HETEROTROPHIC MICROORGANISMS AND VIRUSES IN THE COASTAL WATERS OF THE SEVERNAYA ZEMLYA ARCHIPELAGO (ARCTIC) DURING THE PERIOD OF GLACIERS MELTING

Authors

  • A. I. Kopylov Papanin Institute for Biology of Inland Water, Russian Academy of Sciences
  • E. A. Zabotkina Papanin Institute for Biology of Inland Water, Russian Academy of Sciences
  • A. V. Romanenko Papanin Institute for Biology of Inland Water, Russian Academy of Sciences
  • N. D. Romanova Shirshov Institute of Oceanology, Russian Academy of Sciences
  • A. F. Sazhin Shirshov Institute of Oceanology, Russian Academy of Sciences

DOI:

https://doi.org/10.29006/1564-2291.JOR-2025.53(3).6

Keywords:

bacterioplankton, heterotrophic nanoflagellates, virioplankton, viral infection, viral lysis of bacteria, coastal waters, Severnaya Zemlya archipelago, Arctic

Abstract

For the first time, quantitative data were obtained on bacteria, heterotrophic nanoflagellates and viruses in the coastal waters of the Severnaya Zemlya archipelago. The studies were conducted in August–September 2019 during a cruise on the research vessel Professor Molchanov. The number of bacteria (NB), heterotrophic nanoflagellates (NF) and viruses varied widely: (1.0– 9.1) × 105 cells ml−1, (84–502) cells ml−1, (3.5–74.9) × 105 viruses ml−1, respectively. In the studied waters, a positive correlation was found between NВ and water temperature (R = 0.69, n = 30, p < 0.05) and a negative correlation between NВ and water salinity (R = −0.67, n = 30). A strong positive correlation was observed between NВ and NF values: R = 0.86, n = 30, p < 0.05. The frequency of visibly infected bacteria (FVIC) and virus-induced mortality of bacteria (VMB) varied from 0.7 to 3.9% of NB and from 5.3 to 39.2% of bacterial production. The FVIC and VMB values in the coastal waters of the Severnaya Zemlya archipelago, on average, were significantly higher than those in the open waters of the Kara Sea and the Laptev Sea. It was shown that the influx of large amounts of suspended matter into coastal waters with glacial runoff reduces bacterial mortality caused by viral lysis, since a significant number of viral particles are adsorbed on suspended particles and lose their activity.

References


  1. Azam, F., 1998: Microbial control of oceanic carbon flux: The plot thickens. Science, 28, 694–696, https://doi.org/10.1126/science.280.5364.694.

  2. Binder, B., 1999: Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquatic Microb. Ecol., 18, 207−215, https://doi.org/10.3354/ame018207.

  3. Bintanja, R. and O. Andry, 2017: Towards a Rain-Dominated Arctic. Nature Climat. Change, 7, 263, https://doi.org/10.1038/nclimate3240.

  4. Boras, J. A., M. M. Sala, J. M. Arrieta, E. L. Sà, J. Felipe, S. Agustí, C. M. Duarte, and D. Vaqué, 2010: Effect of ice melting on bacterial carbon fluxes channelled by viruses and protists in the Arctic Ocean. Polar Biol., 33, 1695–1707, https://doi.org/10.1007/s00300‐010‐0798‐8.

  5. Børsheim, K. Y. and G. Bratbak, 1987: Cell volume to carbon conversion factors for bacterivorous Monas sp. enriched from seawater. Marine Ecol. Progr. Ser., 36, 171−175, https://doi.org/10.3354/meps036171.

  6. Caron, D. A., 1983: Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluores-cence microscopy and comparison with other procedures. Appl. Environ. Microbiol., 46 (2), 491−498, PMID: 16346372.

  7. Caruso, G., M. Azzaro, C. Caroppo, F. Decembrini, L. S. Monticelli, M. Leonardi, G. Maimone, R. Zaccone, and R. La Ferla, 2016: Microbial community and its potential as descriptor of environmental status. ICES J. Mar. Sci., 73, 2174–2177, https://doi.org/10.1093/icesjms/fsw101.

  8. Danovaro, R. and M. Middelboe, 2010: Separation of free virus particles from sediments in aquatic systems. Eds. Wilhelm S., M. Weinbauer and C. Suttle. Manual of Aquatic Viral Ecology. ASLO, 74–81, https://doi.org/10.4319/mave.2010.978-0-9845591-0-7.74.

  9. De Corte, D., E. Sintes, T. Yokokawa, and G. J. Herndl, 2011: Changes in viral and bacterial communities during the ice‐melting season in the coastal Arctic (Kongsfjorden, Ny‐Ålesund). Environ. Microbiol., 13, 1827–1841, https://doi.org/10.1111/j.1462-2920.2011.02497.x.

  10. Fenchel, T., 1982: Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Marine Ecol. Progr. Ser., 8, 225–231, https://doi.org/10.3354/meps008225.

  11. Heinrich, H., 1988: Origin and consequences of cycling ice rafting in the northeast Atlantic Ocean during the past 130, 000 years. Quatern. Res., 29 (2), 142–152, https://doi.org/10.1016/0033-5894(88)90057-9.

  12. Hewson, I. and J. A. Fuhrman, 2003: Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microb. Ecol., 46, 337–347, https://doi.org/10.1007/s00248-002-1041-0.

  13. Hill, P. R. and O. C. Nadeau, 1989: Storm-dominated sedimentation on the inner shelf of the Canadian Beaufort Sea. J. Sediment. Res., 59, 455–468, https://doi.org/10.1306/212F8FC1-2824-11D7-8648000102C1865D.

  14. Khromova, T. E., G. A. Nosenko, A. F. Glazovskij, A. Ya. Murav’ev, S. A. Nikitin, and I. I. Lavrent’ev, 2021: Ledniki i Lednikovye pokrovy. Novyj katalog lednikov Rossii po sputnikovym dannym (2016–2019) (New Inventory of the Russian glaciers based on satellite data (2016–2019)). Led i Sneg, 61 (3), 341–358.

  15. Kirchman, D. L., X. Moran, and H. Ducklow, 2009: Microbial growth in the polar oceans – role of temperature and potential impact of climate change. Nature Rev. Microb., 7, 451–459, https://doi.org/10.1038/nmicro2115.

  16. Kopylov, A. I., E. A. Zabotkina, A. V. Romanenko, D. B. Kosolapov, and A. F. Sazhin, 2020: Viruses in the water column and the sediment of the eastern part of the Laptev Sea. Est. Coast. Shelf Sci., 242, e106836, https://doi.org/10.1016/j.ecss.2020.106836.

  17. Kopylov, A. I., E. A. Zabotkina, A. F. Sazhin, N. Romanova, N. Belyaev, and A. Drozdova, 2023: Virioplankton and virus-induced mortality of prokaryotes in the Kara Sea (Arctic) in summer. PEERJ, 11, e154577, https://doi.org/10.7717/peerj.15457.

  18. Kosolapova, N. G., D. B. Kosolapov, A. I. Kopylov, and A. V. Romanenko, 2019: Geterotrofny`e nanoflagellyaty` v pelagiali i donny`x otlozheniyax vostochnoj chasti morya Laptevy`x (Heterotrophic Nanoflagellates in the Pelagic Zone and Sediments of the Eastern Laptev Sea). Oceanology, 59 (6), 974–956, https://doi.org/10.31857/S0030-1574596974-986.

  19. Krembs, C., H. Eicken, K. Junge, and J. W. Deming, 2002: High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Res. P. I. Oceanograph. Res. Pap., 49, 2163–2181, https://doi.org/10.1016/S0967-0637(02)00122-X.

  20. Lara, E., J. Arrieta, J. Garcia-Zarandona, J. Boras, C. M. Duarte, S. Agasti, P. F. Vassmann, and D. Vaque, 2013: Experimental evaluation of the warming effect on viral, bacterial and protistan commonities in two contrasting Arctic system. Aquat. Microb. Ecol., 10, 17–32, https://doi.org/10.3354/ame01636.

  21. Maat, D. S., R. J. W. Visser, and C. P. D. Brussaard, 2019a: Virus removal by gracier-derived suspended fine sediment in the Arctic. J. Exp. Mar. Biol. Ecol., 521, e151227, https://10.1016/j.jembe.2019.151227.

  22. Maat, D. S., M. A. Prins, and C. P. D. Brussaard, 2019b: Sediments from Arctic tide-water glaciers remove coastal marine viruses and delay host infection. Viruses, 11 (2), e123, https://doi.org/10.3390/v11020123.

  23. Müller-Nilkas, G. and J. G. Herndl, 1996: Dynamics of bacterioplankton during a phytoplankton bloom in the high Arctic waters of the Franz-Joseph Land archipelago. Aquat. Microb. Ecol., 11, 111–118, https://doi.org/10.3354/ame011111.

  24. Murav`ev, A. Ya. and R. A. Chernov, 2023: Prory`v lednikovo podprudnogo ozera Spartakovskoe i izmeneniya vy`vodnogo lednika kupola Semeno-Tyan-Shanskogo v 2021 g. (Severnaya Zemlya) (Breakthrough of the glacial-dammed Lake Spartakovskoye and changes in the outlet glacier of the Semeno-Tyan-Shansky dome in 2021 (Severnaya Zemlya)). Led i Sneg, 63 (1), 17–32, https://doi.org/10.31857/S20076673423010118,.EDN:MAJNVD [In Russian].

  25. Newell, S. Y. and R. R. Chrisrian, 1981: Frequency of dividing cells as estimator of bacterial productivity. Appl. Environ. Microb., 42 (1), 23–31, https//doi.org/10.1128/aem.42.1.23-31.

  26. Nguyen, H. T., Y. M. Lee, J. K. Hong, S. Hong, M. Chen, and J. Hur, 2022: Climate Warming-driven changes in the flux of dissolved organic matter and its effects on bacterial communities in the Arctic Ocean: A review. Front. Marin. Sci., 9, e968583, https//doi.org/103389/fmars.2022.968583.

  27. Norland, S., 1993: The relationship between biomass and volume of bacteria. Handbook of Methods in Aquatic Microbial Ecology. P. F. Kemp, J. J. Cole, B. F. Sherrand E. B. Sherr (Eds.), Lewis Publisher, Boca Raton., 303–308, https://doi.org/10.1201/9780203752746-36.

  28. Pfirman, S. L., H. Eicken, D. Bauch, and W. F. Weeks, 1995: The potential transport of pollutants by Arctic sea ice. Sci. Total Environ., 159, 129–146, https://doi.org/10.1016/0048-9697(95)04174-Y.

  29. Pomeroy, L. R., S. A. Macko, P. H. Ostrom, and J. Dumpphy, 1990: The microbial food web in Arctic seawater: concentration of dissolved free amino acids and bacterial abundance and activity in Arctic Ocean and in Resolute Passage. Marin. Ecol. Progr. Ser., 61, 31–40.

  30. Porter, K. G. and Y. S. Feig, 1980: The use DAPI for identifying and counting of aquatic microflora. Limnol. Oceanogr., 25 (5), 943−948, https://doi.org/10.4319/lo.1980.25.5.0943.

  31. Rokkan, I. K. and L. Seuthe, 2011: Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): 1. Heterotrophic bacteria, picoplankton and nanoflagellates. Polar Biol., 34, 731−749, https://doi.org/10.1007/s00300-010-0929-2.

  32. Sarmento, H., J. M. Montoya, E. Vazquez-Dominguez, D. Vaque, and J. M. Gazol, 2010: Warming effects on marine microbial food web processes: How for can we go when it comes to predictions? Philosoph. Transact. Royal Soc. B. Biol. sci., 365, 2137−2149, https://doi.org/10.1098/rstb.2010.0045.

  33. Sazhin, A. F., N. D. Romanova, A. I. Kopylov, A. V. Romanenko, and E. A. Zabotkina, 2023: Geterotrofny`j nano- i mikroplankton Karskogo morya v osennij period (Heterotrophic Nano- and Microplankton in the Kara Sea in Autumn). Oceanology, 63 (2), 243–254.

  34. Sherr, E. B, B. F. Sherr, and L. Fessenden, 1997: Heterotropic protists in the central Arctic Ocean. Deep Sea Res., 44, 1665−1682, https://doi.org/10.1016/S0967-0645(97)00050-7.

  35. Sommaruga, R., 2015: When glaciers and ice sheets melt: Consequences for planktonic organisms. J. Plankt. Res., 37, 509–518, https://doi.org/10.1093/plankt/fbv027.

  36. Steward, G. F., L. B. Fandino, J. T. Hollibaugh, T. E. Whitledge, and F. Azam, 2007: Microbial biomass and viral infections of heterotrophic prokaryotes in the sub-surface layer of the central Arctic Ocean. Deep Sea Res. P. I. Oceanogr. Res. Pap., 54, 1744−1757, https://doi.org/10.1016/j.dsr.2007.04.019.

  37. Suttle, C. A., 1993: Enumeration and isolation of virus. Handbook of Methods in Aquatic Microbial Ecology, 1st Ed. P. F. Kemp, J. J. Cole, B. F. Sherr and E. B. Sherr (Eds.), Lewis Publisher, Boca Raton, 121−134.

  38. Svendsen, H., A. Beszczynska-Møller, J. O. Hagen, B. Lefauconnier, V. Tverberg, S. Gerland, J. Børre Ørbæk, K. Bischof, C. Papucci, M. Zajaczkowski, R. Azzolini, O. Bruland, C. Wiencke, J.-G. Winther, and W. Dallmann, 2002: The physical environment of Kongsfjorden–Krossfjorden, an Arctic fjord system in Svalbard. Polar Res., 21, 133–166, https://doi.org/10.3402/polar.v21i1.6479.

  39. Thomas, D. N. and G. S. Dieckmann, 2002: Antarctic sea ice – a habitat for extremophiles. Science, 295, 641–644, https://doi.org/10.1126/science.1063391.

  40. Vaque, D., E. Lara, J. M. Arrieta, J. Holding, E. L. Sa, I. E. Hendriks, A. Coello-Camba, M. Alvarez, S. Agusti, P. F. Wassmann, and C. M. Duarte, 2019: Warming and CO2 enhance Arctic heterotrophic microbial activity. Front. Microbio., 10, e494, https://doi.org/10.3389/fmicb.2019.00494.

  41. Venger, M. P., 2011: Bakterioplankton severo-vostochnoj chasti Barenceva moray (Bacterioplankton of the northeastern part of the Barents Sea). Vestnik Yuzhnogo Nauchnogo centra RAN, 7 (4), 55–60.

  42. Venger, M. P., A. I. Kopylov, E. A. Zabotkina, and P. R. Makarevich, 2016: Vliyanie virusov na bakterioplankton otkry`toj i pribrezhnoj chasti Barenceva moray (The influence of viruses on bacterioplankton of the open and coastal parts of the Barents Sea). Biologiya moray, 42 (1), 19–26.

  43. Venger, M. P., T. I. Shirokolobova, T. M. Maksimovskaya, M. A. Boltenkova, and A. V. Vashhenko, 2024: Komponenty` mikrobnoj pishhevoj seti v pelagiali f`ordov o. Zapadny`j Shpiczbergen v sovremenny`x klimaticheskix usloviyax (Components of the microbial food web in the pelagic zone of the fjords of West Spitsbergen Island under modern climatic conditions). Trudy` KNCz. Ser. Est. i gum. Nauki, 3 (3), 23–37, https://doi.org/10.37614/2949-1185.2024.3.3.003.

  44. Wang, G., C. Guo, W. Luo, M. Cai, and J. He, 2009: The distribution of picoplankton and nanoplankton in Kongsfjorden, Svalbard during late summer 2006. Polar Biol., 32, 1233–1238. https://doi.org/10.1007/s00300‐009‐0666‐6.

  45. Weinbauer, M. G., 2004: Ecology of prokaryotic viruses. FEMS Microb. Rev., 28 (2), 127–181, https://doi.org/10.1016/j.femsre.2003.08.001.

  46. Weinbauer, M. G., Y. Bettarel, R. Cattaneo, B. Luef, C. Maier, C. Motegi, P. Peduzzi, and X. Mari, 2009: Viral ecology of organic and inorganic particles in aquatic systems: avenues for further research. Aquat. Microb. Ecol., 57, 321‒341, https://doi.org/10.3354/ame01363.

  47. Wells, L. E. and J. W. Deming, 2006: Significance of bacterivory and viral lysis in bottom waters of Franklin Bay, Canadian Arctic, during winter. Aquat. Microb. Ecol., 43, 209−221, https://doi.org/10.3354/ame043209.

Published

2025-09-21

Issue

Section

Ecology of seas and oceans

Most read articles by the same author(s)