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

Abstract

How microbial populations interact influences the availability and flux of organic carbon in the ocean. Understanding how these interactions vary over broad spatial scales is therefore a fundamental aim of microbial oceanography. In this study, we assessed variations in the abundances, production, virus and grazing induced mortality of heterotrophic prokaryotes during summer along a meridional gradient in stratification in the North Atlantic Ocean. Heterotrophic prokaryote abundance and activity varied with phytoplankton biomass, while the relative distribution of prokaryotic subpopulations (ratio of high nucleic acid fluorescent (HNA) and low nucleic acid fluorescent (LNA) cells) was significantly correlated to phytoplankton mortality mode (i.e., viral lysis to grazing rate ratio). Virus-mediate morality was the primary loss process regulating the heterotrophic prokaryotic communities (average 55% of the total mortality), which may be attributed to the strong top-down regulation of the bacterivorous protozoans. Host availability, encounter rate, and HNA:LNA were important factors regulating viral dynamics. Conversely, the abundance and activity of bacterivorous protozoans were largely regulated by temperature and turbulence. The ratio of total microbial mediated mortality to total available prokaryote carbon reveals that over the latitudinal gradient the heterotrophic prokaryote community gradually moved from a near steady state system regulated by high turnover in subtropical region to net heterotrophic production in the temperate region.

Seasonality of top‐down control of bacterioplankton at two central Red Sea sites with different trophic status

“…The positive correlation between total viruses and Synechococcus abundances at KH might indicate that a large fraction of viruses were cyanophages, which tend to increase in more productive systems (Bettarel et al, 2004; Johannessen et al, 2017). The analysis of the 3 different subgroups based on nucleic acid content (V1, V2 and V3, Table S2) consistently observed in our samples, as in most oceanic regions (e.g., Johannessen et al, 2017; Mojica & Brussaard, 2020) can shed more light into specific associations with distinct bacterial groups. The observed changes in the relative contribution of the 3 subgroups between the two years (Table S2) are likely related to the change in absolute abundances, as also observed in other studies (Marston et al, 2013; Marston & Sallee, 2003).…”

Editorial: Unraveling Mechanisms Underlying Annual Plankton Blooms in the North Atlantic and Their Implications for Biogenic Aerosol Properties and Cloud Formation

“…Between late spring and early autumn, net community production (NCP) accumulating as seasonal (semi-labile) surplus DOC increased (Baetge Graff et al), along with the abundance of SAR202 genomes in the euphotic zone (Bolaños et al). This period corresponded to enhanced physiological stress and viral mediated phytoplankton mortality, the latter enhancing substrate for heterotrophic prokaryote growth and potentially impacting community structuring (Mojica and Brussaard, 2020).…”

Extracellular ribosomal RNA provides a window into taxon-specific microbial lysis

“…These observations are congruent with the seed-bank theory of viral infection, in which only a small proportion of viruses are active at any given time 13 . Furthermore, as viral lysis is estimated to cause about 50% of marine prokaryotic mortality 14-15 and kill about 20% of the standing stock each day 16 , lysis must be high in taxa that are affected. Strikingly, of the 31 phyla for which rRNA ext was detected, there are only a few for which viruses have been isolated ( Euryarchaeota, Thaumarchaeota, Proteobacteria, Firmicutes, Bacteriodetes, Actinobacteria, Cyanobacteria, Chlamydiae, Tenericutes and Deinococcus-Thermus ) 17 or are known from single amplified genomes ( Verrucomicrobia and Marinimicrobia ) 18 .…”

“…In summary, we have shown that extracellular RNA (rRNA ext ) in seawater is produced by cell lysis, and not by protistan grazing on bacteria. Although our approach cannot distinguish among different causes of cell lysis, given that lysis by viruses accounts for about half of the mortality of prokaryotes in seawater 14-15 , and kills about 20% of bacteria each day 16 , it is reasonable to infer that most rRNA ext stems from viral infection. Moreover, rRNA ext is stable in seawater and can be sequenced to taxonomically profile the cells in which lysis has occurred.…”