Weekly variations of viruses and heterotrophic nanoflagellates and their potential impact on bacterioplankton in shallow waters of the central Red Sea

Abstract

Bacterioplankton play a pivotal role in marine ecosystems. However, their temporal dynamics and underlying control mechanisms are poorly understood in tropical regions such as the Red Sea. Here, we assessed the impact of bottom-up (resource availability) and top-down (viruses and heterotrophic nanoflagellates) controls on bacterioplankton abundances by weekly sampling a coastal central Red Sea site in 2017. We monitored microbial abundances by flow cytometry together with a set of environmental variables including temperature, salinity, dissolved organic and inorganic nutrients and chlorophyll a. We distinguished five groups of heterotrophic bacteria depending on their physiological properties relative nucleic acid content, membrane integrity and cell-specific respiratory activity, two groups of Synechococcus cyanobacteria and three groups of viruses. Viruses controlled heterotrophic bacteria for most of the year, as supported by a negative correlation between their respective abundances and a positive one between bacterial mortality rates and mean viral abundances. On the contrary, heterotrophic nanoflagellates abundance covaried with that of heterotrophic bacteria. Heterotrophic nanoflagellates showed preference for larger bacteria from both the high and low nucleic acid content groups. Our results demonstrate that top-down control is fundamental in keeping heterotrophic bacterioplankton abundances low (< 5 × 10 5 cells mL−1) in Red Sea coastal waters.

Seasonal impact of grazing, viral mortality, resource availability and light on the group-specific growth rates of coastal Mediterranean bacterioplankton

“…A 2-year study in the same site comparing viruses and protists concluded that, in general, protists were the main cause of mortality, although during some periods, possibly in response to peaks in resource availability, viruses could equal protists as a source of bacterial mortality 7 . In fact, we observed some effect of viruses in the fall; interestingly, this effect coincided with relatively high viral abundances and also with the minimum concentration of heterotrophic nanoflagellate abundance observed in Blanes Bay in the year of the experiments, an observation already noticed for another coastal site 76 . Specifically for SAR11, both grazing and viruses did seem to play an important role in controlling growth (Fig.…”

Significance of Viral Activity for Regulating Heterotrophic Prokaryote Community Dynamics along a Meridional Gradient of Stratification in the Northeast Atlantic Ocean

“…However, no connection was found between grazing rates and viral abundance, prokaryotic abundance, or virus mediated mortality. In the MID we found an opposite effect of HNF on viral abundance ( r = −0.39, n = 12, p -value = 0.09) and lytic virus production ( r = −0.57, n = 8, p -value = 0.04), supporting evidence that the presence of HNF can reduce viral activity [ 80 , 83 ]. As viruses and HNF compete for the same resource (i.e., prey/host), exploitative competition is expected, that is, the activity of one reduces the resource and thereby the activity of the other ( Figure S2c ).…”

“…Instead, lytic virus production was inversely associated with the fraction of HNA cells in the community, and was uncoupled from viral abundance. Data from several studies suggest a link between HNA cells and the dominate (both in terms of abundance and contributions to total lytic production) virus group in the present study—V1 [ 30 , 79 , 80 ]. This inverse relationship between lytic virus production and the fraction of HNA cells in the community may, therefore, reflect predator-prey oscillations in virus production with the density of active hosts.…”

Moderate Seasonal Dynamics Indicate an Important Role for Lysogeny in the Red Sea

“…Although several studies have been performed on microbial communities and bacteria [27][28][29], studies on viral abundances and dynamics in the Red sea are still limited, addressing communities in coral reefs [30,31] and most recently from shoreline waters of the central Red Sea [32], a coastal lagoon [26] and the coastal waters of the Gulf of Aqaba [33], with all studies indicating complex seasonal patterns of abundance and activity of marine viruses.…”