmentmentioning

confidence: 99%

Degradation of cyanobacterial biomass in anoxic tidal-flat sediments: a microcosm study of metabolic processes and community changes

2011

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To follow the anaerobic degradation of organic matter in tidal-flat sediments, a stimulation experiment with 13 C-labeled Spirulina biomass (130 mg per 21 g sediment slurry) was conducted over a period of 24 days. A combination of microcalorimetry to record process kinetics, chemical analyses of fermentation products and RNA-based stable-isotope probing (SIP) to follow community changes was applied. Different degradation phases could be identified by microcalorimetry: Within 2 days, heat output reached its maximum (55 lW), while primary fermentation products were formed (in lmol) as follows: acetate 440, ethanol 195, butyrate 128, propionate 112, H 2 127 and smaller amounts of valerate, propanol and butanol. Sulfate was depleted within 7 days. Thereafter, methanogenesis was observed and secondary fermentation proceeded. H 2 and alcohols disappeared completely, whereas fatty acids decreased in concentration. Three main degraders were identified by RNA-based SIP and denaturant gradient gel electrophoresis. After 12 h, two phylotypes clearly enriched in 13 C: (i) Psychrilyobacter atlanticus, a fermenter known to produce hydrogen and acetate and (ii) bacteria distantly related to Propionigenium. A Cytophaga-related bacterium was highly abundant after day 3. Sulfate reduction appeared to be performed by incompletely oxidizing species, as only sulfate-reducing bacteria related to Desulfovibrio were labeled as long as sulfate was available.

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Major viral impact on the functioning of benthic deep-sea ecosystems

Cited by 365 publications

References 36 publications

Re-examination of the relationship between marine virus and microbial cell abundances

Re-examination of the relationship between marine virus and microbial cell abundances

High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments

Degradation of cyanobacterial biomass in anoxic tidal-flat sediments: a microcosm study of metabolic processes and community changes

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