Unveiling the role and life strategies of viruses from the surface to the dark ocean

Abstract

Viruses are a key component of marine ecosystems, but the assessment of their global role in regulating microbial communities and the flux of carbon is precluded by a paucity of data, particularly in the deep ocean. We assessed patterns in viral abundance and production and the role of viral lysis as a driver of prokaryote mortality, from surface to bathypelagic layers, across the tropical and subtropical oceans. Viral abundance showed significant differences between oceans in the epipelagic and mesopelagic, but not in the bathypelagic, and decreased with depth, with an average power-law scaling exponent of -1.03 km^-1 from an average of 7.76 × 10⁶ viruses ml^-1 in the epipelagic to 0.62 × 10⁶ viruses ml^-1 in the bathypelagic layer with an average integrated (0 to 4000 m) viral stock of about 0.004 to 0.044 g C m^-2, half of which is found below 775 m. Lysogenic viral production was higher than lytic viral production in surface waters, whereas the opposite was found in the bathypelagic, where prokaryotic mortality due to viruses was estimated to be 60 times higher than grazing. Free viruses had turnover times of 0.1 days in the bathypelagic, revealing that viruses in the bathypelagic are highly dynamic. On the basis of the rates of lysed prokaryotic cells, we estimated that viruses release 145 Gt C year^-1 in the global tropical and subtropical oceans. The active viral processes reported here demonstrate the importance of viruses in the production of dissolved organic carbon in the dark ocean, a major pathway in carbon cycling.

Fig. 1. World map showing the location of the Malaspina sampling stations and depth-integrated viral abundance.

(A) Map of the Malaspina 2010 cruise showing the 120 sampling stations. Colors indicate the three different oceanic regions (Atlantic, Indian, and Pacific). Average values of depth-integrated viral abundance and their SEs are shown for the three main oceanic regions in the (B) epipelagic (0 to 200 m), (C) mesopelagic (200 to 1000 m), and (D) bathypelagic (1000 to 4000 m) layers. In (E), all depth average data are summarized. ATL, Atlantic; IN, Indian; PAC, Pacific.

Fig. 2. Viral abundance and depth.

(A) Power-law fit between log-transformed viral abundance and depth in the Atlantic, Indian, and Pacific oceans and in all the data. Lines denote the best power-law model regression. (B) Cumulative percentage curves of integrated viral abundance according to depth for the three oceanic regions and for all the data. Dashed lines in (B) show the depth where half of the integrated viral stock between 0 and 4000 m is contained in each oceanic region and for all the data.

Fig. 3. VPR and relationships between viral and prokaryotic abundances.

Averages values of the VPR and their SEs in the three oceanic regions (Atlantic, Indian, and Pacific) sampled during the cruise in the (A) epipelagic (0 to 200 m), (B) mesopelagic (200 to 1000 m), and (C) bathypelagic (1000 to 4000 m) layers and in (D) all the data. Relationships between viral and prokaryotic abundances in the (E) epipelagic, (F) mesopelagic, and (G) bathypelagic layers from the Atlantic, Indian, and Pacific oceans and in (H) all the data. Dashed lines show the 95% prediction intervals from linear regressions of all data in the epipelagic, mesopelagic, and bathypelagic layers.

Fig. 4. VP_L and VP_LG and prokaryotic mortality due to viruses.

(A) VP_L against VP_LG and (B) VMM against PMM detected at the surface (SURF; 3-m depth), DCM, and bathypelagic (BATHY; 4000-m depth) layers from 11 selected stations: 4 in the Atlantic Ocean, 3 in the Indian Ocean, and 4 in the Pacific Ocean. Three replicates were performed in each experiment. Dashed line is the 1:1 line. Lytic/lysogenic ratios at the surface, DCM, and bathypelagic layers were 4.63 ± 2.76, 10.00 ± 7.23, and 53.89 ± 39.17, respectively. Viral/grazing-mediated mortality ratios were 2.35 ± 1.47 at the surface layer, 7.15 ± 6.52 at the DCM layer, and 173.11 ± 128.91 at the bathypelagic layer.