Viruses and Protists Induced-mortality of Prokaryotes around the Antarctic Peninsula during the Austral Summer

Abstract

During the Austral summer 2009 we studied three areas surrounding the Antarctic Peninsula: the Bellingshausen Sea, the Bransfield Strait and the Weddell Sea. We aimed to investigate, whether viruses or protists were the main agents inducing prokaryotic mortality rates, and the sensitivity to temperature of prokaryotic heterotrophic production and mortality based on the activation energy (Ea) for each process. Seawater samples were taken at seven depths (0.1-100 m) to quantify viruses, prokaryotes and protists abundances, and heterotrophic prokaryotic production (PHP). Viral lytic production, lysogeny, and mortality rates of prokaryotes due to viruses and protists were estimated at surface (0.1-1 m) and at the Deep Fluorescence Maximum (DFM, 12-55 m) at eight representative stations of the three areas. The average viral lytic production ranged from 1.0 ± 0.3 × 10⁷ viruses ml^-1 d^-1 in the Bellingshausen Sea to1.3 ± 0.7 × 10⁷ viruses ml^-1 d^-1 in the Bransfield Strait, while lysogeny, when detectable, recorded the lowest value in the Bellingshausen Sea (0.05 ± 0.05 × 10⁷ viruses ml^-1 d^-1) and the highest in the Weddell Sea (4.3 ± 3.5 × 10⁷ viruses ml^-1 d^-1). Average mortality rates due to viruses ranged from 9.7 ± 6.1 × 10⁴ cells ml^-1 d^-1 in the Weddell Sea to 14.3 ± 4.0 × 10⁴ cells ml^-1 d^-1 in the Bellingshausen Sea, and were higher than averaged grazing rates in the Weddell Sea (5.9 ± 1.1 × 10⁴ cells ml^-1 d^-1) and in the Bellingshausen Sea (6.8 ± 0.9 × 10⁴ cells ml^-1 d^-1). The highest impact on prokaryotes by viruses and main differences between viral and protists activities were observed in surface samples: 17.8 ± 6.8 × 10⁴ cells ml^-1 d^-1 and 6.5 ± 3.9 × 10⁴ cells ml^-1 d^-1 in the Weddell Sea; 22.1 ± 9.6 × 10⁴ cells ml^-1 d^-1 and 11.6 ± 1.4 × 10⁴ cells ml^-1 d^-1 in the Bransfield Strait; and 16.1 ± 5.7 × 10⁴ cells ml^-1 d^-1 and 7.9 ± 2.6 × 10⁴ cells ml^-1 d^-1 in the Bellingshausen Sea, respectively. Furthermore, the rate of lysed cells and PHP showed higher sensitivity to temperature than grazing rates by protists. We conclude that viruses were more important mortality agents than protists mainly in surface waters and that viral activity has a higher sensitivity to temperature than grazing rates. This suggests a reduction of the carbon transferred through the microbial food-web that could have implications in the biogeochemical cycles in a future warmer ocean scenario.

Keywords: Antarctic waters; lysis; lysogeny; mortality; prokaryotes; protists; temperature; viruses.

Figure 1

Location of the visited stations in each delimited area. Data on heterotrophic microorganisms is not available for station 14. Ocean data view is used for mapping (Schlitzer, 2017).

Figure 2

Viral lytic and lysogenic production in each station and depth. Full circles: lytic production at surface; empty circles: lytic production at DFM; full diamonds: lysogenic production at surface; empty diamonds: lysogenic production at DFM. Outlier value for lysogeny at surface of station 7 is indicated.

Figure 3

Rate of lysed (RLC) and grazed (GZ) prokaryotes (A,C,E), and percentage of prokaryotic losses due to viruses and protists (B,D,F) in the three areas. ^*Significant differences between viral and protists activities on prokaryotes at surface; ◦significant differences between viral and protists activities on prokaryotes at DFM.

Figure 4

The energy of activation (Ea), indicated by the slope coefficients of: (A) prokaryotic heterotrophic production (PHP), (B) rates of lysed cells (RLC), and (C) grazing rates (GZ) in the three visited areas. The processes are plotted against the inverse of absolute temperature (T) multiplied by the Boltzmann constant (k) (eV⁻¹). WS, Weddell Sea; BrS, Bransfield Strait; BeS, Bellingshausen Sea.