Abstract
We studied vertical distribution of bacteria and viruses in different layers of the Arctic sea ice drilled at the North Pole. The sampled multi-year ice was characterized by uneven vertical distribution of bacterial abundance. This characteristic varied within the range of 8 ± 1.2 × 103 to 95 ± 2.6 × 103 cells mL–1. The layers with the maximal bacterial abundance were located in the intermediate and lower layers of the ice cores. Bacterial biomass varied from 0.5 to 5 mg C m–3 with the mean value 1.57 ± 0.2 mg C m–3. The ratio of viral to bacterial abundance varied from 0.6 to 28, with the mean value 12.5. The average total number of phages attached to bacteria was 6.2 × 103 viral particles mL–1. The number of viral particles located within the bacterial cells varied from 2 to 21 particles per a bacterial cell. The frequency of visibly infected bacterial cells (FVIC) calculated for the upper, intermediate and lower layers of the ice was 0.92, 1.23 and 0.8% of the total bacterial abundance, respectively. The overall frequency of infected cells (FIC) calculated for the same layers was 6.3, 8.4 and 0.8% of bacteria numbers, respectively, while the viral-mediated mortality of bacteria (VMB) was 7.1, 9.8 and 6.1%, respectively. Our data show that during the study period the rate of viral infection of bacterial cells and the viral-mediated mortality of bacterial cells in the multy-year ice of the North Pole were relatively low.
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REFERENCES
A. I. Kopylov and D. B. Kosolapov, Microbial Loop in Plankton Communities of Marine and Freshwater Ecosystems (KnigoGrad, Izhevsk, 2011) [in Russian].
I. A. Mel’nikov, “Evaluation of modern state and formation of biota of Arctic marine ice according to monitoring results of the area of Northern Pole,” Probl. Ecol. Monit. Model. Ekosist. 28 (1), 83–96 (2017).
N. D. Romanova and A. F. Sazhin, “Relationships between the cell volume and the carbon content of bacteria,” Oceanology (Engl. Transl.) 50, 522–530 (2010).
A. M. Anesio and C. M. Bellas, “Are low temperature habitats hot spots of microbial evolution driven by viruses?” Trends Microbiol. 19 (2), 52–57 (2011).
K. R. Arrigo, D. K. Perovich, et al., “Massive phytoplankton blooms under Arctic sea ice,” Science 336, 1408 (2012).
P. Assmy, J. K. Ehn, M. Fernández-Méndez, et al., “Floating ice-algal aggregates below melting Arctic sea ice,” PLoS One 8, e76599 (2013).
B. Binder, “Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells,” Aquat. Microb. Ecol. 18, 207–215 (1999).
B. A. Bluhm, K. N. Kosobokova, and E. C. Carmack, “A tale of two basins: An integrated physical and biological perspective of the deep Arctic Ocean,” Prog. Oceanogr. 139, 89–121 (2015).
A. Boetius, S. Albrecht, K. Bakker, et al., “Export of algal biomass from the melting Arctic sea ice,” Science 339, 1430–1432 (2013).
A. Boetius, A. M. Anesio, J. W. Deming, et al., “Microbial ecology of the cryosphere: sea ice and glacial habitats,” Nat. Rev. Microbiol. 13, 677–690 (2015).
J. A. Boras, M. M. Sala, J. M. Arrieta, et al., “Effect of ice melting on bacterial carbon fluxes channeled by viruses and protists in the Arctic Ocean,” Polar Biol. 33, 1695–1707 (2010).
M. Borriss, E. Helmke, R. Hanschke, and T. Schweder, “Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice,” Extremophiles 7, 377–384 (2003).
R. Brinkmeyer, K. Knittel, J. Jürgens, et al., “Diversity and structure of bacterial communities in Arctic versus Antarctic Pack Ice,” Appl. Environ. Microbiol. 69 (11), 6610–6619 (2003).
D. J. Cavalieri and C. L. Parkinson, “Arctic sea ice variability and trends, 1979–2010,” Cryosphere 6, 881–889 (2012).
R. E. Collins, Sh. D. Carpenter, and J. W. Deming, “Spatial heterogeneity and temporal dynamics of particles, bacteria, and pEPS in Arctic winter sea ice,” J. Mar. Syst. 74, 902–917 (2008).
J. C. Comiso, “Large decadal decline of the Arctic multiyear ice cover,” J. Clim. 25, 1176–1193 (2012).
D. Delille, M. Fiala, J. Kuparinen, et al., “Seasonal changes in microbial biomass in the first-year ice of the Terre Adelie area (Antarctica),” Aquat. Microb. Ecol. 28, 257–265 (2002).
J. W. Deming, “Bacteria and viruses,” in Sea Ice, Ed. by Thomas D.N. and Dieckmann G.S. (Wiley-Blackwell, Hoboken, NJ, 2010), Ch. 7, pp. 247–282.
J. W. Deming and H. Eicken, “Planets and life,” in The Emerging Science of Astrobiology, Ed. by W. T. Sullivan and J. A. Baross (Cambridge University Press, Cambridge, 2007), pp. 292–312.
M. Fernández-Méndez, F. Wenzhöfer, I. Peeken, et al., “Composition, buoyancy regulation and fate of ice algal aggregates in the central Arctic Ocean,” PLoS One 9, e107452 (2014).
A. G. Fountain, J. L. Campbell, E. A. G. Schuur, et al., “The disappearing cryosphere: impacts and ecosystem responses to rapid cryosphere loss,” Bioscience 62, 405–415 (2012).
K. A. Hoff, “Total and specific bacterial counts by simultaneous staining with DAPI and flourochrome-labeled antibodies,” in Handbook of Methods in Aquatic Microbial Ecology (CRC Press, Boca Ration, 1993), pp. 149–154.
M. M. Gowing, “Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats,” Mar. Biol. 142, 1029–1040 (2003).
M. M. Gowing, D. L. Garrison, A. H. Gibson, et al., “Bacterial and viral abundance in Ross Sea summer pack ice communities,” Mar. Ecol.: Prog. Ser. 279, 3–12 (2004).
M. M. Gowing, B. E. Riggs, D. L. Garrison, et al., “Large viruses in Ross Sea late autumn pack ice habitats,” Mar. Ecol.: Prog. Ser. 241, 1–11 (2002).
R. Gradinger and Q. Zhang, “Vertical distribution of bacteria in Arctic sea ice from the Barents and Laptev seas,” Polar Biol. 17, 448–454 (1997).
N. Guixa-Boixereu, D. Vaqué, J. M. Gasol, et al., “Viral distribution and activity in Antarctic waters,” Deep Sea Res., Part II 49, 827–845 (2002).
O. M. Johannessen, E. V. Shalina, and M. Miles, “Satellite evidence for an Arctic sea ice cover in transformation,” Science 286, 1937–1939 (1999).
K. Junge, H. Eicken, and J. W. Deming, “Bacterial activity at –2 to –20°C in Arctic wintertime sea ice,” Appl. Environ. Microbiol. 70 (1), 550–557 (2004).
K. Junge, F. Imhoff, T. Staley, and J. W. Deming, “Phylogenetic diversity of numerically important Arctic sea-ice bacteria cultured at subzero temperature,” Microb. Ecol. 43 (3), 315–328 (2002).
T. Kaneko, G. Roubal, and R. M. Atlas, “Bacterial populations in the Beaufort Sea,” Nature 270, 596–599 (1977).
S. T. Kottmeier and C. W. Sullivan, “Bacterial biomass and production in pack ice of Antarctic marginal ice edge zones,” Deep-Sea Res. 37 (8), 1311–1330 (1990).
R. Kwok, G. F. Cunningham, M. Wensnahan, et al., “Thinning and volume loss of the Arctic Ocean sea ice cover: 2003–2008,” J. Geophys. Res.: Oceans 114 (7), 1–16 (2009).
M. van Leeuwe, L. Tedesco, K. R. Arrigo, et al., “Microalgal community structure and primary production in Arctic and Antarctic sea ice: a synthesis,” Elem. Sci. Anthropocene 6 (4) (2018). https://doi.org/10.1525/elementa.267
R. Maranger, F. D. Bird, and S. K. Juniper, “Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, N.W.T., Canada,” Mar. Ecol.: Prog. Ser. 111, 121–127 (1994).
K. Meiners, J. Fehling, M. A. Granskog, and M. Spindler, “Abundance, biomass and composition of biota in Baltic Sea ice and underlying water (March 2000),” Polar Biol. 25 (7), 761–770 (2002).
K. Meiners, R. Gradinger, J. Fehling, et al., “Vertical distribution of exopolymer particles in sea ice of the Fram Strait (Arctic) during autumn,” Mar. Ecol.: Prog. Ser. 248, 1–13 (2003).
S. V. Nghiem, I. G. Rigor, D. K. Perovich, et al., “Rapid reduction of Arctic perennial sea ice,” Geophys. Res. Lett. 34 (19), 34–39 (2007).
I. V. Polyakov, J. E. Walsh, and R. Kwok, “Recent changes of Arctic multiyear sea-ice coverage and the likely causes,” Bull. Am. Meteorol. Soc. 93, 145–151 (2012).
K. G. Porter and Y. S. Feig, “The use of DAPI for identifying and counting aquatic microflora,” Limnol. Oceanogr. 25 (5), 943–948 (1980).
D. A. Rothrock, Y. Yu, and G. A. Maykut, “Thinning of the Arctic sea-ice cover,” Geophys. Res. Lett. 26 (23), 3469–3472 (1999).
G. F. Steward, L. B. Fandino, J. T. Hollibaugh, et al., “Microbial biomass and viral infections of heterotrophic prokaryotes in the sub-surface layer of the Central Arctic Ocean,” Deep Sea Res., Part I 54, 1744–1757 (2007).
F. J. Stewart and C. H. Fritsen, “Bacteria-algae relationships in Antarctic sea ice,” Antarct. Sci. 16 (2), 143–156 (2004).
R. Terrado, C. Lovejoy, R. Massana, and W. F. Vincent, “Microbial food web responses to light and nutrients beneath the coastal Arctic Ocean Sea ice during the winter-spring transition,” J. Mar. Syst. 74, 964–977 (2008).
K. Y. Vinnikov, A. Robok, R. Stouffer, et al., “Global warming and northern hemisphere sea ice extent,” Science 286 (5446), 1934–1937 (1999).
L. E. Wells and J. W. Deming, “Modeled and measured dynamics of viruses in Arctic winter sea ice brines,” Environ. Microbiol. 8, 1115–1121 (2006).
M. G. Weinbauer, “Ecology of prokaryotic viruses,” FEMS Microbiol. Rev. 28 (2), 127–181 (2004).
Y. Z. Zheng, R. Web, P. F. Greenfield, and S. Reid, “Improved method for counting virus and virus like particles,” J. Virol. Methods 62, 153–159 (1996).
ACKNOWLEDGMENTS
The authors thank A.N. Novigatsky, N.A. Belyaev and L. E. Reykhard for providing the ice cores used in the study.
Funding
This study was supported by the Russian Ministry of Education and Science, agreement number 14.616.21.0078 (RFMEFI61617X0078).
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Sazhin, A.F., Romanova, N.D., Kopylov, A.I. et al. Bacteria and Viruses in Arctic Sea Ice. Oceanology 59, 339–346 (2019). https://doi.org/10.1134/S0001437019030196
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DOI: https://doi.org/10.1134/S0001437019030196