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

Abstract

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.

A Review on Viral Metagenomics in Extreme Environments

“…There are three central oceanic regions which are considered to be Oxygen Minimum Zones (OMZ), namely the Eastern Tropical North Pacific (ETNP), the Eastern Tropical South Pacific (ETSP) and the Arabian Sea, within which the activity of anaerobic microorganisms is highly significant (Paulmier and Ruiz-Pino, 2009; Thamdrup, 2012). As expected, the viral population diversity closely reflects the microbial diversity in these environments (Cassman et al, 2012; Parvathi et al, 2018; Fuchsman et al, 2019), with the virome composition in OMZ being commonly composed of the Myoviridae and Siphoviridae families, followed by Phycodnaviridae (Figure 2).…”

“…These differences could be related to changes in the viral replication strategy from lytic to lysogenic. It seems that oxygen reduction concurs with a decrease in viral abundance (Cassman et al, 2012; Parvathi et al, 2018). It should be noted that a large proportion of sequences obtained from these regions do not find similarity with other viruses in the databases, but those sequences could be from viruses that infect little known prokaryotic hosts, like ammonia-oxidizing archaea and anaerobic ammonia-oxidizing (anammox) bacteria which predominate in this environment (Parvathi et al, 2018).…”

Microbial Ecology of Oxygen Minimum Zones Amidst Ocean Deoxygenation

“…High virus-induced prokaryotic mortality (up to 90%) has also been observed in an anoxic marine-influenced lake near the Adriatic Sea (Rastelli et al, 2016). Though one study in the subtropical western Pacific shows a relative switch from grazer-driven to virus-driven mortality with increasing depth (Tsai et al, 2016), other studies in the Mediterranean Sea and Arabian Sea estimated viral production and viral-induced prokaryotic mortality to decrease with depth (Weinbauer et al, 2003;Parvathi et al, 2018). Thus, the relationships between the contributions of viral lysis and grazing to prokaryotic mortality based on depth and oxygen concentration have not been resolved.…”

“…Changes in nutrient availability, productivity, and oxygen concentration can cause stress to host organisms and subsequently cause viruses to enter the lysogeny cycle (Howard-Varona et al, 2017;Correa et al, 2021). Direct estimates of lysogeny via prophage induction in OMZs have been generated for the Arabian Sea (Parvathi et al, 2018) and Baltic Sea (Weinbauer et al, 2003). In both cases the percentage of lysogens was estimated to increase between the surface and low-oxygen waters, though the percent lysogeny decreased in the suboxic samples in the Baltic Sea and increased in the Arabian Sea.…”

Uneven host cell growth causes lysogenic virus induction in the Baltic Sea

“…However, using a more refined incubation method, later studies concluded that lysogeny, if detectable at all by mitomycin C, is only of minor importance in the Baltic Sea water column [11,13]. This is in contrast to recent data obtained by the same method from the Arabian Sea showing that lysogeny can be as high as 48% in the suboxic zone and varying between 9–24% in the redoxcline [21]. Although DNA damage and the ensuing RecA-dependent SOS response are well known to induce many but not all lysogenic viruses into the lytic cycle [22,23], other RecA-independent induction mechanism have been described [24–27].…”