Viruses and viral infection of heterotrophic prokaryotes in shelf waters of the western part of the East Siberian Sea

https://doi.org/10.1016/j.jmarsys.2021.103544Get rights and content

Highlights

  • For the first time viruses – bacteria interactions were studied in the East Siberian Sea.

  • A significant number of viruses were attached to suspended particles and bacteria.

  • The parameters determined were comparable in the waters with temperature > and < 0 °C.

  • Viruses play a considerable role in controlling the heterotrophic bacterioplankton.

Abstract

In September 2017, studies were conducted in the East Siberian Sea along the transect from a Indigirka delta to the ice edge at the outer shelf margin. The abundances of planktonic prokaryotes (NPR) and free viruses (NV), frequency of visibly infected prokaryotic cells (FVIC), and virus-mediated mortality of prokaryotes (VMPR) varied within (0.5–3.4) × 106 (on average (1.67 ± 0.69) × 106) cells/mL; (2.3–10.3) × 106 (on average (5.28 ± 1.91) × 106) viruses/mL; 0.6–2.5 (on average 1.1 ± 0.4) % of NPR; and 4.5–22.3 (on average 9.0 ± 3.8) % of the total prokaryotic production, respectively. The proportions of viruses attached to prokaryotic cells (NVPR) and suspended particles (NVP) were 1.9–26.3 (on average 8.0 ± 5.0) % of NV and 0.1–65.9 (on average 8.0 ± 13.3) % of NV, respectively. High concentrations of detrital and mineral particles, to which a significant number of viruses were attached and, as a result, loss of their activity were recorded in the river–sea water mixing zone. In such a situation, the number of virus attacks on prokaryotes and cases of their infection decreased. There was a negative relationship between the concentration of suspended particles 0.5–5.0 μm in size and the abundance of infected prokaryotic cells. Thus, we conclude that viruses played a substantial role in controlling the abundance and production of heterotrophic prokaryotic plankton in the low-productive East Siberian Sea at the beginning of autumn.

Regional index terms: Russian Federation; East Siberian Sea.

Geographic bounding coordinates: 70–78° N; 150–165° E.

Introduction

Viruses are ubiquitous and the most abundant biological entities in marine pelagic environments, with abundances ranging from 106 in the deep sea to 108 viruses mL−1 in productive coastal waters (Fuhrman, 1999; Wommack and Colvell, 2000; Suttle, 2005; Lara et al., 2017). Most of these viruses are believed to be phages, accounting for a significant amount of prokaryotic mortality (Weinbauer, 2004; Suttle, 2005). Viral lysis of prokaryotes may also influence the composition of the prokaryotic community (Weinbauer and Rassoulzadegan, 2004) and trigger the release of intracellular material upon lyses, which in turn stimulates the cycling of dissolved organic carbon (DOC) by heterotrophic prokaryotes (Bratbak et al., 1994; Wilhelm and Suttle, 1999; Suttle, 2007). Previous studies have shown that in Arctic waters, viruses remove a highly variable percentage of bacterial production, from <1 (Steward et al., 2007) to 100% (Wells and Deming, 2006).

The East Siberian Sea (ESS) is one of the least studied in the Siberian Arctic, primarily due to the harsh climate conditions and duration of the ice period. The ESS is completely covered by ice from October–November to June–July. Even at the end of the summer, 65% of its area is covered by ice (Dumanskaya, 2017). The ESS is the shallowest sea of the Arctic seas: about 72% of its area is less than 50 m deep, and 50%, less than 30 m. An important feature is that its western part is subjected to the strong effect of runoff from rivers flowing into the Laptev Sea (the Lena and Yana) (Semiletov et al., 2005; Alling et al., 2010) and rivers of its own basin (the Indigirka and Kolyma) (Osadchiev et al., 2020). The rivers flowing into the ESS are characterized by a high concentration of terrigenous suspended particulate matter (SPM). The Indigirka (210 g/m3) and Kolyma (120 g/m3) are the most turbid among all large rivers of the Russian Arctic (Gordeev et al., 1996). The average SPM concentration in river runoff to the ESS is 134 g/m3, which is three to seven times higher than in rivers entering all other Russian Arctic seas. Winds associated with upwelling near the Indigirka delta result in mixing and intense offshore transport of river plumes over the sloping seafloor and upward penetration of cold subjacent seawater. The upwelling seawater induces resuspension of bottom sediments, transporting them upward to the surface layer. This process strongly depends on the local bathymetry; therefore, it only occurs over certain coastal sea zones. Detachment of river plumes from the river delta and upwelling of subjacent sea water forms large saline, cold, turbid holes within the Indigirka plumes, which can be detected on satellite images (Osadchiev et al., 2020). Another distinct feature of the ESS is its low productivity (Jaschnov, 1940; Demidov and Gagarin, 2019). All the above have significantly influence the distribution and dynamics of microorganisms and viruses in this sea.

The aim of this study is to determine the abundance, size composition, and production of virioplankton, the proportion of infected cells in prokaryotoplankton, and its virus-induced mortality in shelf areas of the ESS, which are influenced to varying extents by Indigirka river runoff and differ in water salinities and temperatures. In particular, we have studied virioplankton under conditions with a high concentration of terrigenous SPM and have observed the rising of saline and cold seawater in the vicinity of the Indigirka delta. We have tested the hypothesis that a high concentration of fine SPM in the freshwater–seawater mixing zone negatively affects viral activity. We have also verified the influence of positive and negative water temperatures on the abundance and functions of virioplankton.

Section snippets

Materials and methods

The studies were conducted during cruise 69 of the R/V Akademik Mstislav Keldysh on September 5–7, 2017, at the transect in the western part of the ESS. The southernmost station (St.) 5598 (71°28.02′ N, 152°53.99′ E) of the transect was located near the Indigirka delta; the northernmost St. 5607 (76°09.91′ N, 163°03.26′ E), near the perennial ice edge (Fig. 1).

Water samples were collected with 5-L Niskin bottles on a Rosette 32 sampler equipped with a CTD (SBE-911, Sea Bird Equipment, USA).

Results

Temperature and salinity in the water column in the studied region of the ESS varied widely from 6.2 to −1.7 °C and from 15.0 to 33.2 psu, respectively (Figs. 2а, 2b). Surface water salinity varied between 15.0 psu in the Indigirka delta and 30.0 psu at the station farthest from the delta (Fig. 2b). At the first two stations of the transect (Sts. 5598 and 5600), the water temperature was positive from surface to bottom; conversely, it was negative at northernmost St. 5607 (Fig. 2a).

The

Discussion

Our studies were conducted in autumn, when the primary phytoplankton production decreased and the number of dead planktonic organisms in water increased (Drits et al., 2019). The average heterotrophic prokaryotic production for 1 m2 (410 ± 289 mgС/(m2 × day)) was significantly higher than the average integral phytoplankton production in the ESS in September 2017 (28 ± 13 mg С /(m2 × day)) (Demidov and Gagarin, 2019). The high ratio of prokaryotic production to primary production can also be

Conclusion

The features of the spatial distribution of the structural and functional characteristics of virioplankton were determined in the ESS along the transect from the Indigirka delta to the ice cover edge at the beginning of autumn with a wide variability of abiotic factors (runoff and wind causing upwelling near the Indigirka delta, temperature, salinity). The abundance of visibly infected prokaryotic cells correlated positively with heterotrophic prokaryotic abundance and production. The high

Declaration of Competing Interest

None.

Acknowledgements

This research was financed by the Ministry of Science and Higher Education of the Russian Federation [governmental project no. АААА-А18-118012690098-5] and partially supported by the Russian Foundation for Basic Research [project no. 18-05-60069]. The authors are deeply grateful to Dr. Aaron Carpenter for correcting the English translation. The authors are also grateful to two anonymous reviewers for their thorough work with the manuscript.

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