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Anoxygenic Phototrophic Bacteria of the Meromictic Lake Bol’shie Khruslomeny (Oleniy Island, Kandalaksha Gulf, Murmansk Oblast, Russia)

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Abstract—

The composition and structure of the anoxygenic phototrophic bacterial (APB) community in the water column of meromictic Lake Bol’shie Khruslomeny during winter were investigated. The community developed at the depth of 4.25 m, and its activity in the ice-cover period was very low (6.2 µmol C L–1 day–1). The water in the zone of highest development of phototrophic bacteria was of an unusual lemon-yellow color, probably due to the production and accumulation of polysulfides. The near-bottom water was also of lemon-yellow color and was resistant to oxidation by the air oxygen. In the zone of peak APB development the content of BChl d from green-colored green sulfur bacteria was considerably higher than that of BChl e from brown-colored green sulfur bacteria: 77 and 23%, respectively. The cultures of green and purple sulfur bacteria were isolated from lake water, and their physiological and genetic characteristics were determined. Two strains of green sulfur bacteria (brown-colored BrKhr17 and green-colored GrKhr17) contained gas vacuoles in their cells. Phylogenetically they were most closely related to the green-colored strain Chlorobium phaeovibrioides DSM 265 and were identified as new strains of the species Chlorobium phaeovibrioides.

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REFERENCES

  1. Berg, J.S., Schwedt, A., Kreutzmann, A.-C., Kuypers, M.M.M., and Milucka, J., Polysulfides as intermediates in the oxidation of sulfide to sulfate by Beggiatoa spp., Appl. Environ. Microbiol., 2014, vol. 80, pp. 629–636.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bulygina, E.S., Kuznetsov, B.B., Marusina, A.I., Turova, T.P., Kravchenko, I.K., Bykova, S.A., Kolganova, T.V., and Gal’chenko, V.F., Study of nucleotide sequences of nifH genes in methanotrophic bacteria, Microbiology (Moscow), 2002, vol. 71, pp. 425‒432.

    Article  Google Scholar 

  3. Emeliantsev, P.S., Zhiltsova, A.A., Krasnova, E.D., Voronov, D.A., Rymar, V.V., and Patsaeva, S.V., Quantification of chlorosomal bacteriochlorophylls using absorption spectra of green sulfur bacteria in natural water, Moscow Univ. Phys. Bull., 2020, vol. 75, no. 2, pp. 137–142. https://doi.org/10.3103/S0027134920020046

    Article  Google Scholar 

  4. Fedulov, V.Yu., Belyaev, N.A., and Konovalov, B.V., Geochemical investigation of Lake Bol’shie Khruslomeny, Protsess. v Geosredakh, 2018, vol. 17, pp. 143–144.

  5. Gorlenko, V.M., Dubinina, G.A., and Kuznetsov, S.I., Ekologiya vodnykh mikroorganizmov (Ecology of Aquatic Microorganisms), Moscow: Nauka, 1977, pp. 62, 119–130, 151–200.

  6. Gorlenko, V.M., Mikheev, P.V., Rusanov, I.I., Pimenov, N.V., and Ivanov, M.V., Ecophysiological properties of photosynthetic bacteria from the Black Sea chemocline zone, Microbiology (Moscow), 2005, vol. 74, pp. 201‒209.

    Article  CAS  Google Scholar 

  7. Grouzdev, D.S., Lunina, O.N., Gaisin, V.A., Krutkina, M.S., Baslerov, R.V., Savvichev, A.S., and Gorlenko, V.M., Genome sequences of green- and brown-colored strains of Chlorobium phaeovibrioides with gas vesicles, Microbiol. Resour. Announc., 2019, vol. 8. e00711–19. https://doi.org/10.1128/MRA.00711-19

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., and Vinh, L.S., UFBoot2: improving the ultrafast bootstrap approximation, Mol. Biol. Evol., 2017, vol. 35, pp. 518–522. https://doi.org/10.1093/molbev/msx281

    Article  CAS  PubMed Central  Google Scholar 

  9. Jørgensen, B.B., Findlay, A.J., and Pellerin, A., The biogeochemical sulfur cycle of marine sediments, Front. Microbiol., 2019, vol. 10, p. 849. https://doi.org/10.3389/fmicb.2019.00849

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kadnikov, V.V., Savvichev, A.S., Mardanov, A.V., Beletsky, A.V., Ravin, N.V., and Pimenov, N.V., Metagenomic data of the microbial community of the chemocline layer of the meromictic subarctic Lake Bolshie Hruslomeny, North European Russia, Data in Brief, 2019, vol. 23, p. 103800. https://doi.org/10.1016/j.dib.2019.103800

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A., and Jermiin, L.S., ModelFinder: fast model selection for accurate phylogenetic estimates, Nat. Methods, 2017, vol. 14, pp. 587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Katoh, K. and Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 2013, vol. 30, pp. 772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kharcheva, A.V., Krasnova, E.D., Gorlenko, V.M., Lunina, O.N., Savvichev, A.S., Voronov, D.A., Zhiltsova, A.A., and Patsaeva, S.V., Depth profiles of spectral and hydrological characteristics of water and their relation to abundances of green sulfur bacteria in the stratified lakes of the White Sea, Proc. SPIE‒The International Society for Optical Engineering, 2016, vol. 9917, pp. 99170Q-1–99170Q-16. https://doi.org/10.1117/12.2229855

  14. Kharcheva, A.V., Zhiltsova, A.A., Lunina, O.N., Krasnova, E.D., Voronov, D.A., Savvichev, A.S., and Patsaeva, S.V., Bacteriochlorophyll fluorescence of green sulfur bacteria in the anaerobic zone of two natural water bodies, Moscow Univ. Phys. Bull., 2018, vol. 73, no. 4, pp. 377–381. https://doi.org/10.3103/S0027134918040082

    Article  Google Scholar 

  15. Kharcheva, A.V., Zhiltsova, A.A., Lunina, O.N., Savvichev, A.S., and Patsaeva, S.V., Quantification of two forms of green sulfur bacteria in their natural habitat using bacteriochlorophyll fluorescence spectra, Proc. SPIE, 2016b, vol. 9917, pp. 99170P-0–99170P-8. https://doi.org/10.1117/12.2229848

  16. Kleinjan, W.E., Keizer, A., and Janssen, A.J.H., Biologically produced sulfur, Top. Curr. Chem., 2003, vol. 230, pp. 167–188. https://doi.org/10.1007/b12114

    Article  CAS  Google Scholar 

  17. Krasnova, E.D. and Voronov, D.A., An underwater meromictic lake in the Biofilter Bay (White Sea, Kandalaksha Gulf, area of the MSU White Sea Biological Station), Geol. Morei i Okeanov: Proc. 27th Int. Sci. Conf (School) on Marine Geology, Moscow: IO RAN, 2019, vol. 3, pp. 165–169.

  18. Krasnova, E.D., Voronov, D.A., Demidenko, N.A., Kokryatskaya, N.M., Pantyulin, A.N., Rogatykh, T.A., Samsonov, T.E., Frolova, N.L., and Shaporenko, S.I., On inventarization of the relic basins separating from the White Sea: comprehensive studies of the Bab’e More, a semi-isolated White Sea lagoon: geology,hydrology, and biota‒changes accompanying shore transgression, Trudy Belomor. Biol. St. Mos. Gos. Univ., Moscow: KMK, 2016, vol. 12, pp. 211–241.

    Google Scholar 

  19. Krasnova, E., Matorin, D., Belevich, T., Efimova, L., Kharcheva, A., Kokryatskaya, N., Losyuk, G., Todorenko, D., Voronov, D., and Patsaeva, S., The characteristic pattern of multiple colored layers in coastal stratified lakes in the process of separation from the White Sea, Chinese J. Oceanol. Limnol., 2018, pp. 1–16. https://doi.org/10.1007/s00343-018-7323-2

  20. Lane, D.J., 16S/23S sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., Chichester: Wiley, 1991, pp. 115–175. https://doi.org/10.12691/jaem-2-4-11

    Book  Google Scholar 

  21. Lis, G., Biokhimiya avtotrofnykh bakterii (Biochemistry of Autotrophic Bacteria), Moscow: In. Lit., 1958.

  22. Lunina, O.N., Savvichev, A.S., Babenko, V.V., Boldyreva, D.I., Kuznetsov, B.B., Kolganova, T.V., Krasnova, E.D., Kokryatskaya, N.M., Veslopolova, E.F., Voronov, D.A., Demidenko, N.A., Letarova, M.A., Letarov, A.V., and Gorlenko, V.M., Seasonal changes in the community structure of anoxygenic phototrophic bacteria in meromictic Trekhtsvetnoe Lake (Kandalaksha Bay, White sea), Microbiology (Moscow), 2019, vol. 88, pp. 100–114. https://doi.org/10.1134/S0026261719010041

    Article  CAS  Google Scholar 

  23. Lunina, O.N., Savvichev, A.S., Krasnova, E.D., Kokryatskaya, N.M., Veslopolova, E.F., Kuznetsov, B.B., and Gorlenko, V.M., Succession processes in the anoxygenic phototrophic bacterial community in Lake Kislo-Sladkoe (Kandalaksha Bay, White Sea), Microbiology (Moscow), 2016, vol. 85, pp. 570–582. https://doi.org/10.1134/S0026261716050118

    Article  CAS  Google Scholar 

  24. Lunina, O.N., Savvichev, A.S., Kuznetsov, B.B., Pimenov, N.V., and Gorlenko, V.M., Anoxygenic phototrophic bacteria of the Kislo-Sladkoe stratified lake (White Sea, Kandalaksha Bay), Microbiology (Moscow), 2013, vol. 82, pp. 815–832. https://doi.org/10.1134/S0026261714010081

    Article  CAS  Google Scholar 

  25. Montesinos, E., Guerrero, R., Abella, C., and Esteve, I., Ecology and physiology of the competition for light between Chlorobium limicola and Chlorobium paeobacteroides in natural habitans, Appl. Environ. Microbiol., 1983, vol. 46, p. 1008. https://doi.org/10.1128/aem.46.5.1007-1016.1983

    Article  Google Scholar 

  26. Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B.Q., IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 2015, vol. 32, pp. 268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  27. Overmann, J. and Tilzer, M.M., Control of primary productivity and the significance of photosynthetic bacteria in a meromictic kettle Lake Mittlerer Buchensee, West-Germany, Aquatic Sci., 1989, vol. 51, p. 4. https://doi.org/10.1007/bf00877171

    Article  Google Scholar 

  28. Pfennig, N. and Lippert, K.D., Über das Vitamin B12-Bedürfnis phototropher Schwefelbakterien, Arch. Mikro-biol., 1966, vol. 55, pp. 245–256. https://doi.org/10.1007/BF00410246

    Article  CAS  Google Scholar 

  29. Prange, A., Arzberger, I., Engemann, C., Modrow, H., Schumann, O., Trüper, H.G., Steudel, R., Dahl, C., and Hormes, J., In situ analysis of sulfur in the sulfur globules of phototrophic sulfur bacteria by X-ray absorption near edge spectroscopy, Biochim. Biophys. Acta, 1999, vol. 1428, pp. 446–454.

    Article  CAS  PubMed  Google Scholar 

  30. Saint-Hilare, K.K., Report on the White Sea excursion of the Yur’ev University natural sciences students in summer 1908, Uch. Zap. Imper. Yur’ev Univ., 1909, vol. 17, pp. 1–67.

    Google Scholar 

  31. Sanger, F., Nicklen, S., and Coulson, A.R., DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. U. S. A., 1977, vol. 84, pp. 5463–5467. https://doi.org/10.1073/pnas.74.12.5463

    Article  Google Scholar 

  32. Savvichev, A.S., Kadnikov, V.V., Kallistova, A.Yu., Rusanov, I.I., Voronov, D.A., Krasnova, E.D., Ravin, N.V., and Pimenov, N.V., Light-dependent methane oxidation is the major process of the methane cycle in the water column of the Bol’shie Khruslomeny Polar Lake, Microbiology (Moscow), 2019, vol. 88, pp. 370–374. https://doi.org/10.1134/S0026365619030108

    Article  CAS  Google Scholar 

  33. Savvichev, A.S., Kadnikov, V.V., Rusanov, I.I., Beletsky, A.V., Krasnova, E.D., Voronov, D.A., Kallistova, A.Yu., Veslopolova, E.F., Zakharova, E.E., Kokryatskaya, N.M., Losyuk, G.N., Demidenko, N.A., Belyaev, N.A., Sigalevich, P.A., Mardanov, A.V., Ravin, N.V., and Pimenov N.V., Microbial processes and microbial communities in the water column of the polar meromictic lake Bol’shie Khruslomeny at the White Sea coast, Front. Microbiol., 2020, vol. 11, p. 1945. https://doi.org/10.3389/fmicb.2020.01945

    Article  PubMed  PubMed Central  Google Scholar 

  34. Savvichev, A.S., Kulakova, A.A., Krasnova, E.D., Voronov, D.A., Kadnikov, V.V., Beletskii, A.V., Kozyaeva, V.V., Rusanov, I.I., Letarova, M.A., Veslopolova, E.F., Belenkova, V.V., Demidenko, N.A., and Gorlenko, V.M., Microbial community of a marine meromictic trough (Biofilter Bay) in the Kandalaksha Bay, White Sea, Microbiology (Moscow), 2022, vol. 91, pp. 432–444. https://doi.org/10.1134/S0026261722100940

    Article  CAS  Google Scholar 

  35. Zhiltsova, A.A., Filippova, O.A., Krasnova, E.D., Voronov, D.A., and Patsaeva, S.V., Comparative analysis of spectral methods for determining bacteriochlorophyll d concentration in green sulfur bacteria in water, Atmospheric and Oceanic Optics, 2022, vol. 35, pp. 5627–568. https://doi.org/10.15372/AOO20220411

    Article  Google Scholar 

  36. Zhiltsova, A.A., Kharcheva, A.V., Krasnova, E.D., Lunina, O.N., Voronov, D.A., Savvichev, A.S., Gorshkova, O.M., and Patsaeva, S.V., Spectroscopic study of green sulfur bacteria in stratified water bodies of the Kandalaksha Gulf of the White Sea, Atmospheric and Oceanic Optics, 2018, vol. 31, pp. 390–396. https://doi.org/10.15372/AOO20180315

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

The authors are grateful to V.M. Gorlenko for comprehensive support during the work and to T.V. Kolganova and I.I. Rusanov for giving expert advice during the preparation of the article.

Funding

This work was supported by the Ministry of Science and Higher Education of the Russian Federation (state assignment of the Federal Research Center for Biotechnology, Russian Academy of Sciences). Biogeochemical and molecular genetic studies were supported by the Russian Science Foundation, project no. 23-24-00208.

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Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, 117312, Moscow, Russia

    O. N. Lunina, E. F. Veslopolova & A. S. Savvichev

  2. ciBear OU, Tartu Mnt 67/1-13b, Kesklinna Linnaosa, 10115, Tallinn, Estonia

    D. S. Grouzdev

  3. Faculty of Physics, Moscow State University, 119234, Moscow, Russia

    S. V. Patsaeva & A. A. Zhil’tsova

  4. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”, 142290, Pushchino, Russia

    N. E. Suzina

  5. Pertsov White Sea Biological Station, Biological Faculty, Moscow State University, 119234, Moscow, Russia

    E. D. Krasnova

  6. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, 127051, Moscow, Russia

    D. A. Voronov

  7. Laverov Federal Center for Integrated Arctic Research, Ural Branch, Russian Academy of Sciences, 163020, Arkhangelsk, Russia

    N. M. Kokryatskaya

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  1. O. N. Lunina
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  6. E. D. Krasnova
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  8. N. M. Kokryatskaya
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Correspondence to O. N. Lunina.

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Lunina, O.N., Grouzdev, D.S., Patsaeva, S.V. et al. Anoxygenic Phototrophic Bacteria of the Meromictic Lake Bol’shie Khruslomeny (Oleniy Island, Kandalaksha Gulf, Murmansk Oblast, Russia). Microbiology 92, 792–806 (2023). https://doi.org/10.1134/S0026261723602051

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