Skip to main content
Log in

Structure of Microbial Mats in the Mramornaya Bay (Crimea) Coastal Areas

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The structure of microbial mats from the Mramornaya Bay (Crimea) was investigated. Light microscopy in combination with transmission and scanning electron microscopy revealed the base of bacterial mats to be interwoven thin filaments (100 to 500 nm in diameter) consisting mainly of sulfur. Numerous bean-shaped single microbial cells (~1.6 × 0.7 µm), some of which were attached to sulfur filaments, were also revealed. High-throughput sequencing of the 16S rRNA genes revealed predominance of bacteria of the genera Arcobacter (27%), Alcaligenes (17%), and Desulfuromonas (8.5%) as well as of uncultured members of the family Lachnospiraceae (4.9%). No clearly predominant microbial taxa were revealed in the detritus sample below the mats. Similar to the bacterial mat, bacteria of the genera Arcobacter and Desulfuromonas were predominant in the detritus, but their relative abundance was significantly lower (4.1 and 6%, respectively). Analysis of the 16S rRNA gene sequences specific for the genus Arcobacter revealed considerable phylogenetic diversity of this group in the samples from both the upper bacterial mats and the detritus sediment. Most of obtained sequences formed common clusters with the sequences of various uncultured members of the genus Arcobacter, while an insignificant share of them was related to the recently described sulfide-oxidizing bacterium “Candidatus Arcobacter sulfidicus.” Thus, members of the phylogenetically heterogeneous group of epsilonproteobacteria of the genus Arcobacter were the dominant component of the Mramornaya Bay microbial communities.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

REFERENCES

  1. Akagawa, M. and Yamasato, K., Synonymy of Alcaligenes aquamarinus, Alcaligenes faecalis subsp. homari, and Deleya aesta: Deleya aquamarina comb. nov. as the type species of the genus Deleya, Int. J. Syst. Evol. Microbiol., 1989, vol. 39, pp. 462–466.

    Google Scholar 

  2. Anisimova, M. and Gascuel, O., Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative, Syst. Biol., 2006, vol. 55, pp. 539–552.

    Article  PubMed  Google Scholar 

  3. Bienhold, C., Zinger, L., Boetius, A., and Ramette, A., Diversity and biogeography of bathyal and abyssal seafloor bacteria, PLoS One, 2016, vol. 11, no. 1, pp. e0148016.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Bowman, J.P., McCammon, S.A., and Dann, A.L., Biogeographic and quantitative analyses of abundant uncultivated gamma-proteobacterial clades from marine sediment, Microb. Ecol., 2005, vol. 49, pp. 451–460.

    Article  PubMed  CAS  Google Scholar 

  5. Bryukhanov, A.L., Vlasova, M.A., Malakhova, T.V., Perevalova, A.A., and Pimenov, N.V., Phylogenetic diversity of the sulfur cycle bacteria in the bottom sediments of the Chersonesus Bay, Microbiology (Moscow), vol. 87, no. 3, pp. 372–381.

  6. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., et al., QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 2010, vol. 7, pp. 335–336.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Chao, A., Nonparametric estimation of the number of classes in a population, Scand. J. Statistics, 1984, vol. 11, pp. 265–270.

    Google Scholar 

  8. Dyksma, S., Bischof, K., Fuchs, B.M., Hoffmann, K., Meier, D., Meyerdierks, A., Pjevac, P., Probandt, D., Richter, M., Stepanauskas, R., and Mußmann, M., Ubiquitous gammaproteobacteria dominate dark carbon fixation in coastal sediments, ISME J., 2016, vol. 10, pp. 1939–1953.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST, Bioinformatics, 2010, vol. 26, pp. 2460–2461.

    Article  PubMed  CAS  Google Scholar 

  10. Egorov, V.N., Pimenov, N.V., Malakhova, T.V., Kanapatskii, T.A., Artemov, Yu.G., and Malakhova, L.V., Biogeochemical characteristics of methane distribution in the water and bottom sediments at gas seep jets in the Sevastopol Bay area, Morsk. Ekol. Zh., 2012, vol. 11, no. 3, pp. 41–52.

    Google Scholar 

  11. Fadrosh, D.W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R.M., and Ravel, J., An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform, Microbiome, 2014, vol. 2, no. 1, pp. 6.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Fossing, H., Gallardo, V.A., Jørgensen, B.B., Hüttel, M., Nielsen, L.P., Schulz, H., Canfield, D.E., Forster, S., Glud, R.N., Gundersen, J.K., Küver, J., Ramsing, N.B., Teske, A., Thamdrup, B., and Ulloa, O., Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca, Nature, 2002, vol. 374, pp. 713–715.

    Article  Google Scholar 

  13. Ghai, R., Mizuno, C.M., Picazo, A., Camacho, A., and Rodriguez-Valera, F., Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria, Sci. Rep., 2013, vol. 3, pp. 2471.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Grünke, S., Felden, J., Lichtschlag, A., Girnth, A.-C., De Beer, D., Wenzhofer, F., and Boetius, A., Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea), Geobiology, 2011, vol. 9, pp. 330–348.

    Article  PubMed  CAS  Google Scholar 

  15. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O., New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0, Syst. Biol., 2010, vol. 59, pp. 307–321.

    Article  PubMed  CAS  Google Scholar 

  16. Ivanov, M.V. and Lein, A.Yu., Fractionation of stable isotopes of carbon and sulfur during biological processes in the Black Sea, in Past and Present Water Column Anoxia, Neretin, L.N., Ed., Berlin: Springer, 2006, pp. 373–417.

    Google Scholar 

  17. Ivanov, V.E., Lomakin, I.E., Topolyuk, A.S., Efremtseva, L.L., and Boldyrev S.N., Patterns of tectonics of the Southwestern Crimea, Geol. Polez. Isko., Mir. Okeana, 2009, no. 4, pp. 27–39.

  18. Jessen, G.L., Lichtschlag, A., Struck, U., and Boetius, A., Distribution and composition of thiotrophic mats in the hypoxic zone of the Black Sea (150–170 m water depth, Crimea margin), Front. Microbiol., 2016, vol. 7, pp. 1011–1024.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Jørgensen B.B., Mineralization of organic matter in the sea bed–the role of sulfate reduction, Nature, 1982, vol. 296, pp. 643–645.

    Article  Google Scholar 

  20. Jørgensen, B.B., Fossing, H., Wirsen, C.O., and Jannasch, H.W., Sulfide oxidation in the anoxic Black Sea chemocline, Deep-Sea Res., 1991, vol. 38, pp. 1083S–1103S.

    Article  Google Scholar 

  21. Kuever, J., Rainey, F.A., and Widdel, F., Desulfuromonas, in Bergey’s Manual of Systematics of Archaea and Bacteria, Wiley, 2015, pp. 1–7.

    Google Scholar 

  22. Lein, A., Pimenov, N., Guillou, C., Martin, J.-M., Lancelot, C., Rusanov, I., Yusupov, S., Miller, Yu., and Ivanov, M., Seasonal dynamics of the sulphate reduction rate on the north-western Black Sea shelf, Estuarine Coastal Shelf Sci., 2002, vol. 54, pp. 385–401.

    Article  CAS  Google Scholar 

  23. Lein, A.Yu., Egorov, V.N., Pimenov, N.V., Gulin, M.B., Lyut, K., Lyut, U., Artemov, Yu.G., Polikarpov, G.G., Til’, Kh, and Ivanov, M.V., Sulfide structures from the Black Sea bottom, Doklady Akad. Nauk, 1995, vol. 340, no. 5, pp. 676–680.

    CAS  Google Scholar 

  24. Lever, M.A., Torti, A., Eickenbusch, P., Michaud, A.B., Šantl-Temkiv, T., and Jørgensen, B.B., A modular method for the extraction of DNA and RNA, and the separation of DNA pools from diverse environmental sample types, Front. Microbiol., 2015, vol. 6, p. 476.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Lloyd, K.G., Albert, D.B., Biddle, J.F., Chanton, J.P., Pizarro, O., and Teske, A., Spatial structure and activity of sedimentary microbial communities underlying a Beggiatoa spp. mat in a Gulf of Mexico hydrocarbon seep, PLoS One, 2010, vol. 5, no. 1, pp. e8738. doi 10.1371/journal.pone.0008738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Malakhova, T.V., Egorov, V.N., Malakhova, L.V., Artemov, Y.G., Evtushenko, D.B., Gulin, S.B., Kanapatskii, T.A., and Pimenov, N.V., Microbial processes and genesis of methane gas jets in the coastal areas of the Crimean Peninsula, Microbiology (Moscow), 2015, vol. 84, no.6, pp. 838–845.

    Article  CAS  Google Scholar 

  27. McKay, L.J., MacGregor, B.J., Biddle, J.F., Albert, D.B., Mendlovitz, H.P., Hoer, D.R., Lipp, J.S., Lloyd, K.G., and Teske, A.P., Spatial heterogeneity and underlying geochemistry of phylogenetically diverse orange and white Beggiatoa mats in Guaymas Basin hydrothermal sediments, Deep Sea Res., 2012, vol. 67, pp. 21–31.

    Article  CAS  Google Scholar 

  28. Merkel, A.Y., Pimenov, N.V., Rusanov, I.I., Slobodkin, A.I., Slobodkina, G.B., Tarnovetckii, I.Y., Frolov, E.N., Dubin, A.V., Perevalova, A.A., and Bonch-Osmolovskaya, E.A., Microbial diversity and autotrophic activity in Kamchatka hot springs, Extremophiles, 2017, vol. 21, pp. 307–317.

    Article  PubMed  CAS  Google Scholar 

  29. Michaelis, W., Seifert, R., and Nauhaus, K., Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane, Science, 2002, vol. 297, pp. 1013–1015.

    Article  PubMed  CAS  Google Scholar 

  30. Mußmann, M., Pjevac, P., Krüger, K., and Dyksma, S., Genomic repertoire of the Woeseiaceae/JTB255, cosmopolitan and abundant core members of microbial communities in marine sediments, ISME J., 2017, vol. 11, pp. 1276–1281.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Niemann, H., Lösekann, T., Beer, D.D., Elvert, M., Nadalig, T., Knittel, K., Amann, R., Sauter, E.J., Schlüter, M., Klages, M., Foucher, J.P., and Boetius, A., Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink, Nature, 2006, vol. 443, pp. 854–858.

    Article  PubMed  CAS  Google Scholar 

  32. Omoregie, E.A., Mastalerz, V., de Lange, G., Straub, K.L., Kappler, A., Røy, H., Stadnitskaia, A., Foucher, J.-P., and Boetius, A., Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren Mud Volcano (Nile Deep Sea Fan, Eastern Mediterranean), Appl. Environ. Microbiol., 2008, vol. 74, pp. 3198–3215.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Pimenov, N.V., Rusanov, I.I., Poglazova, M.N., Mityushina, L.L., Sorokin, D.Yu., Khmelenina, V.N., and Trotsenko, Yu.A., Bacterial mats on coral-like structures at methane seeps in the Black Sea, Microbiology (Moscow), 1997, vol. 66, no. 3, pp. 354–360.

    CAS  Google Scholar 

  34. Pimenov, N.V., Savvichev, A.S., Rusanov, I.I., Ivanov, M.V., and Lein, A.Yu., Microbiological processes of the carbon and sulfur cycles at cold methane seeps of the North Atlantic, Microbiology (Moscow), 2000, vol. 69, no. 6, pp. 709–720.

    Article  CAS  Google Scholar 

  35. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res., 2013. Database issue, pp. D590–D596.

  36. Reeburgh, W.S., Bess, B.W., Whalen, S.C., Sandbeck, K.A., and Kilpatrick, K.A., Black Sea methane geochemistry, Deep-Sea Res., 1991, vol. 38, pp. S1189–S1210.

    Article  Google Scholar 

  37. Roalkvam, I., Jørgensen, S.L., Chen, Y., Stokke, R., Dahle, H., Hocking, W.P., Lanzén, A., Haflidason, H., and Steen, I.H., New insight into stratification of anaerobic methanotrophs in cold seep sediments, FEMS Microbiol. Ecol., 2011, vol. 78, pp. 233–243.

    Article  PubMed  CAS  Google Scholar 

  38. Savvichev, A.S., Kadnikov, V.V., Kravchishina, M.D., Galkin, S.A., Novigatskii, A.N, Sigalevich, P.A., Merkel, A.Yu., Ravin, N.V., Pimenov, N.V., and Flint, M.V., Methane as an organic matter source and the trophic basis of a Laptev Sea cold seep microbial community, Geomicrobiol. J., 2018, vol. 35, no. 5, pp. 411–423.

    Article  Google Scholar 

  39. Schloss, P.D. and Handelsman, J., Toward a census of bacteria in soil, PLoS Comput. Biol., 2006, vol. 2, p. e92.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Schulz, H.N., Brinkhoff, T., Ferdelman, T.G., Mariné, M.H., Teske, A., and Jorgensen, B.B., Dense populations of a giant sulfur bacterium in Namibian shelf sediments, Science, 1999, vol. 284, pp. 493–495.

    Article  PubMed  CAS  Google Scholar 

  41. Sievert, S.M., Wieringa, E.B.A., Wirsen, C.O., and Taylor, C.D., Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients, Environ. Microbiol., 2007, vol. 9, pp. 271–276.

    Article  PubMed  CAS  Google Scholar 

  42. Sorokin, Yu.I., The Black Sea, in Ecosystems of the World: Estuaries and Enclosed Seas, Ketchum, B.H., Ed., Amsterdam: Elsevier, 1983, pp. 253–292.

    Google Scholar 

  43. Taylor, C.D., Wirsen, C.O., and Gaill, F., Rapid microbial production of filamentous sulfur mats at hydrothermal vents, Appl. Environ. Microbiol. 1999, vol. 65, pp. 2253–2255.

    PubMed  PubMed Central  CAS  Google Scholar 

  44. Treude, T., Orphan, V., Knittel, K., Gieseke, A., House, C.H., and Boetius, A., Consumption of methane and CO2 by Methanotrophic microbial mats from gas seeps of the anoxic Black Sea, Appl. Environ. Microbiol., 2007, vol. 73, pp. 2271–2283.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Wirsen, C.O., Sievert, S.M., Cavanaugh, C.M., Molyneaux, S.J., Ahmad, A., Taylor, L.T., DeLong, E.F., and Taylor, C.D., Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur, Appl. Environ. Microbiol., 2002, vol. 68, pp. 316–325.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The work was supported by the Russian Foundation for Basic Research, project no. 17-04-00023, and Government Assignment no. 0104-2018-0030; the analysis of high-throughput sequencing data was supported by the Russian Science Foundation, Grant no. 17-74-30025.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. V. Pimenov.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pimenov, N.V., Merkel, A.Y., Tarnovetskii, I.Y. et al. Structure of Microbial Mats in the Mramornaya Bay (Crimea) Coastal Areas. Microbiology 87, 681–691 (2018). https://doi.org/10.1134/S0026261718050132

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261718050132

Keywords:

Navigation