Abstract
Since the beginning of the last century, bacteria, including cyanobacteria, have been known to be involved in the extracellular formation and precipitation of CaCO3. It is also known that some marine bacteria form calcite granules in Ca-containing artificial media. However, a detailed analysis of these granules has not yet been performed. The objective of the present study was to isolate marine bacteria that form CaCO3 granules in a culture medium to analyze the structure of the granules in detail. Pseudovibrio sp. 01OK 105-5-5, belonging to the class Alphaproteobacteria, was isolated from an ascidian in a coral reef at On-na, Okinawa, Japan. It produced extracellular granules of CaCO3 in a Ca-containing artificial medium. X-ray diffraction analysis, infrared spectroscopy, and inductively coupled plasma atomic emission spectrometry demonstrated that the extracellular granules contained Mg-rich calcite-like crystal polymorphs. This crystal form of CaCO3 was similar to that of Mg-rich calcite found in the skeletons of many marine invertebrates. This bacterium provides a promising tool for studying the mechanisms involved in the formation of Mg-rich biogenic calcite.
Similar content being viewed by others
References
Aizenberg J, Lambert G, Weiner S, Addadi L (2002) Factors involved in the formation of amorphous and crystalline calcium carbonate: a study of an ascidian skeleton. J Am Chem Soc 124:32–39
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Boquet E, Boronat A, Ramos-Cormenzana A (1973) Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246:527–529
Buck JD, Greenfield LJ (1964) Calcification in marine-occurring yeasts. Bull Mar Sci Gulf Carib 14:239–245
Drew GH (1913) On the precipitation of calcium carbonate in the sea by marine bacteria, and on the action of denitrifying bacteria in tropical and temperate seas. J Mar Biol Ass 9:479–524
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ferrer MR, Quevedo-Sarmiento J, Rivadeneyra MA, Bejar V, Delgado R, Ramos-Cormenzana A (1988) Calcium carbonate precipitation by two groups of moderately halophilic microorganisms at different temperatures and salt concentrations. Curr Microbiol 17:221–227
Fujita Y, Ferris FG, Lawson RD, Colwell FS, Smith RW (2000) Calcium carbonate precipitation by ueolytic subsurface bacteria. Geomicrobiol J 17:305–318
Hiraishi A (1992) Direct automated sequencing of 16S rDNA amplified by polymerase chain reaction from bacterial cultures without DNA purification. Lett Appl Microbiol 15:210–213
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kitano Y, Hood DW (1962) Calcium carbonate crystal forms formed from seawater by inorganic processes. J Oceanogr Soc Jpn 18:141–145
Kogure K, Ikemoto E, Morisaki H (1998) Attachment of Vibrio alginolyticus to glass surfaces is dependent on swimming speed. J Bacteriol 180:932–937
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Kumar JPJ, Babu BR, Nandhagopal G, Ragumaran S, Ramakritinan CM, Ravichandran V (2019) In vitro synthesis of bio-brick using locally isolated marine ureolytic bacteria, a comparison with natural calcareous rock. Ecol Eng 138:97–105
Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, New York
McCallum MF, Guhathakurta K (1970) The precipitation of calcium carbonate from seawater by bacteria isolated from Bahama Bank sediments. J Appl Bacteriol 33:649–655
Morita RY (1980) Calcite precipitation by marine bacteria∗. Geomicrobiol J 2:63–82
Nishino T, Ikemoto E, Kogure K (2004) Application of atomic force microscopy to observation of marine bacteria. J Oceanogr 60:219–225
Novitsky JA (1981) Calcium carbonate precipitation by marine bacteria. Geomicrobiol J 2:375–388
Oomori T, Tokuyama A, Oode S (1988) The coral reefs of Okinawa. In: Nishihira M (ed) The coral reefs of Okinawa. Okinawa Prefecture Environment Science Center, Okinawa, pp 51–65 ((in Japanese))
Paerl HW, Steppe TF, Reid RP (2001) Bacterially mediated precipitation in marine stromatolites. Environ Microbiol 3:123–130
Pan J, Zhao H, Tucker ME, Zhou J, Jiang M, Wang Y, Zhao Y, Sun B, Han Z, Yan H (2019) Biomineralization of monohydrocalcite induced by the halophile Halomonas smyrnensis WMS-3. Minerals 9:632
Rautaray D, Ahmad A, Sastry M (2003) Biosynthesis of CaCO3 crystals of complex morphology using a fungus and an actinomycete. J Am Chem Soc 125:14656–14657
Rivadeneyra MA, Delgado R, Delgado G, Moral AD, Ferrer MR, Ramos-Cormenzana A (1993) Precipitation of carbonates by Bacillus sp. isolated from saline soils. Geomicrobiol J 11:175–184
Rivadeneyra MA, Delgado R, Moral A, Ferrer MR, Ramos-Cormenzana A (1994) Precipatation of calcium carbonate by Vibrio spp. from an inland saltern. FEMS Microbiol Ecol 13:197–204
Rodriguez-Navarro C, Rodriguez-Gallego M, Ben Chekroun KB, Gonzalez-Muñoz MT (2003) Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Appl Environ Microbiol 69:2182–2193
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shieh WY, Lin YT, Jean WD (2004) Pseudovibrio denitrificans gen. nov., sp. nov., a marine, facultatively anaerobic, fermentative bacterium capable of denitrification. Int J Syst Evol Microbiol 54:2307–2312
Shinano H (1972a) Studies of marine microorganisms taking part in the precipitation of calcium carbonate-III. Nippon Suisan Gakkaishi 38:717–725
Shinano H (1972b) Studies of marine microorganisms taking part in the precipitation of calcium carbonate-IV. Nippon Suisan Gakkaishi 38:825–832
Shinano H (1972c) Studies of marine microorganisms taking part in the precipitation of calcium carbonate-V. Nippon Suisan Gakkaishi 38:833–838
Stocks-Fischer S, Galinat JK, Bang SS (1999) Microbiological precipitation of CaCO3. Soil Biol Biochem 31:1563–1571
Thornton DCO, Fejes EM, DiMarco SF, Clancy KM (2007) Measurement of acid polysaccharides in marine and freshwater samples using alcian blue. Limnol Oceanogr Method 5:73–87
Vincent J, Colin B, Lanneluc I, Sabot R, Sopéna V, Turcry P, Mahieux PY, Refait P, Jeannin M, Sablé S (2021) New biocalcifying marine bacterial strains isolated from calcareous deposits and immediate surroundings. Microorganisms 10:76
Von Knorre H, Krumbein WE (2000) Bacteria calcification. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer-Verlag, Berlin, pp 23–31
Warren LA, Mauri PA (2001) Microbially mediated calcium carbonate precipitation: implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol J 18:93–115
Webster NS, Hill RT (2001) The culturable microbial community of the great barrier reef sponge rhopaloeides odorabile is dominated by an α-Proteobacterium. Mar Biol 138:843–851
Weinbauer MG, Brandstätter F, Velimirov B (2000) On the potential use of magnesium and strontium concentrations as ecological indicators in the calcite skeleton of the red coral (Corallium rubrum). Mar Biol 137:801–809
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Yasumoto K, Yasumoto-Hirose M, Yasumoto J, Murata R, Sato S, Baba M, Mori-Yasumoto K, Jimbo M, Oshima Y, Kusumi T, Watabe S (2014) Biogenic polyamines capture CO2 and accelerate extracellular bacterial CaCO3 formation. Mar Biotechnol (NY) 16:465–474
Acknowledgements
We thank Ms. Seiko Matsuo for providing assistance with the ICP-AES analysis and Ms. Izumi Yamashima for assistance with identification of bacterial strains. We also thank Mr. Minoru Yasumoto for providing sampling assistance. We are grateful to Prof. Tadashi Maruyama of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) for reviewing the manuscript. This work was supported by The Industrial Science and Technology Project for Technology Development of Biological Resources in Bioconsortia, funded by the New Energy and Industrial Technology Development Organization of Japan; the project “Construction of a Genetic Resource Library of Unidentified Microorganisms,” funded by the Ministry of Economy, Trade and Industry of Japan; a Grant-in-Aid for Creative Basic Research No. 12NP0201 (DOBIS) funded by the Ministry of Education Culture, Sports Science, and Technology (MEXT), Japan; and by Grants-in-Aid from the Japan Society for the Promotion of Science (KAKENHI grant nos. 19K12310).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yasumoto-Hirose, M., Yasumoto, K., Iijima, M. et al. Mg-rich calcite-producing marine bacterium Pseudovibrio sp. isolated from an ascidian in coral reefs at Okinawa, Japan. Fish Sci 88, 625–634 (2022). https://doi.org/10.1007/s12562-022-01627-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-022-01627-9