The Viral Shunt and the Deep-Sea Paradox

Deep-sea ecosystems cover about 65% of the Earth’s surface and therefore they play a fundamental role in the global biogeochemical cycles and biomass production. This vast, extreme and dark ecosystem frequently experiences organic nutrient limitation because it lacks photosynthetic primary production and thus it mainly depends on the carbon export from the sea surface. Despite this, the prokaryotic biomass in the top 10cm of deep-sea sediments, is surprisingly high (approximately 160 Pg) and even though in situ experiments suggest that procariotes do not significantly contribute to the food requirements of higher trophic levels, it represents a potentially enormous food source for deep-sea benthic consumers. The high prokaryotic biomass in a food-limited ecosystem and the non-use of this component by benthic fauna represents currently, the two unsolved paradoxes of the deep oceans, which could be partially explained, according to the authors, through the deep 'viral shunt'.

Analyzing 232 deep-sea sediment samples coming from all over the world and from all depths from 165m to 5,571m, the authors shows that viriobenthos is a highly dynamic and active component of deep-sea ecosystems and by far, is probably the most abundant ‘life form’ in the world’s oceans.

They found that:

• Viral production and abundance are consistently high in surface sediments (top 1-cm) at all depths worldwide, with values similar to those reported for coastal sediments.

• Viruses are responsible for the abatement of 80% of the total prokaryotic production in deep-sea sediments.

• Virus-induced prokaryotic mortality increases significantly with water depth (from 16% in coastal sediments to 89% in sediments beneath 1,000m depth).

The intracellular material released by viral lysis of infected microbes has two main effects: It drastically reduce the microbial biomass potentially available to higher trophic levels and it provides an important bioavailable organic source to non-infected prokaryotes; balancing in this way the low and often limiting amount of organic detritus available in deep sediments.

In other words viruses kills an important fraction of benthic prokaryotes reducing the competition for resources (top down, predatory control) and generating labile organic material that stimulates the metabolism of others uninfected deep-sea prokaryotes (bottom-up mechanism). The significant and positive relationship between viral and prokaryotic production and between the release of carbon from viral lysis and prokaryotic turnover, demonstrate that in deep environments a stronger viral shunt is required for high prokaryotic growth rates. The viral shunt thus, can help us to better understand the paradox of a fast prokaryotic turnover in a food-limited deep-sea ecosystem.

This shunt of most of the prokaryotic carbon production into organic detritus has also important implications for nutrient cycling on a global scale. Organic carbon supplied by viral lysis promotes the microbial turnover and thus the recycling of most key elements (including nitrogen and phosphorus). The viral infection has therefore, an important role in the functioning of the largest ecosystem of the biosphere and the integration of the viral component into biogeochemical models is of primary importance for an improved understanding of global oceanic processes.

Reference:

Danovaro R, Dell'Anno A, Corinaldesi C, Magagnini M, Noble R, Tamburini C, Weinbauer M, (2008): Major viral impact on the functioning of benthic deep-sea ecosystems. Nature, 454:1084-1087.