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Preliminary assessment of methanogenic microbial communities in marine caves of Zakynthos Island (Ionian Sea, Greece)

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PARASKEVI POLYMENAKOU (http://orcid.org/0000-0002-9787-7372), MANOLIS MANDALAKIS, THANOS DAILIANIS, CHARALAMPOS DIMITRIADIS, MATEJ MEDVECKY, ANTONIOS MAGOULAS, VASILIS GEROVASILEIOU
PARASKEVI POLYMENAKOU, MANOLIS MANDALAKIS, THANOS DAILIANIS, CHARALAMPOS DIMITRIADIS, MATEJ MEDVECKY, ANTONIOS MAGOULAS, VASILIS GEROVASILEIOU

Abstract


Mediterranean marine caves remain largely unexplored, while particularly limited information is available about the microbial life existing in these unique environments. The present study is a preliminary assessment of the composition of the active anaerobic microbial community colonizing the walls of newly explored systems of underwater caves and small cavities in Zakynthos Island. The interior of these caves is densely coated with egg-shaped, foam-shaped and filamentous biological structures that are characterised by a strong odor of hydrogen sulfide gas. A total of twelve structures scrapped from cave rocks were subjected to anaerobic cultivation for up to 208 days. Strong to moderate methanogenesis was observed in two different types of egg-shaped structures and one foam-like structure. Interestingly, this was observed in experiments that were performed at room temperature (i.e. 25oC) which is substantially lower than those typically considered optimum for methane production (e.g. 35oC). Analysis of the 16S rRNA genes revealed a clear dominance of archaea and bacteria closely related to known methane producers and sulfate reducers, including members of the families Methanomicrobiaceae, Desulfobulbaceae, Desulfobacteraceae, Desulfuromonaceae, Campylobacteraceae, Marinifilaceae, Clostridiaceae, Incertae Sedis – Family I & II. These results show that Mediterranean marine caves can host members of archaea and bacteria with potential biotechnological interest that deserve further investigation.


Keywords


16S rRNA gene analysis, Anaerobic cultures, Mediterranean marine caves, Methanogens, Sulfate reducers

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Barton, L.L., Fauque, G.D., 2009. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Advances in Applied Microbiology, 68, 41-98.

Canganella, F., Bianconi, G., Gambacorta, A., Kato, C., Uematsu, K., 2002. Characterisation of Heterotrophic Microorganisms Isolated form the “Grotta Azzura” of Cape Palinuro (Salerno, Italy). Marine Ecology, 23, 1-10.

Canganella, F., Bianconi, G., Kato, C., Gonzalez, J., 2007. Microbial ecology of submerged marine caves and holes characterised by high levels of hydrogen sulphide. Reviews in Environmental science and Biotechnology, 6, 61-70.

Dianou, D., Miyaki, T., Asakawa, S., Morii, H., Nagaoka, K. et al., 2001. Methanoculleus chikugoensis sp. nov., a novel methanogenic archaeon isolated from paddy field soil in Japan, and DNA-DNA hybridization among Methanoculleus species. International Journal of Systematic and Evolutionary Microbiology, 51, 1663-1669.

Engel, A.S., 2010. Microbial diversity of cave ecosystems. p. 219-238. In Geomicrobiology: Molecular and Environmental Perspective. Barton, L.L. et al. (Eds.), Springer Science+Business Media B.V.

Friedrich, M., Springer, N., Ludwig, W., Schink, B., 1996. Phylogenetic positions of Desulfofustis glycolicus gen. nov., sp. nov., and Syntrophobotulus glycolicus gen. nov., sp. nov., two new strict anaerobes growing with glycolic acid. International Journal of Systematic and Evolutionary Microbiology, 46, 1065-1069.

Gerovasileiou, V., Voultsiadou, E., 2012. Marine caves of the Mediterranean Sea: a sponge biodiversity reservoir within a biodiversity hotspot. Plos One, 7, e39873. doi: 10.1371/journal.pone.0039873

Gerovasileiou, V., Voultsiadou, E., 2014. Mediterranean marine caves as biodiversity reservoirs: a preliminary overview. p. 45-50. In: Proceedings of the 1st Mediterranean Symposium on the conservation of Dark Habitats (Portorož, Slovenia, 31 October 2014). Bouafif, C., Langar, H., Ouerghi, A. (Eds). RAC/SPA, Tunis.

Gerovasileiou, V., Chintiroglou, C., Vafidis, D., Koutsoubas, D., Sini, M. et al., 2015. Census of biodiversity in marine caves of the Eastern Mediterranean Sea. Mediterranean Marine Science, 16, 245-265.

Gerovasileiou, V., Martínez, A., Álvarez, F., Boxshall, G., Humphreys, W. et al., 2016. World Register of marine Cave Species (WoRCS): a new Thematic Species Database for marine and anchialine cave biodiversity. Research Ideas and Outcomes, 2, e10451. doi: 10.3897/rio.2.e10451

Guido, A., Mastandrea, A., Rosso, A., Sanfilippo, R., Russo, F., 2012. Micrite precipitation induced by sulphate reducing bacteria in serpulid bioconstructions from submarine caves (Syracuse, Sicily). Rendiconti Online della Societa Geologica Italiana, 21, 933-934.

Guido, A., Heindel, K., Birgel, D., Rosso, A., Mastandrea, A. et al., 2013. Pendant bioconstructions cemented by microbial carbonate in submerged marine caves (Holocene, SE Sicily). Palaeogeography, Palaeoclimatology, Palaeoecology, 388, 166-180.

Guido, A., Mastandrea, A., Rosso, A., Sanfilippo, R., Tosti, F. et al., 2014. Commensal symbiosis between agglutinated polychaetes and sulfate reducing bacteria. Geobiology, 12, 265-275.

Guido, A., Rosso, A., Sanfilippo, R., Russo, F., Mastrandrea, A., 2016. Submarine caves: a laboratory for geomicrobiology studies. Rendiconti Online della Societa Geologica Italiana, 38, 62-64.

Guido, A., Jimenez, C., Achilleos, K., Rosso, A., Sanfilippo, R. et al., 2017. Cryptic serpulid-microbialite bioconstructions in the Kakoskali submarine cave (Cyprus, Eastern Mediterranean). Facies, 63, 21.

Heyer, J., 1990. Der Kreislauf des Methans. Akademie-Verlag Berlin, 250 pp.

Hussain, A., Hasan, A., Javid, A., Iqbal Qazi, J., 2016. Exploited application of sulfate-reducing bacteria for concomitant treatment of metallic and non-metallic wastes: a mini review. 3 Biotech, 6, 119.

Jaenicke, S., Ander, C., Bekel, T., Bisdorf, R., Dröge, M. et al., 2011. Comparative and joint analysis of two metagenomic datasets from a biogas fermenter obtained by 454-pyrosequencing. Plos One, 6, e14519. doi: 10.1371/journal.pone.0014519

Lane, D.J., 1991. 16S/23S rRNA sequencing. p. 115–175. In: Nucleic acid techniques in bacterial systematics. Stackebrandt, E., Goodfellow, M. (Eds). Wiley, New York.

Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A. et al., 2007. Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947-2948.

Letunic, I., Bork, P., 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research, 44, W242-245.

Liesack, W., Finster, K., 1994. Phylogenetic analysis of five strains of gram-negative, obligately anaerobic, sulfur-reducing bacteria and description of Desulfuromusa gen. nov., including Desulfuromusa kysingii sp. nov., Desulfuromusa bakii sp. nov., and Desulfuromusa succinoxidans sp. nov. International Journal of Systematic Bacteriology, 44, 753-758.

Maestrojuan, G.M., Boone, D.R., Xun, L., Mah, R.A., Zhang, L., 1990. Transfer of Methanogenium bourgense, Methanogenium marisnigri, Methanogenium olentangyi, and Methanogenium thermophilicum to the genus Methanoculleus gen. nov., emendation of Methanoculleus marisnigri and Methanogenium, and description of new strains of Methanoculleus bourgense and Methanoculleus marisnigri. International Journal of Systematic Bacteriology, 40, 117-122.

Mattison, R., Abbiati, M., Dando, P., Fitzsimons, M.F., Pratt, S.M. et al., 1998. Chemoautotrophic microbial mats in submarine caves with hydrothermal sulphidic springs at Cape Palinuro, Italy. Microbial Ecology, 35, 58-71.

Maugeri, T.L., Bianconi, G., Canganella, F., Danovaro, R., Gugliandolo, C. et al., 2010. Shallow hydrothermal vents in the southern Tyrrhenian Sea. Chemistry and Ecology, 26, 285-298.

Maus, I., Wibberg, D., Stantscheff, R., Eikmeyer, F.-G., Seffner, A. et al., 2012. Complete genome sequence of the hydrogenotrophic, methanogenic archaeon Methanoculleus bourgensis strain MS2T, isolated from a sewage sludge digester. Journal of Bacteriology, 194, 5487-5488.

Oren, A., 2014. The family Methanomicrobiaceae. p. 165-193. In: The Prokaryotes – Other Major Lineages of Bacteria and the Archaea. Rosenberg, E, DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (Eds), Springer-Verlag Berlin Heidelberg.

Polymenakou, P.N., Bertilsson, S., Tselepides, A., Stephanou, E.G., 2005. Bacterial community composition in different sediments from the Eastern Mediterranean Sea: a comparison of four 16S ribosomal DNA clone libraries. Microbial Ecology, 50, 447-462.

Romesser, J.A., Wolfe, R.S., Mayer, F., Spiess, E., Walther-Mauruschat, A., 1979. Methanogenium, a new genus of marine methanogenic bacteria, and characterization of Methanogenium cariaci sp. nov. Archives of Microbiology, 121, 147-153.

Ronquist, F., Huelsenbeck, J.P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.

Sánchez, E., Borja, R., Weiland, P., Travieso, L., Martin, A., 2000. Effect of temperature and pH on the kinetics of methane production, organic nitrogen and phosphorus removal in the batch anaerobic digestion process of cattle manure. Bioprocess Engineering, 22, 247-252.

Sanfilippo, R., Rosso, A., Guido, A., Mastrandrea, A., Russo, F. et al., 2015. Metazoan/microbial biostalactites from present-day submarine caves in the Mediterranean Sea. Marine Ecology, 36, 1277-1293.

Sanfilippo, R., Rosso, A., Guido, A., Gerovasileiou, V., 2017. Serpulid communities from two marine caves in the Aegean Sea, eastern Mediterranean. Journal of the Marine Biological Association of the United Kingdom, 97, 1059-1068.

Southward A.J., Kennicutt M.C., Alcalà-Herrera J., Abbiati M., Airoldi L. et al., 1996. On the biology of submarine caves with Sulphur springs: appraisal of 13C/12C ratios as a guide to trophic relations. Journal of the Marine Biological Association of the United Kingdom, 76, 265–285.

Teske, A., Hinrichs, K.-U., Edgcomb, V.P., de Vera Gomez, A., Kysela D. et al., 2002. Microbial diversity in hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Applied and Environmental Microbiology, 68, 1994-2007.

Wolfe, R., 2011. Techniques for cultivating methanogens. Methods in Enzymology, 494, 1-22.


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