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Environmental Features of Freshwater Planktonic Actinobacteria

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Contemporary Problems of Ecology Aims and scope

Abstract

This overview deals with freshwater actinobacteria (one of the dominant groups of the heterotrophic bacterioplankton), their biology and ecology, and their role in cycling some of the main biogenic elements and in the transformation of recalcitrant organic compounds in freshwater reservoirs. The most distinctive features of the most abundant groups of planktonic freshwater actinobacteria, methods of isolation, obtaining pure cultures, and further cultivation have been considered. The general and individual ecophysiological, phenotypic, genotypic, and metabolic characteristics are given.

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REFERENCES

  1. Allgaier, M. and Grossart, H.P., Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany, Appl. Environ. Microbiol., 2006, vol. 72, no. 5, pp. 3489–3497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Barka, E.A., Vatsa, P., Sanchez, L., Gaveau-Vaillant, N., Jacquard, C., Meier-Kolthoff, J.P., Klenk, H.P., Clément, C., Ouhdouch, Y., and van Wezel, G.P., Taxonomy, physiology, and natural products of Actinobacteria, Microbiol. Mol. Biol. Rev., 2015, vol. 80, no. 1, pp. 1–43.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Beier, S. and Bertilsson, S., Uncoupling of chitinase activity and uptake of hydrolysis products in freshwater bacterioplankton, Limnol. Oceanogr., 2011, vol. 56, no. 4, pp. 1179–1188.

    Article  CAS  Google Scholar 

  4. Biderre-Petit, C., Boucher, D., Kuever, J., Alberic, P., Jézéquel, D., Chebance, B., Borrel, G., Fonty, G., and Peyret, P., Identification of sulfur-cycle prokaryotes in a low-sulfate lake (Lake Pavin) using aprA and 16S rRNA gene markers, Microb. Ecol., 2011, vol. 61, no. 2, pp. 313–327.

    Article  CAS  PubMed  Google Scholar 

  5. Boucher, D., Jardillier, L., and Debroas, D., Succession of bacterial community composition over two consecutive years in two aquatic systems: a natural lake and a lake-reservoir, FEMS Microbiol Ecol., 2006, vol. 55, no. 1, pp. 79–97.

    Article  CAS  PubMed  Google Scholar 

  6. Buck, U., Grossart, H.-P., Amann, R., and Pernthaler, J., Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake, Environ. Microbiol., 2009, vol. 11, no. 7, pp. 1854–1865.

    Article  CAS  PubMed  Google Scholar 

  7. Bunse, C., Bertos-Fortis, M., Sassenhagen, I., Sildever, S., Sjöqvist, C., Godhe, A., Gross, S., Kremp, A., Lips, I., Lundholm, N., Rengefors, K., Sefbom, J., Pinhassi, J., and Legrand, C., Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom, Front. Microbiol., 2016, vol. 7, pp. 1–10.

    Article  Google Scholar 

  8. Burman, N.P., The occurrence and significance of actinomycetes in water supply, in Actinomycetales: Characteristics and Practical Importance, Soc. Appl. Bacteriol. Symp. Ser. no. 2, New York: Academic, 1973, pp. 219–230.

  9. Button, D.K., Schut, F., Quang, P., Martin, R., and Robertson, B.R., Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results, Appl. Environ. Microbiol., 1993, vol. 59, no. 3, pp. 881–891.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cabello-Yeves, P.J., Zemskaya, T.I., Rosselli, R., Coutinho, F.H., Zakharenko, A.S., Blinov, V.V., and Rodriguez-Valera, F., Genomes of novel microbial lineages assembled from the sub-ice waters of Lake Baikal, Appl. Environ. Microbiol., 2018, vol. 84, no. 1, pp. 1–21.

    Article  CAS  Google Scholar 

  11. Cho, J.C. and Giovannoni, S.J., Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria, Appl. Environ. Microbiol., 2004, vol. 70, no. 1, pp. 432–440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Clingenpeel, S., Macur, R.E., Kan, J., Inskeep, W.P., Lovalvo, D., Varley, J., Mathur, E., Nealson, K., Gorby, Y., Jiang, H., La Fracois, T., and McDermott, T.R., Yellowstone Lake: high-energy geochemistry and rich bacterial diversity, Environ. Microbiol., 2011, vol. 13, no. 8, pp. 2172–2185.

    Article  PubMed  Google Scholar 

  13. Connon, S.A. and Giovannoni, S.J., High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates, Appl. Environ. Microbiol., 2002, vol. 68, no. 8, pp. 3878–3885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Cross, T., Aquatic actinomycetes: a critical survey of the occurrence, growth and role of actinomycetes in aquatic habitats, J. Appl. Bacteriol., 1981, vol. 50, no. 3, pp. 397–423.

    Article  CAS  PubMed  Google Scholar 

  15. Crump, B.C., Peterson, B.J., Raymond, P.A., Amon, R.M.W., Rinehart, A., McClelland, J.W., and Holmes, R.M., Circumpolar synchrony in big river bacterioplankton, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 50, pp. 21208–21212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Debroas, D., Humbert, J.F., Enault, F., Bronner, G., Faubladier, M., and Cornillot, E., Metagenomic approach studying the taxonomic and functional diversity of the bacterial community in a mesotrophic lake (Lac du Bourget–France), Environ. Microbiol., 2009, vol. 11, no. 9, pp. 2412–2424.

    Article  CAS  PubMed  Google Scholar 

  17. Duda, V.I., Suzina, N.E., Polivtseva, V.N., and Boronin, A.M., Ultramicrobacteria: formation of the concept and contribution of ultramicrobacteria to biology, Microbiology (Moscow), 2012, vol. 81, no. 4, pp. 379–390.

    Article  CAS  Google Scholar 

  18. Eckert, E.M., Salcher, M.M., Posch, T., Eugster, B., and Pernthaler, J., Rapid successions affect microbial n‑acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom, Environ. Microbiol., 2012, vol. 14, no. 3, pp. 794–806.

    Article  CAS  PubMed  Google Scholar 

  19. Eckert, E.M., Baumgartner, M., Huber, I. M., and Pernthaler, J., Grazing resistant freshwater bacteria profit from chitin and cell-wall-derived organic carbon, Environ. Microbiol., 2013, vol. 15, no. 7, pp. 2019–2030.

    Article  CAS  PubMed  Google Scholar 

  20. Elifantz, H., Malmstrom, R.R., Cottrell, M.T., and Kirchman, D.L., Assimilation of polysaccharides and glucose by major bacterial groups in the Delaware estuary, Appl. Environ. Microbiol., 2005, vol. 71, no. 12, pp. 7799–7805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fuhrman, J.A., McCallum, K., and Davis, A.A., Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific oceans, Appl. Environ. Microbiol., 1993, vol. 59, pp. 1294–1302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Garcia, S.L., McMahon, K.D., Martinez-Garcia, M., Srivastava, A., Sczyrba, A., Stepanauskas, R., Grossart, H.P., Woyke, T., and Warnecke, F., Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton, ISME J., 2013, vol. 7, no. 1, pp. 137–147.

    Article  CAS  PubMed  Google Scholar 

  23. Garcia, S.L., McMahon, K.D., Grossart, H.P., and Warnecke, F., Successful enrichment of the ubiquitous freshwater acl Actinobacteria, Environ. Microbiol. Rep., 2014, vol. 6, no. 1, pp. 21–27.

    Article  CAS  PubMed  Google Scholar 

  24. Ghai, R., Rodŕíguez-Valera, F., McMahon, K.D., Toyama, D., Rinke, R., Souza de Oliveira, T.C., Garcia, J.W., Pellon de Miranda, F., and Henrique-Silva, F., Metagenomics of the water column in the pristine upper course of the Amazon River, PLoS One, 2011, vol. 9, no. 5, pp. 1–12.

    Google Scholar 

  25. Ghai, R., McMahon, K.D., and Rodriguez-Valera, F., Breaking a paradigm: cosmopolitan and abundant freshwater Actinobacteria are low GC, Environ. Microbiol. Rep., 2012, vol. 4, no. 1, pp. 29–35.

    Article  CAS  PubMed  Google Scholar 

  26. Ghai, R., Mizuno, C.M., Picazo, A., Camacho, A., and Rodriguez-Valera, F., Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing, Mol. Ecol., 2014, vol. 23, no. 24, pp. 6073–6090.

    Article  CAS  PubMed  Google Scholar 

  27. Ghylin, T.W., Garcia, S.L., Moya, F., Oyserman, B.O., Schwientek, P., Forest, K.T., Mutschler, J., Dwulit-Smith, J., Chan, L.K., Martinez-Garcia, M., Sczyrba, A., Stepanauskas, R., Grossart, H.-P., Woyke, T., Warnecke, F., et al., Comparative single-cell genomics reveals potential ecological niches for the freshwater acl Actinobacteria lineage, ISME J., 2014, vol. 8, no. 12, pp. 2503–2516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Giovannoni, S.J., Thrash, J.C., and Temperton, B., Implications of streamlining theory for microbial ecology, ISME J., 2014, vol. 8, no. 8, pp. 1553–1565.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Glöckner, F.O., Zaichikov, E., Belkova, N., Denissova, L., Pernthaler, J., Pernthaler, A., and Amann, R., Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria, Appl. Environ. Microbiol., 2000, vol. 66, no. 11, pp. 5053–5065.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Goodfellow, M. and Williams, S.T., Ecology of actinomycetes, Annu. Rev. Microbiol., 1983, vol. 37, pp. 189–216.

    Article  CAS  PubMed  Google Scholar 

  31. Gregersen, L.H., Habicht, K.S., Peduzzi, S., Tonolla, M., Canfield, D.E., Miller, M., Cox, R.P., and Frigaard, N.U., Dominance of a clonal green sulfur bacterial population in a stratified lake, FEMS Microbiol. Ecol., 2009, vol. 70, no. 1, pp. 30–41.

    Article  CAS  PubMed  Google Scholar 

  32. Hahn, M.W., Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria, Int. J. Syst. Evol. Microbiol., 2009, vol. 59, pp. 112–117.

    Article  CAS  PubMed  Google Scholar 

  33. Hahn, M.W. and Pöckl, M., Ecotypes of planktonic Actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats, Appl. Environ. Microbiol., 2005, vol. 71, no. 2, pp. 766–773.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hahn, M.W., Lunsdorf, H., Wu, Q., Schauer, M., Höfle, M.G., Boenigk, J., and Stadler, P., Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia, Appl. Environ. Microbiol., 2003, vol. 69, no. 3, pp. 1442–1451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hahn, M.W., Stadler, P., Wu, Q.L., and Pöckl, M., The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria, J. Microbiol. Methods, 2004, vol. 57, no. 3, pp. 379–390.

    Article  CAS  PubMed  Google Scholar 

  36. Hahn, M.W., Schmidt, J., Taipale, S.J., Doolittle, W.F., and Koll, U., Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome, Int. J. Syst. Evol. Microbiol., 2014, vol. 64, pp. 3254–3263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hiorns, W.D., Methe, B.A., Nierzwicki-Bauer, S.A., and Zehr, J.P., Bacterial diversity in Adirondack mountain lakes as revealed by 16S rRNA gene sequences, Appl. Environ. Microbiol., 1997, vol. 63, no. 7, pp. 2957–2960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Holmfeldt, K., Dziallas, C., Titelman, J., Pohlmann, K., Grossart, H.P., and Riemann, L., Diversity and abundance of freshwater Actinobacteria along environmental gradients in the brackish northern Baltic Sea, Environ. Microbiol., 2009, vol. 11, no. 8, pp. 2042–2054.

  39. Huang, Y., Zeng, Y., Lu, H., Feng, H., Zeng, Y., and Koblížek, M., Novel acsF gene primers revealed a diverse phototrophic bacterial population, including Gemmatimonadetes, in Lake Taihu (China), Appl. Environ. Microbiol., 2016, vol. 82, no. 18, pp. 5587–5594.

  40. Humbert, J.F., Dorigo, U., Cecchi, P., Le Berre, B., Debroas, D., and Bouvy, M., Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems, Environ. Microbiol., 2009, vol. 11, no. 9, pp. 2339–2350.

    Article  CAS  PubMed  Google Scholar 

  41. Ivanova, E.P., Bakunina, I.Yu., Gorshkova, N.M., Romanenko, L.A., Mikhailov, V.V., Elyakov, L.A., and Parfenova, V.V., Distribution of chitin-decomposing enzymes in marine and freshwater microorganisms, Biol. Morya (Vladivostok), 1992, nos. 3–4, pp. 69–75.

  42. Jezbera, J., Hornak, K., and Šimek, K., Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization, FEMS Microbiol. Ecol., 2005, vol. 52, no. 3, pp. 351–363.

    Article  CAS  PubMed  Google Scholar 

  43. Jezbera, J., Sharma, A.K., Brandt, U., Doolittle, W.F., and Hahn, M.W., Candidatus “Planktophila limnetica”, an Actinobacterium representing one of the most numerically important taxa in freshwater bacterioplankton, Int. J. Syst. Evol. Microbiol., 2009, vol. 59, pp. 2864–2869.

    Article  CAS  PubMed  Google Scholar 

  44. Jiang, C.L. and Xu, H.L., Diversity of aquatic actinomycetes in lakes of the Middle Plateau, Yunnan, China, Appl. Environ. Microbiol., 1996, vol. 62, no. 1, pp. 249–253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jin, L., Huy, H., Kim, K.K., Lee, H.G., Kim, H.S., Ahn, Ch.Y., and Oh, H.M., Aquihabitans daechungensis gen. nov., sp. nov., an Actinobacterium isolated from reservoir water, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 2970–2974.

    Article  CAS  PubMed  Google Scholar 

  46. Kan, J., Evans, S.E., Chen, F., and Suzuki, M.T., Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay, Aquat. Microbiol. Ecol., 2008, vol. 51, pp. 55–66.

    Article  Google Scholar 

  47. Kang, I., Lee, K., Yang, S.J., Choi, A., Kang, D., Lee, Y.K., and Cho, J.C., Genome sequence of Candidatus “Aquiluna” sp. strain IMCC13023, a marine member of the Actinobacteria isolated from an arctic fjord, J. Bacteriol., 2012, vol. 194, no. 13, pp. 3550–3551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kang, I., Kim, S., Islam, M.R., and Cho, J.C., The first complete genome sequences of the acI lineage, the most abundant freshwater Actinobacteria, obtained by whole genome-amplification of dilution to-extinction cultures, Sci. Rep., 2017, vol. 7, pp. 1–13.

    CAS  Google Scholar 

  49. Karlov, D.S., Marie, D., Chuvochina, M.S., Alekhina, I.A., and Bulat, S.A., Microbial communities of water column of Lake Radok, East Antarctica, dominated by abundant actinobacterium “Candidatus Planktophila limnetica,” Microbiology (Moscow), 2011, vol. 80, no. 4, pp. 576–579.

    Article  CAS  Google Scholar 

  50. Kim, S., Kang, I., Seo, J.-H., and Cho, J.C., Culturing the ubiquitous freshwater actinobacterial acI lineage by supplying a biochemical ‘helper’ catalase, ISME J., 2019, vol. 13, no. 9, pp. 2252–2263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kirchman, D.L. and Hanson, T.E., Bioenergetics of photoheterotrophic bacteria in the oceans, Environ. Microbiol. Rep., 2013, vol. 5, no. 2, pp. 188–199.

    Article  CAS  PubMed  Google Scholar 

  52. Kormas, K.A., Vardaka, E., Moustaka-Gouni, M., Kontoyanni, V., Petridou, E., Gkelis, S., and Neofitou, C., Molecular detection of potentially toxic cyanobacteria and their associated bacteria in lake water column and sediment, World J. Microbiol. Biotechnol., 2010, vol. 26, no. 8, pp. 1473–1482.

    Article  CAS  Google Scholar 

  53. Lapteva, N.A., Specific characteristics of heterotrophic bacteria in Lake Baikal, Mikrobiologiya (Moscow), 1990, vol. 59, no. 3, pp. 499–506.

    Google Scholar 

  54. Li, H., Xing, P., Chen, M., Bian, Yu., and Wu, Q.L., Short-term bacterial community composition dynamics in response to accumulation and breakdown of Microcystis blooms, Water Res., 2011, vol. 45, no. 4, pp. 1702–1710.

    Article  CAS  PubMed  Google Scholar 

  55. Lindh, M.V., Lefebure, R., Degerman, R., Lundin, D., Andersson, A., and Pinhassi, J., Consequences of increased terrestrial dissolved organic matter and temperature on bacterioplankton community composition during a Baltic Sea mesocosm experiment, Ambio, 2015, vol. 44, pp. 402–412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lipko, I.A., Phylogeny of the freshwater lineages within the phyla Actinobacteria (Overview), Limnol. Freshwater Biol., 2020, vol. 3, no. 1, pp. 358–363.

    Article  Google Scholar 

  57. Liu, Y., Yao, T., Jiao, N., Kang, S., Zeng, Y., and Huang, S., Microbial community structure in moraine lakes and glacial meltwaters, Mount Everest, FEMS Microbiol. Lett., 2006, vol. 265, no. 1, pp. 98–105.

    Article  CAS  PubMed  Google Scholar 

  58. Liu, Y., Yao, T., Jiao, N., Tian, L., Hu, A., Yu, W., and Li, S., Microbial diversity in the snow, a moraine lake and a stream in Himalayan glacier, Extremophiles, 2011, vol. 15, no. 3, pp. 411–421.

    Article  PubMed  Google Scholar 

  59. Ludwig, W., Euzéby, J., Schumann, P., Busse, H.-J., Trujillo, M.E., Kämpfer, P., and Whitman, W.B., Road map of the phylum Actinobacteria, in Bergey’s Manual of Systematic Bacteriology, New York: Springer-Verlag, 2012, pp. 1–28.

    Google Scholar 

  60. Maksimova, E.A. and Maksimov, V.N., Mikrobiologiya vod Baikala (Microbiology of Baikal Lake Waters), Irkutsk: Irkutsk. Gos. Univ., 1989.

  61. Maresca, J.A., Keffer, J.L., Hempel, P.P., Polson, S.W., Shevchenko, O., Bhavsar, J., Powell, D., Miller, K.J., Singh, A., and Hahn, M.W., Light modulates the physiology of nonphototrophic Actinobacteria, J. Bacteriol., 2019, vol. 201, no. 10, pp. 1–20.

    Article  Google Scholar 

  62. Martinez-Garcia, M., Swan, B.K., Poulton, N.J., Gomez, M.L., Masland, D., Sieracki, M.E., and Stepanauskas, R., High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton, ISME J., 2012, vol. 6, no. 1, pp. 113–123.

    Article  CAS  PubMed  Google Scholar 

  63. Matsumoto, A., Kasai, H., Matsuo, Y., Omura, S., Shizuri, Y., and Takahashi, Y., Ilumatobacter fluminis gen. nov., sp. nov., a novel Actinobacterium isolated from the sediment of an estuary, J. Gen. Appl. Microbiol., 2009, vol. 55, no. 3, pp. 201–205.

    Article  CAS  PubMed  Google Scholar 

  64. Matsumoto, A., Kasai, H., Matsuo, Y., Shizuri, Y., Ichikawa, N., Fujita, N., Omura, S., and Takahashi, Y., Ilumatobacter nonamiense sp. nov. and Ilumatobacter coccineum sp. nov., isolated from seashore sand, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, no. 9, pp. 3404–3408.

    Article  CAS  PubMed  Google Scholar 

  65. Methé, B.A., Hiorns, W.D., and Zehr, J.P., Contrasts between marine and freshwater bacterial community composition: analyses of communities in Lake George and six other Adirondack lakes, Limnol. Oceanogr., 1998, vol. 43, no. 2, pp. 368–374.

    Article  Google Scholar 

  66. Mueller-Spitz, S.R., Goetz, G.W., and McLellan, S.L., Temporal and spatial variability in near-shore bacterioplankton communities of Lake Michigan, FEMS Microbiol. Ecol., 2009, vol. 67, no. 3, pp. 511–522.

    Article  CAS  PubMed  Google Scholar 

  67. Neuenschwander, S.M., Ghai, R., Pernthaler, J., and Salcher, M.M., Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria, ISME J., 2018, vol. 12, no. 1, pp. 185–198.

    Article  CAS  PubMed  Google Scholar 

  68. Newton, R.J., Jones, S.E., Helmus, M.R., and McMahon, K.D., Phylogenetic ecology of the freshwater Actinobacteria acI lineage, Appl. Environ. Microbiol., 2007, vol. 73, no. 22, pp. 7169–7176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Parveen, B., Reveilliez, J.-P., Mary, I., Ravet, V., Bronner, G., Mangot, J.F., Domaizon, I., and Debroas, D., Diversity and dynamics of free-living and particle-associated Betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities, FEMS Microbiol. Ecol., 2011, vol. 77, no. 3, pp. 461–476.

    Article  CAS  PubMed  Google Scholar 

  71. Percent, S.F., Frischer, M.E., Vescio, P.A., Duffy, E.B., Milano, V., McLellan, M., Stevens, B.M., Boylen, C.W., and Nierzwicki-Bauer, S.A., Bacterial community structure of acid-impacted lakes: what controls diversity? Appl. Environ. Microbiol., 2008, vol. 74, no. 6, pp. 1856–1868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Pérez, M.T., Hörtnagl, P., and Sommaruga, R., Contrasting ability to take up leucine and thymidine among freshwater bacterial groups: implications for bacterial production measurements, Environ. Microbiol., 2010, vol. 12, no. 1, pp. 74–82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Pérez, M.T., Rofner, C., and Sommaruga, R., Dissolved organic monomer partitioning among bacterial groups in two oligotrophic lakes, Environ. Microbiol. Rep., 2015, vol. 7, no. 2, pp. 265–272.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Pernthaler, J., Posch, T., Šimek, K., Vrba, J., Pernthaler, A., Glöckner, F.O., Nubel, U., Psenner, R., and Amann, R., 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Pitt, A., Schmidt, J., Koll, U., and Hahn, M.W., Rhodoluna limnophila sp. nov., a bacterium with 1.4 Mbp genome size isolated from freshwater habitats located in Salzburg, Austria, Int. J. Syst. Evol. Microbiol., 2019, vol. 69, no. 12, pp. 3946–3954.

    Article  CAS  PubMed  Google Scholar 

  76. Proctor, C.R., Besmer, M.D., Langenegger, T., Beck, K., Walser, J.C., Ackermann, M., Bürgmann, H., and Hammes, F., Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems, ISME J., 2018, vol. 12, no. 5, pp. 1344–1359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Rappé, M.S., Gordon, D.A., Vergin, K.L., and Giovannoni, S.J., Phylogeny of Actinobacteria small subunit (SSU) rRNA gene clones recovered from marine bacterioplankton, Syst. Appl. Microbiol., 1999, vol. 22, pp. 106–112.

    Article  Google Scholar 

  78. Rheims, H., Felske, A., Seufert, S., and Stackebrandt, E., Molecular monitoring of an uncultured group of the class Actinobacteria in two terrestrial environments, J. Microbiol. Methods, 1999, vol. 36, nos. 1–2, pp. 65–75.

    Article  CAS  PubMed  Google Scholar 

  79. Riemann, L., Leitet, C., Pommier, T., Simu, K., Holmfeldt, K., Larsson, U., and Hagstro, A., The native bacterioplankton community in the central Baltic Sea is influenced by freshwater bacterial species, Appl. Environ. Microbiol., 2008, vol. 74, no. 2, pp. 503–515.

    Article  CAS  PubMed  Google Scholar 

  80. Salcher, M.M., Same but different: ecological niche partitioning of planktonic freshwater prokaryotes, J. Limnol., 2014, vol. 73, no. 1, pp. 74–87.

    Google Scholar 

  81. Salcher, M.M., Pernthaler, J., and Posch, T., Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake, Limnol. Oceanogr., 2010, vol. 55, no. 2, pp. 846–856.

    Article  CAS  Google Scholar 

  82. Salcher, M.M., Neuenschwander, S.M., Posch, T., and Pernthaler, J., The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign, ISME J., 2015, vol. 9, no. 11, pp. 2442–2453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Schutte, U.M.E., Cadieux, S.B., Hemmerich, C., Pratt, L.M., and White, J.R., Unanticipated geochemical and microbial community structure under seasonal ice cover in a dilute, dimictic arctic lake, Front. Microbiol., 2016, vol. 7, pp. 1–5.

    Article  Google Scholar 

  84. Sharma, A.K., Zhaxybayeva, O., Papke, R.T., and Doolittle, W.F., Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments, Environ. Microbiol., 2008, vol. 10, no. 4, pp. 1039–1056.

    Article  CAS  PubMed  Google Scholar 

  85. Sharma, A.K., Sommerfeld, K., Bullerjahn, G.S., Matteson, A.R., Wilhelm, S.W., Jezbera, J., Brandt, U., Doolittle, W.F., and Hahn, M.W., Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria, ISME J., 2009, vol. 3, no. 6, pp. 726–737.

    Article  CAS  PubMed  Google Scholar 

  86. Shaw, A.K., Halpern, A.L., Beeson, K., Tran, B., Venter, J.C., and Martiny, J.B.H., It’s all relative: ranking the diversity of aquatic bacterial communities, Environ. Microbiol., 2008, vol. 10, no. 9, pp. 2200–2210.

    Article  PubMed  Google Scholar 

  87. Šimek, K., Kasalický, V., Jezbera, J., Horňák, K., Nedoma, J., Hahn, M.W., Bass, D., Jost, S., and Boenigk, J., Differential freshwater flagellate community response to bacterial food quality with a focus on Limnohabitans bacteria, ISME J., 2013, vol. 7, no. 8, pp. 1519–1530.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Šimek, K., Nedoma, J., Znachor, P., Kasalicky, V., Jezbera, J., Hornak, K., and Sed’a, J., A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring, Limnol. Oceanogr., 2014, vol. 59, no. 5, pp. 1477–1492.

    Article  CAS  Google Scholar 

  89. Sjostedt, J., Koch-Schmidt, P., Pontarp, M., Canback, B., Tunlid, A., Lundberg, P., Hagstrom, A., and Riemann, L., Recruitment of members from the rare biosphere of marine bacterioplankton communities after an environmental disturbance, Appl. Environ. Microbiol., 2012, vol. 78, no. 5, pp. 1361–1369.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Song, Y., Wang, Y., Mao, G., Gao, G., and Wang, Y., Impact of planktonic low nucleic acid-content bacteria to bacterial community structure and associated ecological functions in a shallow lake, Sci. Total. Environ., 2019, vol. 658, pp. 868–878.

    Article  CAS  PubMed  Google Scholar 

  91. Stocker, R., Marine microbes see a sea of gradients, Science, 2012, vol. 338, pp. 628–633.

    Article  CAS  PubMed  Google Scholar 

  92. Taipale, S., Jones, R.I., and Tiirola, M., Vertical diversity of bacteria in an oxygen-stratified humic lake, evaluated using DNA and phospholipid analyses, Aquat. Microb. Ecol., 2009, vol. 55, pp. 1–16.

    Article  Google Scholar 

  93. Tarao, M., Jezbera, J., and Hahn, M.W., Involvement of cell surface structures in size-independent grazing resistance of freshwater Actinobacteria, Appl. Environ. Microbiol., 2009, vol. 75, no. 14, pp. 4720–4726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Terkina, I.A., Drukker, V.V., Parfenova, V.V., and Kostornova, T.Ya., The biodiversity of actinomycetes in Lake Baikal, Microbiology (Moscow), 2002, vol. 71, no. 3, pp. 346–349.

    Article  CAS  Google Scholar 

  95. Urbach, E., Vergin, K.L., Young, L., and Morse, A., Unusual bacterioplankton community structure in ultra-oligotrophic Crater Lake, Limnol. Oceanogr., 2001, vol. 46, no. 3, pp. 557–572.

    Article  CAS  Google Scholar 

  96. van den Wyngaert, S., Salcher, M.M., Pernthaler, J., Zeder, M., and Posch, T., Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake, Limnol. Oceanogr., 2011, vol. 56, no. 1, pp. 97–109.

    Article  Google Scholar 

  97. van der Gucht, K., Vandekerckhove, T., Vloemans, N., Cousin, S., Muylaert, K., Sabbe, K., Gillis, M., Declerk, S., De Meester, L., and Vyverman, W., Characterization of bacterial communities in four freshwater lakes differing in nutrient load and food web structure, FEMS Microbiol. Ecol., 2005, vol. 53, no. 2, pp. 205–220.

    Article  CAS  PubMed  Google Scholar 

  98. Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G.F., Chater, K.F., and van Sinderen, D., Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum, Microbiol. Mol. Biol. Rev., 2007, vol. 71, no. 3, pp. 495–548.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Warnecke, F., Amann, R., and Pernthaler, J., Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages, Environ. Microbiol., 2004, vol. 6, no. 3, pp. 242–253.

    Article  CAS  PubMed  Google Scholar 

  100. Warnecke, F., Sommaruga, R., Sekar, R., Hofer, J.S., and Pernthaler, J., Abundances, identity, and growth state of Actinobacteria in mountain lakes of different UV transparency, Appl. Environ. Microbiol., 2005, vol. 71, no. 9, pp. 5551–5555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Wu, Q.L., Zwart, G., Wu, J., Kamst-van Agterveld, M.P., Liu, S., and Hahn, M.W., Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China, Environ. Microbiol., 2007, vol. 9, no. 11, pp. 2765–2774.

    Article  CAS  PubMed  Google Scholar 

  102. Yang, T., Lyons, S., Aguilar, C., Cuhel, R., and Teske, A., Microbial communities and chemosynthesis in Yellowstone Lake sublacustrine hydrothermal vent waters, Front. Microbiol., 2011, vol. 2, pp. 1–17.

    Article  CAS  Google Scholar 

  103. Zhang, R., Wu, Q., Piceno, Y.M., Desantis, T.Z., Saunders, F.M., Andersen, G.L., and Liu, W.T., Diversity of bacterioplankton in contrasting Tibetan lakes revealed by high-density microarray and clone library analysis, FEMS Microbiol. Ecol., 2013, vol. 86, no. 2, pp. 277–287.

    Article  CAS  PubMed  Google Scholar 

  104. Zeng, J., Bian, Y., Xing, P., and Wu, Q.L., Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake, Appl. Environ. Microbiol., 2012, vol. 78, no. 1, pp. 177–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zeng, J., Deng, L.J., Lou, K., Zhang, T., Yang, H.M., Shi, Y.W., and Lin, Q., Molecular characterization of the planktonic microorganisms in water of two mountain brackish lakes, J. Basic Microbiol., 2014, vol. 54, no. 6, pp. 509–520.

    Article  CAS  PubMed  Google Scholar 

  106. Zwart, G., Crump, B.C., Agterveld, M.P., Hagen, F., and Han, S.K., Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers, Aquat. Microb. Ecol., 2002, vol. 28, pp. 141–155.

    Article  Google Scholar 

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Funding

This work was supported by project no. 0345-2016-0003 (AAAA-A16-116122110061-6).

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  1. Limnological Institute, Siberian Branch, Russian Academy of Sciences, 664033, Irkutsk, Russia

    I. A. Lipko & O. I. Belykh

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Lipko, I.A., Belykh, O.I. Environmental Features of Freshwater Planktonic Actinobacteria . Contemp. Probl. Ecol. 14, 158–170 (2021). https://doi.org/10.1134/S1995425521020074

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