Features of the Functioning of the Microbial “Loop” in the Black Sea

A. V. Parkhomenko

A. O. Kovalevsky Institute of Biology of the Southern Seas of RAS, Sevastopol, Russia

* e-mail: parkhomenko.46@mail.ru

Abstract

The article analyses biotic interactions (competition, predation and commensalism) between the main components of the microbial “loop” during summer and winter in the upper mixed layer of the Black Sea pelagic zone. In summer, the interaction between bacteria and phytoplankton in a phosphate-deficient environment resulted in a high contribution of bacteria and phytoplankton to the total phosphate uptake by microplankton, which was 47 and 53%, respectively, indicating a strong competition between bacteria and phytoplankton for uptake of this nutrient. The high total rate of phosphate uptake by bacteria and phytoplankton (119·10–4 µM·h–1) and its low concentrations in the upper mixed layer ensured a short turnover time of 1.9 hours, which contributed to accelerated phosphate recycling in this layer. In the interaction (predator–prey) between protozoa and picofraction (bacteria + picophytoplankton), high values of the specific rate of phosphate excretion by protozoa (zooflagellates, ciliates) were noted. This suggests their active participation in the consumption of bacteria, picophytoplankton and heterotrophic nanoplankton, thus indicating the high functional activity of the microbial “loop”. In winter, in the upper mixed layer above the pycnocline, at a temperature of 5.5–10°C, the production and daily coefficient Р/B of bacteria, picophytoplankton, zooflagellates, and ciliates decreased significantly compared to the summer period, with the exception of high levels of phytoplankton biomass and production. The contribution of the picofraction (bacteria + pico-phytoplankton) to the total phosphate uptake decreased to 8% compared to summer. The average total rate of phosphate uptake by microplankton decreased to 15·10–4 µM·h–1 relative to the summer period, with an interval of 9·10–4–24·10–4 µM·h–1. At the same time, the phosphate turnover time in the upper mixed layer increased to 38 hours, indicating a slowdown in its recycling and a low level of functional activity in the microbial “loop”. A data analysis suggests that the uptake of nutrients by bacteria and phytoplankton and their excretion by protozoa are subject to seasonal fluctuations, which should be taken into account when calculating the annual balance of matter and energy in the Black Sea pelagic zone.

Keywords

Black Sea, microbial loop, bacteria, protozoa, picophytoplankton, nanophytoplankton, phosphate uptake, phosphate excretion

Acknowledgments

The study was carried out under IBSS state research assignment “Transformation of the structure and functions of marine pelagic ecosystems under conditions of anthropogenic impact and climate change” (state registration number 124030400057-4).

About the authors

Aleksandr V. Parkhomenko, Senior Researcher, A. O. Kovalevsky Institute of Biology of the Southern Seas of the Russian Academy of Sciences (2 Nakhimov Ave., Sevastopol, 299011, Russia), PhD (Biol.), ORCID ID: 0000-0002-4070-434X, Scopus Author ID: 7006612604, ResearcherID: W-3623-2019, parкhomenko.46@mail.ru

For citation

Parkhomenko, A.V., 2026. Features of the Functioning of the Microbial “Loop” in the Black Sea. Ecological Safety of Coastal and Shelf Zones of Sea, (2), pp. 57–75.

References

  1. Sorokin, Yu.I. and Avdeev, V.A., 1991. Bacterial Production and Chemosynthesis. In: M. E. Vinogradov, ed., 1991. [Variability of the Black Sea ecosystem: Natural and Anthropogenic Factors]. Moscow: Nauka, pp. 157–166 (in Russian).
  2. Sorokin, Jy.I., Sorokin, P.Ju., Sorokin, О.V., Sorokin, D.Ju. and Sukhomlin, А.V., 1992. Distribution and Microflora Functional Activity in the Water Column of the Black Sea in Winter-Early Spring 1991. In: IO RAS, 1992. Ecosystem of the Open Black Sea in Winter. Moscow: Institute of Oceanology RАS, 1992, pp. 89–102 (in Russian).
  3. Sorokin, Jy.I., Sukhomlin, А.V. and Sorokina, О.V., 1991. Phytoplankton Primary Production in the Black Sea in Winter-Early Spring 1991. In: IO RAS, 1992. Ecosystem of the Open Black Sea in Winter. Moscow: Institute of Oceanology RАS, 1992, pp. 72–76 (in Russian).
  4. Vedernikov, V.I. and Demidov, A.B., 1997. Vertical Distribution of Primary Production and Chlorophyll During Different Seasons in the Deep Regions of the Black Sea. Oceanology, 37(3), pp. 376–384.
  5. Azam, F., 1998. Microbial Control of Oceanic Carbon Flux: the Plot Thickens. Science, 280(5364), pp. 694–696. https://doi.org/10.1126/science.280.5364.694
  6. Kopylov, A.I. and Kosolapov, D.B., 2011. [Microbial “Loop” on Planktonic Communities in Marine and Fresh-Water Ecosystems]. Izhevsk: KnigoGrad, 332 p. (in Russian).
  7. Mukhanov, V.S., Rylkova, O.A., Churilova, T.Y., Sakhon, E.G. and Pimenov, N.V., 2016. Structure and Seasonal Trophodynamics of Picophytoplankton in Sevastopol Bay and Adjacent Waters (the Black Sea). Microbiology, 85(5), pp. 553–561. https://doi.org/10.1134/S002626171605012X
  8. Mukhanov, V., Sakhon, E., Rodionova, N. and Tsai A.-Y., 2022. Journal of Marine Systems, 234, 103779. https://doi.org/10.1016/j.jmarsys.2022.103779
  9. Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A. and Thingstad F., 1982. The Ecological Role of Water – Column Microbes in the Sea. Marine Ecology Progress Series, 10, pp. 257–263. https://doi.org/10.3354/meps010257
  10. Pace, M.L., 1993. Heterotrophic Microbial Processes. In: S.R. Carpenter and J.F. Kitchell, eds., 1993. The Trophic Cascade in Lakes. Cambridge: Cambridge University Press. pp. 252–277.
  11. Boulion, V.V., 2002. [The Structure and Function of the “Microbial Loop” in the Plankton of Lake Ecosystems]. Biologiya Vnutrennih Vod, (2), pp. 5–14 (in Russian).
  12. Baines, S.B. and Pace, M.L., 1991. The Production of Dissolved Organic Matter by Phytoplankton and Its Importance to Bacteria: Patterns Across Marine and Freshwater Systems. Limnology and Oceanography, 36(6), pp. 1078–1090. https://doi.org/10.4319/lo.1991.36.6.1078
  13. Sommaruga, R., 1995. Microbial and Classical Food Webs: a Visit to a Hypertrophic Lake. FEMS Microbiology Ecology, 17(4), pp. 257–270. https://doi.org/10.1016/0168-6496(95)00030-E
  14. Boulion, V.V., Nikulina, V.N., Pavelyeva, E.B., Stepanova, L.A. and Khlebovich, Т.V., 1998. Biotic Interactions in the Ecosystem of a Potential Eutrophic Lake. Doklady Akademii Nauk, 359(2), pp. 277–279 (in Russian).
  15. Parkhomenko, A.V., 2009. Seasonal Variability of Mineral Phosphorus Uptake by Microplankton in Deep-Water Area of the Black Sea. Marine Ekological Journal, 8(2), pp. 5–23 (in Russian).
  16. Parkhomenko, A.V., 2009. Phosphates Uptake by Different Size Fractons of Microplankton in Open Part of the Black Sea. Ecology of the Sea, 77, pp. 5–10 (in Russian).
  17. Parkhomenko, A.V., 2000. Quantitative Estimation of Phosphate Uptake by Microplankton in the Black Sea During Winter Period. Ecology of the Sea, 51, pp. 14–19 (in Russian).
  18. Parkhomenko, A.V., 1984. The Use of Phosphorus-32 in Estimation of the Membrane Filter Retentivity in Experiments with Microplankton. Gidrobiologicheskiy Zhurnal, 20(2), pp. 76–79 (in Russian).
  19. Popovichev, V.N. and Parkhomenko, A.V., 2001. Methodological Aspects of the Phosphorus-32 Beta-Emission Registration by the Gas-Discharge and Scintillation Counters in the Investigations of the Phosphoric Metabolism of the Sea Particulate Matter. Ecology of the Sea, 56, pp. 107–112 (in Russian).
  20. Parkhomenko, A.V. and Kirikova, M.V., 2004. Uptake and Turnover Time of Inorganic Phosphorus in Black Sea Waters over the Autumn Season. Marine Ekological Journal, 3(2), pp. 5–23 (in Russian).
  21. Popovichev, V.N. and Egorov, V.N., 1992. Uptake of Inorganic Phosphorus by Suspended Matter in the Photic Zone. In: Polikarpov, G.G., 1992. Molismology of the Black Sea. Kiev: Naukova Dumka, pp. 62–70 (in Russian).
  22. Popovichev, V.N. and Egorov, V.N., 2003. Phosphorus Exchange of Natural Suspended Matter in the Estuaries of Danube and Corukh Rivers. Marine Ekological Journal, 2(1), pp. 83–97 (in Russian).
  23. Gutelmakher, B.L. and Pashkevich, A.I., 1987. [Methods for Measuring the Rates at which Inorganic Phosphorus is Converted into Seston and the Availability of this Element to Algae]. In: N. A. Petrova and B. L. Gutelmakher, eds., 1987. [Elements of Phosphorus Turnover in Water Bodies]. Leningrad: Nauka, pp. 32–39 (in Russian).
  24. Sorokin, Yu.I., 1985. [Quantitative Assessment of Mineral Phosphorus Fluxes in Pelagic Plankton Communities]. Zhurnal Obshchey Biologii, 46(5), pp. 606–624 (in Russian).
  25. Parkhomenko, A.V., 1984. Determination of Low Concentrations of Mineral Phosphorus in the Sea Water with Application of 32P. Gidrobiologicheskiy Zhurnal, 20(3), pp. 92–96 (in Russian).
  26. Parkhomenko, A.V., 2005. Phosphorus Excretion by Zooplankton in the Black Sea. Marine Ekological Journal, 4(4), pp. 17–32 (in Russian).
  27. Gutelmakher, B.L., 1986. [Plankton Metabolism as a Unified Whole: Trophometabolic Interactions Between Zooplankton and Phytoplankton]. Leningrad: Nauka, 154 p. (in Russian).
  28. Lebedeva, L.I., 1987. [Planktonic Animals and Phosphorus Regeneration in the Ocean]. Okeanologiya, 27(6), pp. 980–984 (in Russian).
  29. Vadstein, O., Olsen, Y. and Reinertsen, H., 1993 The Role of Planktonic Bacteria in Phosphorus Cycling in Lakes – Sink and Link. Limnology and Oceanography, 38(7), pp. 1539–1544. https://doi.org/10.4319/lo.1993.38.7.1539
  30. Donald, K.M., Joint, I., Rees, A.P., Woodward, E.M.S. and Savidge, G., 2001. Uptake of Carbon, Nitrogen and Phosphorus by Phytoplankton Along the 20oW Meridian in the NE Atlantic between 57.5oN and 37oN. Deep Sea Research Part II: Topical Studies in Oceanography, 48(4–5), pp. 873–897. https://doi.org/10.1016/S0967-0645(00)00102-8
  31. Shish, F.-K. and Ducklow, H.W., 1994. Temperature Regulation of Heterotrophic. Bacterioplankton Abundance, Production, and Specific Growth Rate in Chesapeake Bay. Limnology and Oceanography, 39(6), pp. 1243–1258. https://doi.org/10.4319/lo.1994.39.6.1243
  32. Goldman, J.C. and Dennett, M.R., 1991. Ammonium Regeneration and Carbon Utilization by Marine Bacteria Grown on Mixed Substrates. Marine Biology, 109(3), pp. 369–378. https://doi.org/10.1007/BF01313502
  33. Dolan, J.R., 1997. Phosphorus and Ammonia Excretion by Planktonic Protists. Marine Geology, 139(1–4), pp. 109–122. https://doi.org/10.1016/S0025-3227(96)00106-5
  34. Sazhin, A.F. and Kopylov, A.I., 1989. Bacterioplankton in the Oxygen Zone of the Black Sea Open Area. In: M.E. Vinogradov, M.V. Flint, eds., 1989. [The Structure and Productivity Characteristics of Planktonic Communities in the Black Sea]. Moscow: Nauka, pp. 122–139 (in Russian).
  35. Senichkina, L.G., Georgieva, L.V., Nesterova, D.A., Fashchuk, D.Ya and Lifshiz, A.V., 1991. Phytoplankton of the Black Sea in Summer Period, 1989: Biomass and Connection with Hydrological Conditions. In: M.E. Vinogradov, ed., 1991. [Variability of the Black Sea ecosystem: Natural and Anthropogenic Factors]. Moscow: Nauka, pp. 157–166 (in Russian).
  36. Churilova, T.Y., Berseneva, G.P. and Georgieva, L.V., 2004. Variability of the Biooptical Characteristics of Phytoplankton in the Black Sea. Oceanology, 44(2), pp. 192–204.
  37. Vedernikov, V.I. and Demidov, A.B., 1992. Seasonal Variability of the Primary Production and Chlorophyll in the Open Regions of the Black sea. In: M. E. Vinogradov, ed., 1992. Ecosystem of the Open Black Sea in Winter. Moscow: Institute of Oceanology RАS, pp. 77–89 (in Russian).
  38. Shushkina, E.A. and Vinogradov, M.E., 1991. [Long-Term Changes in Plankton Biomass in the Open Waters of the Black Sea]. Okeanologiya, 31(6), pp. 973–980 (in Russian).
  39. Ducklow, H.W., 1999. The Bacterial Component of the Oceanic Euphotic Zone. FEMS Microbiology Ecology, 30(1), pp. 1–10. https://doi.org/10.1016/S0168-6496(99)00031-8
  40. Vinogradov, M.E., Sapozhnikov, V.V. and Shushkina, E.A., 1992. [Ecosystem of the Black Sea]. Moscow: Nauka, 112 p. (in Russian).
  41. Moiseev, E.V., 1980. [Zooflagellates from the Open Waters of the Black Sea]. In: M. E. Vinogradov, ed., 1980. [Pelagic Ecosystems of the Black Sea]. Moscow: Nauka, pp. 174–179 (in Russian).
  42. Kopylov, A.I. and Sazhin, A.F., 1989. Reproduction Rate and Production of Heterotrophic Nanoplankton in the Open Areas of the Black Sea. In: M. E. Vinogradov and M. V. Flint, eds., 1989. [The Structure and Productivity Characteristics of Planktonic Communities in the Black Sea]. Moscow: Nauka, pp. 180–187 (in Russian).
  43. Kopylov, A.I. and Sazhin, A.F., 1989. Heterotrophic Nanoplankton in the Oxygen Zone of the Black Sea. In: M. E. Vinogradov and M. V. Flint, eds., 1989. [The Structure and Productivity Characteristics of Planktonic Communities in the Black Sea]. Moscow: Nauka, pp. 139–155 (in Russian).
  44. Kopylov, A.I., 1989. Ciliates of the Oxygen Zone of the Black Sea. In: M. E. Vinogradov and M. V. Flint, eds., 1989. [The Structure and Productivity Characteristics of Planktonic Communities in the Black Sea]. Moscow: Nauka, pp. 156–172 (in Russian).
  45. Fenchel, T.S., 1986. The Ecology of Heterotrophic Microflagellates. In: K. C. Marshall, ed., 1986. Advances in Microbial Ecology. Boston: Springer. Vol. 9, pp. 35–42. https://doi.org/10.1007/978-1-4757-0611-6_2
  46. Kopylov, A.I. and Tumantseva, N.I., 1991. Nano- and Microplankton Protozoans in the Oxygen Zone of the Black Sea in Spring, 1988. In: M. E. Vinogradov, ed., 1991. [Variability of the Black Sea ecosystem: Natural and Anthropogenic Factors]. Moscow: Nauka, pp. 118–196 (in Russian).
  47. Nagata, T., Takai, K., Kawabata, K., Nakanishi, M. and Urabe, J., 1996. The Trophic Transfer via Picoplankton – Flagellate – Copepod Food Chain During a Picocyanobacterial Bloom in Lake Biwa. Archiv für Hydrobiologie, 137(2), pp. 145–160. https://doi.org/10.1127/archiv-hydrobiol/137/1996/145
  48. Le Corre, P., Wafar, M., L'Helguen, S. and Maguer, J.F., 1996. Ammonium Assimilation and Regeneration by Size-Fractionated Plankton in Permanently Well-Mixed Temperature Waters. Journal of Plankton Research, 18(3), pp. 355–374. https://doi.org/10.1093/plankt/18.3.355
  49. Harrison, W.G., 1992. Regeneration of Nutrients. In: P. G. Falkowski, A. D. Woodshed, K. Vivirito, eds., 1992. Primary productivity and biogeochemical cycles in the Sea. New York: Plenum press. pp. 385–407. https://doi.org/10.1007/978-1-4899-0762-2_21

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