SpringerLink
Log in

Size-Morphological Structure and Ecological Strategies of Prokaryotoplankton in the Large Mountain Lake Sevan (Armenia)

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The dynamics of the size-morphological groups of heterotrophic prokaryotoplankton of the largest freshwater reservoir in the Caucasus, Lake Sevan (Armenia), has been studied, which makes it possible to explain its spatiotemporal organization and succession. The lake is characterized by an alternation of stable and unstable periods of existence of hydrobionts due to abrupt changes in environmental conditions, mainly caused by anthropogenic impacts. In the community of planktonic prokaryotes of the lake, the following size-morphological groups were distinguished: small cocci and coccobacilli, small rods and vibrios, medium-sized cocci and coccobacilli, large rods and vibrios, filaments, and particle attached cells. The main contribution (on average 55.5%) to the formation of the prokaryotoplankton biomass of the lake was made by small rods and vibrios. The biomass of each of the groups fluctuated in time and space within relatively narrow limits, and the development of the groups occurred in close relationship to each other. Apparently, different size-morphological groups of prokaryotes are adapted to exist within similar ecological and phylogenetic niches and jointly and consistently perform common functions in the mineralization of organic matter and trophic interactions in the lake. At the same time, these groups implement various ecological strategies that can be successful at different periods of the ecosystem’s existence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Andrews, J.H. and Harris, R.F., r- and K-selection and microbial ecology, in Advances in Microbial Ecology, New-York: Springer Science+Business Media, 1986, pp. 99–147.

  2. Asatryan, V., Stepanyan, L., Hovsepyan, A., Khachikyan, T., Mamyan, A., and Hambaryan, L., The dynamics of phytoplankton seasonal development and its horizontal distribution in Lake Sevan (Armenia), Environ. Monit. Assess., 2022, vol. 194, p. 757. https://doi.org/10.1007/s10661-022-10446-5

    Article  PubMed  Google Scholar 

  3. Batani, G., Pérez, G., Martínez de la Escalera, G., Piccini, C., and Fazi, S., Competition and protist predation are important regulators of riverine bacterial community composition and size distribution, J. Freshwater Ecol., 2016, vol. 31, no. 4, pp. 609–623. https://doi.org/10.1080/02705060.2016.1209443

    Article  CAS  Google Scholar 

  4. Beveridge, T.J., The bacterial surface: General considerations towards design and function, Can. J. Microbiol., 1988, vol. 34, no. 4, pp. 363–372. https://doi.org/10.1139/m88-067

    Article  CAS  PubMed  Google Scholar 

  5. Borsheim, K.Y., Native marine bacteriophages, FEMS Microbiol. Ecol., 1993, vol. 102, pp. 141–159. https://doi.org/10.1016/0378-1097(93)90197-A

    Article  Google Scholar 

  6. Caron, D.A., Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures, Appl. Environ. Microbiol., 1983, vol. 46, no. 2, pp. 491–498. https://doi.org/10.1128/aem.46.2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Caron, D.A., Dam, H.G., Kremer, P., Lessard, E.J., Madin, L.P., et al., The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda, Deep Sea Res., 1995, vol. 42, pp. 943–972. https://doi.org/10.1016/0967-0637(95)00027-4

    Article  CAS  Google Scholar 

  8. Comte, J., Jacquet, S., Viboud, S., Fontvieille, D., Millery, A., et al., Microbial community structure and dynamics in the largest natural French lake (Lake Bourget), Microb. Ecol., 2006, vol. 52, pp. 72–89. https://doi.org/10.1007/s00248-004-0230-4

    Article  CAS  PubMed  Google Scholar 

  9. Corno, G., Caravati, E., Callieri, C., and Bertoni, R., Effects of predation pressure on bacterial abundance, diversity, and size-structure distribution in an oligotrophic system, J. Limnol., 2008, vol. 67, no. 2, pp. 107–119. https://doi.org/10.4081/jlimnol.2008.107

    Article  Google Scholar 

  10. Falkowski, P.G., Fenchel, T., and Delong, E.F., The microbial engines that drive Earth’s biogeochemical cycles, Science, 2008, vol. 320, no. 5879, pp. 1034–1039. https://doi.org/10.1126/science.1153213

    Article  CAS  PubMed  Google Scholar 

  11. Fischer, U.R. and Velimirov, B., Comparative study of the abundance of various bacterial morphotypes in an eutrophic freshwater environment determined by AODC and TEM, J. Microbiol. Methods, 2000, vol. 39, no. 3, pp. 213–224. https://doi.org/10.1016/S0167-7012(99)00121-9

    Article  CAS  PubMed  Google Scholar 

  12. Foster, K.R. and Bell, T., Competition, not cooperation, dominates interactions among culturable microbial species, Curr. Biol., 2012, vol. 22, no. 19, pp. 1845–1850. https://doi.org/10.1016/j.cub.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  13. Fuhrman, J.A. and Noble, R.T., Viruses and protists cause similar bacterial mortality in coastal seawater, Limnol. Oceanogr., 1995, vol. 40, pp. 1236–1242. https://doi.org/10.4319/lo.1995.40.7.1236

    Article  Google Scholar 

  14. Garcia, A., Goñi, P., Cieloszyk, J., Fernandez, M.T., Calvo-Beguería, L., et al., Identification of free-living amoebae and amoeba-associated bacteria from reservoirs and water treatment plants by molecular techniques, Environ. Sci. Technol., 2013, vol. 47, no. 7, pp. 3132–3140. https://doi.org/10.1021/es400160k

    Article  CAS  PubMed  Google Scholar 

  15. Gasol, J.M., Del Giorgio, P.A., Massana, R., and Duarte, C.M., Active versus inactive bacteria: Size-dependence in a coastal marine plankton community, Mar. Ecol.: Prog. Ser., 1995, vol. 128, pp. 91–97. https://doi.org/10.3354/meps128091

    Article  Google Scholar 

  16. Hahn, M.W., Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones, Appl. Environ. Microbiol., 2003, vol. 69, pp. 5248–5254. https://doi.org/10.1128/AEM.69.9.5248-5254.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hahn, M.W. and Hofle, M.G., Flagellate predation on a bacterial model community: Interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition, Appl. Environ. Microbiol., 1999, vol. 65, pp. 4863–4872. https://doi.org/10.1128/AEM.65.11.4863-4872.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hahn, M.W. and Hofle, M.G., Grazing of protozoa and its effect on populations of aquatic bacteria, FEMS Microbiol. Ecol., 2001, vol. 35, pp. 113–121. https://doi.org/10.1111/j.1574-6941.2001.tb00794.x

    Article  CAS  PubMed  Google Scholar 

  19. Hambaryan, L.R., Stepanyan, L.G., Mikaelyan, M.V., and Gyurjyan, Q.G., The bloom and toxicity of cyanobacteria in Lake Sevan, Proc. Yerevan State University, Chemistry and Biology, 2020, vol. 54, no. 2, pp. 168–176. https://doi.org/10.46991/PYSU:B/2020.54.2.168

    Article  Google Scholar 

  20. Jia, Yu. and Whalen, J.K., A new perspective on functional redundancy and phylogenetic niche conservatism in soil microbial communities, Pedosphere, 2020, vol. 30, no. 1, pp. 18–24. https://doi.org/10.1016/S1002-0160(19)60826-X

    Article  CAS  Google Scholar 

  21. Jurgens, K. and Matz, C., Predation as a sha** force for the phenotypic and genotypic composition of planktonic bacteria, Antonie van Leeuwenhoek, 2002, vol. 81, pp. 413–434. https://doi.org/10.1023/a:1020505204959

    Article  CAS  PubMed  Google Scholar 

  22. Jurgens, K., Pernthaler, J., Schalla, S., and Amann, R., Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing, Appl. Environ. Microbiol., 1999, vol. 65, no. 3, pp. 1241–1250. https://doi.org/10.1128/AEM.65.3.1241-1250.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kirschner, A.K.T. and Velimirov, B., Seasonal study of bacterial community succession in a temperate backwater system indicated by variation in morphotype numbers, biomass, and secondary production, Microb. Ecol., 1997, vol. 34, pp. 27–38. https://www.jstor.org/ stable/4251501.

    Article  CAS  PubMed  Google Scholar 

  24. Kosolapov, D.B., Bacterioplankton of Lake Sevan, in Ozero Sevan. Ekologicheskoe sostoyanie v period izmeneniya urovnya vody (Lake Sevan. The Ecological State during the Change of Water Level), Yaroslavl: Filigran’, 2016, pp. 79–92.

  25. Krambeck, C., Krambeck, H.-J., and Overbeck, J., Microcomputer-assisted biomass determination of plankton bacteria on scanning electron micrographs, Appl. Environ. Microbiol., 1981, vol. 42, no. 1, pp. 142–149. https://doi.org/10.1128/aem.42.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Krylov, A.V., Hayrapetyan, A.O., Ovsepyan, A.A., Sabitova, R.Z., and Gabrielyan, B.K., Interannual changes in the spring zooplankton of the pelagic zone of Lake Sevan (Armenia) in the course of increasing fish biomass, Inland Water Biol., 2021, vol. 14, no. 1, pp. 113–116. https://doi.org/10.1134/S1995082921010053

    Article  Google Scholar 

  27. La Ferla, R., Azzaro, F., Azzaro, M., Caruso, G., Decembrini, F., et al., Microbial contribution to carbon biogeochemistry in the Central Mediterranean Sea: Variability of activities and biomass, J. Mar. Syst., 2005, vol. 57, nos. 1–2, pp. 146–166. https://doi.org/10.1016/j.jmarsys.2005.05.001

    Article  Google Scholar 

  28. Lampert, W., Daphnia: Development of a Model Organism in Ecology and Evolution, Oldendorf/Luhe: IEI Publishers, 2011.

  29. Langenheder, S. and Jurgens, K., Regulation of bacterial biomass and community structure by metazoan and protozoan predation, Limnol. Oceanogr., 2001, vol. 46, pp. 121–134. https://doi.org/10.4319/lo.2001.46.1.0121

    Article  Google Scholar 

  30. Lebaron, P., Servais, P., Agogue, H., Courties, C., and Joux F., Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems?, Appl. Environ. Microbiol., 2001, vol. 67, pp. 1775–1782. https://doi.org/10.1128/AEM.67.4.1775-1782.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Martiny, A.C., Treseder, K., and Pusch, G., Phylogenetic conservatism of functional traits in microorganisms, ISME J., 2013, vol. 7, pp. 830–838. https://doi.org/10.1038/ismej.2012.160

    Article  CAS  PubMed  Google Scholar 

  32. Newton, R.J. and Shade, A., Lifestyles of rarity: Understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere, Aquat. Microb. Ecol., 2016, vol. 78, pp. 51–63. https://doi.org/10.3354/ame01801

    Article  Google Scholar 

  33. Newton, R.J., Jones, S.E., Eiler, A., McMahon, K.D., and Bertilsson, S., A guide to the natural history of freshwater lake bacteria, Microbiol. Mol. Biol. Rev., 2011, vol. 75, no. 1, pp. 14–49. https://doi.org/10.1128/MMBR.00028-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Norland, S., The relationship between biomass and volume of bacteria, in Handbook of Methods in Aquatic Microbial Ecology, Boca Raton: Lewis Publishers, 1993, pp. 303–308.

    Google Scholar 

  35. Ozero Sevan. Ekologicheskoe sostoyanie v period izmeneniya urovnya vody (Lake Sevan. The Ecological State during the Change of Water Level), Krylov, A.V., Ed., Yaroslavl: Filigran’, 2016.

    Google Scholar 

  36. Pavlova, M.D., Asaturova, A.M., and Kozitsyn, A.E., Bacterial cell shape: Some fea-tures of ultrastructure, evolution, and ecology, Biol. Bull. Rev., 2022, vol. 12, no. 3, pp. 254–265. https://doi.org/10.1134/S2079086422030070

    Article  Google Scholar 

  37. Pernthaler, A., Pernthaler, J., and Amann, R., Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms, in Molecular Microbial Ecology Manual, Dordrecht: Kluwer Academic Publishers, 2004, pp. 711–726.

    Google Scholar 

  38. Pernthaler, J., Predation on prokaryotes in the water column and its ecological implications, Nat. Rev. Microbiol., 2005, vol. 3, pp. 537–546. https://doi.org/10.1038/nrmicro1180

    Article  PubMed  Google Scholar 

  39. Pernthaler, J., Sattler, B., Simek, K., Schwarzenbacher, A., and Psenner, R., Top-down effects on the size biomass distribution of a freshwater bacterioplankton community, Aquat. Microb. Ecol., 1996, vol. 10, pp. 255–263. https://doi.org/10.3354/ame010255

    Article  Google Scholar 

  40. Pernthaler, J., Glockner, F.-O., Unterholzner, S., Alfreider, A., Psenner, R., and Amann, R., Seasonal community and population dynamics of pelagic bacteria and Archaea in a high mountain lake, Appl. Environ. Microbiol., 1998, vol. 64, pp. 4299–4306. https://doi.org/10.1128/AEM.64.11.4299-4306.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Pernthaler, J., Posch, T., Simek, K., Vrba, J., Pernthaler, A., et al., Predator-specific enrichment of Actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture, Appl. Environ. Microbiol., 2001, vol. 67, no. 5, pp. 2145–2155. https://doi.org/10.1128/AEM.67.5.2145-2155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Porter, K.G. and Feig, Y.S., The use of DAPI for identifying and counting aquatic microflora, Limnol. Oceanogr., 1980, vol. 25, no. 5, pp. 943–948. https://doi.org/10.4319/lo.1980.25.5.0943

    Article  Google Scholar 

  43. Posch, T., Franzoi, J., Prader, M., and Salcher, M.M., New image analysis tool to study biomass and morphotypes of three major bacterioplankton groups in an alpine lake, Aquat. Microb. Ecol., 2009, vol. 54, pp. 113–126. https://doi.org/10.3354/ame01269

    Article  Google Scholar 

  44. Pradeep Ram, A.S., Nishimura, Y., Tomaru, Y., Nagasaki, K., and Nagata, T., Seasonal variation in viral-induced mortality of bacterioplankton in the water column of a large mesotrophic lake (Lake Biwa, Japan), Aquat. Microb. Ecol., 2010, vol. 58, pp. 249–259. https://doi.org/10.3354/ame01381

    Article  Google Scholar 

  45. Pradeep Ram, A.S., Mari, X., Brune, J., Torréton, J.P., Chu, V.T., et al., Bacterial-viral interactions in the sea surface microlayer of a black carbon-dominated tropical coastal ecosystem (Halong Bay, Vietnam), Elementa: Sci. Antropocene, 2018, vol. 6, p. 13. https://doi.org/10.1525/elementa.276

    Article  Google Scholar 

  46. Rothhaupt, K.O., Nutrient turnover by freshwater bacterivorous flagellates: Differences between a heterotrophic and mixotrophic chrysophyte, Aquat. Microb. Ecol., 1997, vol. 12, pp. 65–70. https://doi.org/10.3354/ame012065

    Article  Google Scholar 

  47. Sakharova, E.G., Krylov, A.V., Sabitova, R.Z., Tsvetkov, A.I., Gambaryan, L.R., et al., Horizontal and vertical distri-bution of phytoplankton in the alpine lake Sevan (Armenia) during the summer cyanoprokaryota bloom, Contemp. Probl. Ecol., 2020, vol. 13, no. 1, pp. 60–70. https://doi.org/10.1134/S1995425520010072

    Article  Google Scholar 

  48. Salcher, M.M., Same but different: Ecological niche partitioning of planktonic freshwater prokaryotes, J. Limnol., 2014, vol. 73, pp. 74–87. https://doi.org/10.4081/jlimnol.2014.813

    Article  Google Scholar 

  49. Salcher, M.M., Hofer, J., Hornák, K., Jezbera, J., Sonntag, B., et al., Modulation of microbial predator-prey dynamics by phosphorus availability. Growth patterns and survival strategies of bacterial phylogenetic clades, FEMS Microbiol. Ecol., 2007, vol. 60, pp. 40–50. https://doi.org/10.1111/j.1574-6941.2006.00274.x

    Article  CAS  PubMed  Google Scholar 

  50. Sanders, R.W., Porter, K.G., Bennett, S.J., and DeBiase, A.E., Seasonal patterns of bacteriovory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community, Limnol. Oceanogr., 1989, vol. 34, pp. 673–687. https://doi.org/10.4319/lo.1989.34.4.0673

    Article  Google Scholar 

  51. Schauer, M. and Hahn, M.W., Diversity and phylogenetic affiliations of morphologically conspicuous large filamentous bacteria occurring in the pelagic zones of a broad spectrum of freshwater habitats, Appl. Environ. Microbiol., 2005, vol. 71, no. 4, pp. 1931–1940. https://doi.org/10.1128/AEM.71.4.1931-1940.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Schuech, R., Hoehfurtner, T., Smith, D.J., and Humphries, S., Motile curved bacteria are Pareto-optimal, Proc. Natl. Acad. Sci. USA, 2019, vol. 116, no. 29, pp. 14440–14447. https://doi.org/10.1073/pnas.1818997116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Schulz, H.N. and Jørgensen, B.B., Big bacteria, Annu. Rev. Microbiol., 2001, vol. 55, pp. 105–137. https://doi.org/10.1146/annurev.micro.55.1.105

    Article  CAS  PubMed  Google Scholar 

  54. Siefert, J.L. and Fox, G.E., Phylogenetic map** of bacterial morphology, Microbiology, 1998, vol. 144, pp. 2803–2808. https://doi.org/10.1099/00221287-144-10-2803

    Article  CAS  Google Scholar 

  55. Simon, M., Grossart, H.-P., Schweitzer, B., and Ploug, H., Microbial ecology of organic aggregates in aquatic ecosystems, Aquat. Microb. Ecol., 2002, vol. 28, pp. 175–211. https://doi.org/10.3354/ame028175

    Article  Google Scholar 

  56. Thingstad, T.F., Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems, Limnol. Oceanogr., 2000, vol. 45, pp. 1320–1328. https://doi.org/10.4319/lo.2000.45.6.1320

    Article  Google Scholar 

  57. van Bergeijk, D.A., Terlouw, B.R., Medema, M.H., and van Wezel, G.P., Ecology and genomics of Actinobacteria: New concepts for natural product discovery, Nat. Rev. Microbiol., 2020, vol. 18, pp. 546–558. https://doi.org/10.1038/s41579-020-0379-y

    Article  CAS  PubMed  Google Scholar 

  58. Walsby, A.E., Stratification by cyanobacteria in lakes: A dynamic buoyancy model indicates size limitations met by Planktothrix rubescens filaments, New Phytol., 2005, vol. 168, pp. 365–376. https://doi.org/10.1111/j.1469-8137.2005.01508.x

    Article  PubMed  Google Scholar 

  59. Weinbauer, M.G., Ecology of prokaryotic viruses, FEMS Microbiol. Rev., 2004, vol. 28, pp. 127–181. https://doi.org/10.1016/j.femsre.2003.08.001

    Article  CAS  PubMed  Google Scholar 

  60. Weinbauer, M.G., Hornák, K., Jezbera, J., Nedoma, J., Dolan, J.R., and Simek, K., Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production, and diversity, Environ. Microbiol., 2007, vol. 9, pp. 777–788. https://doi.org/10.1111/j.1462-2920.2006.01200.x

    Article  CAS  PubMed  Google Scholar 

  61. Young, K.D., The selective value of bacterial shape, Microbiol. Mol. Biol. Rev., 2006, vol. 70, no. 3, pp. 660–703. https://doi.org/10.1128/MMBR.00001-06

    Article  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

We express our gratitude to A.I. Tsvetkov (Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences) for the hydrological data obtained during expeditions to Lake Sevan in 2018–2019.

Funding

This work was carried out within the framework of state assignment no. 121051100102-2.

Author information

Authors and Affiliations

  1. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Nekouzsky district, Yaroslavl region, Russia

    E. V. Kuznetsova, D. B. Kosolapov, N. G. Kosolapova & M. Yu. Skopina

  2. Cherepovets State University, 162600, Cherepovets, Vologda region, Russia

    D. B. Kosolapov

Authors
  1. E. V. Kuznetsova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. B. Kosolapov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. G. Kosolapova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Yu. Skopina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. V. Kuznetsova.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuznetsova, E.V., Kosolapov, D.B., Kosolapova, N.G. et al. Size-Morphological Structure and Ecological Strategies of Prokaryotoplankton in the Large Mountain Lake Sevan (Armenia). Biol Bull Rev 14, 286–303 (2024). https://doi.org/10.1134/S2079086424030058

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086424030058

Search

Navigation