Biomineralization Potential of Bacillus subtilis, Rummeliibacillus Stabekisii and Staphylococcus Epidermidis Strains In Vitro Isolated from Speleothems, Khasi Hill Caves, Meghalaya, India

References

• Adetutu EM, Thorpe K, Shahsavari E, Bourne S, Cao X, Fard RMN, Kirby G, Ball AS. 2012. Bacterial community survey of sediments at Naracoorte Caves, Australia. Int J Speleol. 41(2):137–47. doi:10.5038/1827-806X.41.2.2.
   Web of Science ®Google Scholar
• Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lip- man DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res. 25:3389–402. doi:10.1093/nar/25.17.3389. PMID:9254694.
   PubMed Web of Science ®Google Scholar
• APHA. 2005. Standard methods for the examination of water and waste water. 21st ed. Washington, DC: American Public Health Association.
   Google Scholar
• Bajnόcsi B, Kovács-Kis V. 2006. Origin of pedogenic needle-fiber calcite revealed by micromorphology and stable isotope composition— a case study of a quaternary paleosol from Hungary. Chemie der Erde. 66:203–12. doi:10.1016/j.chemer.2005.11.002.
   Web of Science ®Google Scholar
• Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT. 2007. Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology. 5:401–11. doi:10.1111/j.1472-4669.2007.00117.x.
   Web of Science ®Google Scholar
• Barton HA, Taylor NM, Kreate MP, Springer AC, Oehrle SA, Bertog JL. 2007. the impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments. 36:93–104.
   Google Scholar
• Baskar S, Baskar R, Mauclaire L, McKenzie JA. 2005. Role of microbial community in stalactite formation, Sahastradhara caves, Dehradun, India. Curr Sci. 88:1305–8.
   Web of Science ®Google Scholar
• Baskar S, Baskar R, Mauclaire L, McKenzie JA. 2006. Microbially induced calcite precipitation by culture experiments—possible origin for stalactites in Sahastradhara, Dehradun, India. Curr Sci. 90:58–64.
   Web of Science ®Google Scholar
• Baskar S, Baskar R, Thorseth IH, Ovreas L, Pedersen RB. 2012. Microbial iron precipitation associated with a neutrophilic spring of Borra caves, Vishakapatanam, India. Astrobiol J. 12(4):327–46. doi:10.1089/ast.2011.0672.
   PubMed Web of Science ®Google Scholar
• Baskar S, Routh J, Baskar R, Kumar A, Miettinen H, Itävaara M. 2016. Evidences for microbial precipitation of calcite in speleothems from Krem Syndai in Jaintia Hills, Meghalaya, India. Geomicrbiol J. 33(10):906–33. doi:10.1080/01490451.2015.1127447.
   Web of Science ®Google Scholar
• Boquet E, Boronat A, Ramos-Cormenza A. 1973. Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature. 246:527–9. doi:10.1038/246527a0.
   Web of Science ®Google Scholar
• Blyth AJ, Frisia S. 2008. Molecular evidence for bacterial mediation of calcite formation in cold high-altitude caves. Geomicrobiol J. 25:101–11. doi:10.1080/01490450801934938.
   Web of Science ®Google Scholar
• Cacchio P, Ercole C, Cappuccio G, Lepidi A. 2003. Calcium carbonate precipitation by bacterial strains isolated from a limestone cave and from a loamy soil. Geomicrobiol J. 20(2):85–98. doi:10.1080/01490450303883.
   Web of Science ®Google Scholar
• Cacchio P, Contento R, Ercole C, Cappuccio G, Martinez MP, Lepidi A. 2004. Involvement of microorganisms in the formation of carbonate speleothems in the Cervo Cave (L'Aquila-Italy). Geomicrobiol J. 21:497–509. doi:10.1080/01490450490888109.
   Web of Science ®Google Scholar
• Cañaveras JC, Sanchez-Moral S, Soler V, Saiz-Jimenez C. 2001. Microorganisms and microbially induced fabrics in cave walls. Geomicrobiol J. 18:223–40. doi:10.1080/01490450152467769.
   Web of Science ®Google Scholar
• Campbell JW, Watson A, Watson C, Ball H, Pirkle R. 2011. Escherichia coli, other coliform, and environmental chemoheterotrophic bacteria in isolated pools from six caves in northern Alabama and northwestern Georgia. J Cave Kar Stud. 75:75–82. doi:10.4311/jcks2009mb0131.
   Web of Science ®Google Scholar
• Castanier S, Métayer-Levrel GL, Pertuisot JP. 1999. Ca-carbonate precipitation and limestone genesis— the microbiogeologist point of view. Sed Geol. 126:9–23. doi:10.1016/S0037-0738(99)00028-7.
   Web of Science ®Google Scholar
• Chalia S, Baskar S, Minakshi P, Baskar R, Ranjan K. 2017. Biomineralization abilities of cupriavidus strain and Bacillus subtilis strains in vitro isolated from Speleothems, Rani Cave, Chhattisgarh, India. Geomicrobiol J. 34(9):737–52. doi:10.1080/01490451.2016.1257663.
   Web of Science ®Google Scholar
• Cox G, James JM, Leggett KEA, Osborne RAL. 1989. Cyanobacterially deposited speleothems: subaerial stromatolites. Geomicrobiol J. 7(4):245–52. doi:10.1080/01490458909377870.
   Web of Science ®Google Scholar
• Curry MD, Boston PJ, Spilde MN, Baichtal JF, Campbell AR. 2009. Cottonballs, a unique subaqeous moonmilk, and abundant subaerial moonmilk in Cataract Cave, tongas National Forest, Alaska. Int J Speleol. 38:111–28. doi:10.5038/1827-806X.38.2.3.
   Web of Science ®Google Scholar
• da Mota FF, Vollú RE, Jurelevicius D, Seldin L. 2016. Whole-genome sequence of Rummeliibacillus stabekisii strain PP9 isolated from Antarctic soil. Genome Announc. 4(3):e00416–6. doi:10.1128/genomeA.00416-16. PMID:27231360.
   PubMedGoogle Scholar
• Danielli HMC, Edington MA. 1983. Bacterial calcification in limestone caves. Geomicrobiol J. 3(1):1–16. doi:10.1080/01490458309377780.
   Web of Science ®Google Scholar
• Davis DG, Palmer MV, Palmer AN. 1990. Extraordinary subaqueous speleothems in Lechuguilla Cave, New Mexico. J Cave Kar Stud. 52:70–86.
   Google Scholar
• Davis DG. 2000. Extraordinary features of Lechuguilla Cave, Guadalupe Mountains, New Mexico. J Cave Kar Stud. 62:147–57.
   Google Scholar
• Dick J, De Windt W, De Graef B, Saveyn H, Van der Meeren P, De Belie N, Verstraete W. 2006. Bio-deposition of a calcium carbonate layer on degraded limestone by Bacillus species. Biodegradation. 17:357–67. doi:10.1007/s10532-005-9006-x. PMID:16491305.
   PubMed Web of Science ®Google Scholar
• Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, Visscher PT. 2009. Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev. 96:141–62. doi:10.1016/j.earscirev.2008.10.005.
   Web of Science ®Google Scholar
• Engel AS. 2010. Microbial diversity of cave ecosystems. In: Barton LL, Mandl M, Loy A, editors. Geomicrobiology: molecular and environmental perspective. New York: Springer. p. 219–38.
   Google Scholar
• Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. 39(4):783–91.
   Google Scholar
• Freytet P, Verrecchia EP. 1998. Freshwater organisms that build stromatolites: a synopsis of biocrystallization by prokaryotic and eukariotic algae. Sedimentology. 45:535–63. doi:10.1046/j.1365-3091.1998.00155.x.
   Web of Science ®Google Scholar
• Fernandez-Cortes A, Cuezva S, Sanchez-Moral S, Cañaveras J, Porca E, Jurado V, Martin Sanchez P, Saiz-Jimenez C. 2011. Detection of human-induced environmental disturbances in a show cave. Environ Sci Poll Res. 18:1037–45. doi:10.1007/s11356-011-0513-5.
   PubMed Web of Science ®Google Scholar
• Frisia S, Borsato A, Drysdale RN, Paul B, Greig A, Cotte M. 2012. A re-evaluation of the palaeoclimatic significance of phosphorus variability in speleothems revealed by high resolution synchrotron micro XRF mapping. Clim Past. 8:2039–51. doi:10.5194/cp-8-2039-2012.
   Web of Science ®Google Scholar
• Frisia S. 2015. Microstratigraphic logging of calcite fabrics in speleothems as tool for palaeoclimate studies. Int J Speleol. 44:1–16.
   Web of Science ®Google Scholar
• Frisia S, Borsato A. 2010. Karst. Carbonates in continental settings: facies, environments, and processes. Developments in sedimentology. vol. 61. Elsevier. p. 269–318.
   Google Scholar
• Folk RL. 1965. Some aspects of recrystallization in ancient limestone. Soc Econ Paleont Mineral Spec Publ. 13:14–48.
   Google Scholar
• Fujita Y, Ferris FG, Lawson RD, Colwell FS, Smith RW. 2000. Calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol J. 17:305–18. doi:10.1080/782198884.
   Web of Science ®Google Scholar
• Gonzalez-Muñoz MT, Rodriguez-Navarro C, Martinez-Ruiz F. 2010. Bacterial biomineralization: new insights from Myxococcus-induced mineral precipitation. Geol Soc London Sp Publ. 336:31–50. doi:10.1144/SP336.3.
   Google Scholar
• Gradzíński M, Chmiel MJ, Lewandowska A, Michalska-Kasperkiewicz B. 2010. Siliciclastic micro-stromatolites in a sandstone cave: role of trapping and binding of detrital particles in formation of cave deposits. Ann Soc Geol Polon. 80(3):303–14.
   Web of Science ®Google Scholar
• Groth I, Schumann P, Laiz L, Sanchez-Moral S, Canaveras JC, Saiz-Jimenez C. 2001. Geomicrobiological study of the Grotta dei Cervi, Porto Badisco, Italy. Geomicrobiol J. 18:241–58. doi:10.1080/01490450152467778.
   Web of Science ®Google Scholar
• Heber JR, Sevenson R, Boldman O. 1952. Infrared spectroscopy as a means for identification of bacteria. Science. 116:111–12. doi:10.1126/science.116.3005.111. PMID:14950198.
   PubMed Web of Science ®Google Scholar
• Ikner LA, Toomey RS, Nolan G, Neilson JW, Pryor BM, Maier RM. 2007. Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microbial Ecol. 53:30–42. doi:10.1007/s00248-006-9135-8.
   PubMed Web of Science ®Google Scholar
• Jansson C, Northen T. 2010. Calcifying cyanobacteria — the potential of biomineralization for carbon capture and storage. Curr Opin Biotechnol. 21(3):365–71. doi:10.1016/j.copbio.2010.03.017. PMID:20456936.
   PubMed Web of Science ®Google Scholar
• Jones B. 1991. Genesis of terrestrial oncoids, Cayman Islands, British West Indies. Canadian J Earth Sci. 28:382–97. doi:10.1139/e91-035.
   Web of Science ®Google Scholar
• Jones B. 1995. Processes associated with microbial biofilms in the twilight zone of caves: examples from the Cayman Islands. J Sediment Res A. 65:552–60.
   Web of Science ®Google Scholar
• Jones B. 2009. Mineralized actinomycetes and phosphates in speleothems from Grand Cayman, British West Indies. Sediment Geol. 219:302–17. doi:10.1016/j.sedgeo.2009.05.020.
   Web of Science ®Google Scholar
• Jones B. 2010. Speleothems in a wave-cut notch, Cayman Brac, British West Indies: the integrated product of subaerial precipitation, dissolution, and microbes. Sediment Geol. 232:15–34. doi:10.1016/j.sedgeo.2010.09.003.
   Web of Science ®Google Scholar
• Jones B. 2011. Biogenicity of terrestrial oncoids formed in soil pockets, Cayman Brac, British West Indies. Sediment Geol. 236:95–108. doi:10.1016/j.sedgeo.2010.12.009.
   Web of Science ®Google Scholar
• Jones B, Motyka A. 1987. Biogenic structures and micrite in stalactites from Grand Cayman Island, British West Indies. Can J Earth Sci. 24:1402–11. doi:10.1139/e87-132.
   Web of Science ®Google Scholar
• Jones B, Kahle CF. 1993. Morphology, relationship, and origin of Žber and dendrite calcite crystals. J Sed Petrol. 63:1018–31.
   Google Scholar
• Jroundi F, Fernández-Vivas A, Rodriguez-Navarro C, Bedmar EJ, González-Muñoz MT. 2010. Bioconservation of deteriorated monumental calcarenite stone and identification of bacteria with carbonatogenic activity. Microb Ecol. 60:39–54. doi:10.1007/s00248-010-9665-y. PMID:20386895.
   PubMed Web of Science ®Google Scholar
• Jurado V, Laiz L, Sanchez-Moral S, Saiz-Jimenez C. 2014. Pathogenic microorganisms related to human visits in Altamira Cave, Spain. In: Saiz-Jimenez C, editor. The conservation of subterranean cultural heritage. 2014. Taylor and Francis. p. 229–320. ISBN. 978-1-138-02694-0.
   Google Scholar
• Kasama T, Murakami T. 2001. The effect of microorganisms on Fe precipitation rates at neutral pH. Chem Geol. 180:117–28. doi:10.1016/S0009-2541(01)00309-6.
   Web of Science ®Google Scholar
• Kharpran Daly BD. 2006. The caves of Meghalaya. Shillong: The Directorate of Information and Public Relations Government of Meghalaya.
   Google Scholar
• Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H, Park S, Jeon Y, Lee J, Yi H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol. 62:716–21. doi:10.1099/ijs.0.038075-0. PMID:22140171.
   PubMed Web of Science ®Google Scholar
• Lavoie KH, Northup DE. 2006. Bacteria as indicators of human impact in caves. Proceedings of the 2005 National Cave and Karst Management Symposium; Albany, New York. October 31 to November 4, 2005, the NCKMS Steering Committee, Huntsville, AL. p. 40–7.
   Google Scholar
• Macalady JL, Banfield J. 2004. Molecular geomicrobiology: genes and geochemical cycling. Earth Plan Sci Lett. 209:1–17. doi:10.1016/S0012-821X(02)01010-5.
   Web of Science ®Google Scholar
• Macalady JL, Jones DS, Lyon EH. 2007. Extremely acidic, pendulous microbial biofilms from the Frasassi cave system, Italy. Environ Microbiol. 9:1402–14. doi:10.1111/j.1462-2920.2007.01256.x. PMID:17504478.
   PubMed Web of Science ®Google Scholar
• McConnaughey TA, Whelan JF. 1997. Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev. 42(1–2):95–117. doi:10.1016/S0012-8252(96)00036-0.
   Web of Science ®Google Scholar
• Melim LA, Shinglman KM, Boston PJ, Northup DE, Spilde MN, Queen JM. 2001. Evidence for microbial involvement in pool finger precipitation, Hidden Cave, New Mexico. Geomicrobiol J. 18:311–29. doi:10.1080/01490450152467813.
   Web of Science ®Google Scholar
• Melim LA, Northup DE, Spilde MN, Jones B, Boston PJ, Bixby RJ. 2008. Reticulated filaments in cave pool speleothems: microbe or mineral? J Cave Karst Stud. 70:135–41.
   Web of Science ®Google Scholar
• Melim LA, Liescheidt R, Northup DE, Spilde MN, Boston PJ, Queen JM. 2009. A biosignature suite from cave pool precipitates, Cottonwood Cave, New Mexico. Astrobiol. 9(9):907–17. doi:10.1089/ast.2009.0345.
   PubMed Web of Science ®Google Scholar
• Mulec J, Kosi G, Vrhovšek D. 2007. Algae promote growth of stalagmites and stalactites in karst caves (Škocjanske jame, Slovenia). Carbonates Evaporates. 22(1):6–9.
   Web of Science ®Google Scholar
• Muyzer G, De Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. App Environ Microbiol. 59:695–700.
   PubMed Web of Science ®Google Scholar
• National Bureau of Soil Survey and Land Use Planning. 1996. Geological map of Meghalaya. [Accessed 15 January 2015]. http://megsoil.gov.in/images/meghalaya_soil_map.jpg.
   Google Scholar
• Norris KP. 1959. Infra-red spectroscopy and its application to microbiology. J Hygiene. 57:326–45. doi:10.1017/S0022172400020192.
   PubMedGoogle Scholar
• Northup DE, Lavoie KH. 2001. Geomicrobiology of caves: a review. Geomicrobiol J. 18:199–222. doi:10.1080/01490450152467750.
   Web of Science ®Google Scholar
• Pacton M, Breitenbach SFM, Lechleitner F A, Vaks A, Rollion-Bard C, Gutareva OS, Osintcev AV, Vasconcelos C. 2013. The role of microorganisms in the formation of a stalactite in Botovskaya Cave, Siberia-paleoenvironmental implications. Biogeosciences. 10:6115–30. doi:10.5194/bg-10-6115-2013.
   Web of Science ®Google Scholar
• Polyak VJ, Cokendolpher JC. 1992. Recovery of microfossils from carbonate speleothems. NSS Bull. 54:66–8.
   Google Scholar
• Portillo MC, Porca E, Cuezva S, Sanchez-Moral S, Gonzalez JM. 2009. Is the availability of different nutrients a critical factor for the impact of bacteria on subterraneous carbon budgets? Naturwissenschaften. 96:1035–42. doi:10.1007/s00114-009-0562-5. PMID:19488732.
   PubMed Web of Science ®Google Scholar
• Pflitsch A, Piasecki J. 2003. Detection of an airflow system in Niedzwiedzia (Bear) Cave, Kletno, Poland. J Cave Kar Stud. 65:160–73.
   Web of Science ®Google Scholar
• Preston LJ, Melim LA, Polyak VJ, Asmerom Y, Southam G. 2014. Infrared Spectroscopic Biosignatures from Hidden Cave, New Mexico: possible applications for remote life detection. Geomicrobiol J. 31(10):929–41. doi:10.1080/01490451.2014.913096.
   Web of Science ®Google Scholar
• Ramseyer K, Miano T, D'Orazio V, Wildberger A, Wagner T, Geister J. 1997. Nature and origin of organic matter in carbonates from speleothems, marine cements and coral skeletons. Org Geochem. 26:361–78. doi:10.1016/S0146-6380(97)00008-9.
   Web of Science ®Google Scholar
• Riding R. 1991. Classification of microbial carbonates. In: Riding R, editor. Calcareous algae and stromatolites. Berlin: Springer. p. 21–51.
   Google Scholar
• Rivadeneyra MA, Párraga J, Delgado R, Ramos-Cormenzana A, Delgado G. 2004. Biomineralization of carbonates by Halobacillus trueperi in solid and liquid media with different salinities. FEMS Microbiol Ecol. 48(1):39–46. doi:10.1016/j.femsec.2003.12.008. PMID:19712429.
   PubMed Web of Science ®Google Scholar
• Robinson JW, Frame EMS, Frame GM II. 2004. Undergraduate instrumental analysis. 6th ed. New York: CRC Press, Taylor and Francis Group. p. 1079.
   Google Scholar
• Schabereiter-Gurtner C, Saiz-Jimenez C, Piñar G, Lubitz W, Rölleke S. 2002. Phylogenetic 16S rRNA analysis reveals the presence of complex and partly unknown bacterial communities in Tito Bustillo cave, Spain, and on its Palaeolithic paintings. Environ Microbiol. 4:392–400. doi:10.1046/j.1462-2920.2002.00303.x. PMID:12123475.
   PubMed Web of Science ®Google Scholar
• Schabereiter-Gurtner C, Saiz-Jimenez C, Piñar G, Lubitz W, Rölleke S. 2004. Phylogenetic diversity of bacteria associated with paleolithic paintings and surrounding rock walls in two Spanish caves (Llonín and La Garma). FEMS Microbiol Ecol. 47:235–47. doi:10.1016/S0168-6496(03)00280-0. PMID:19712338.
   PubMed Web of Science ®Google Scholar
• Stomeo F, Portillo MC, Gonzalez JM. 2009. Assessment of bacterial and fungal growth on natural substrates: consequences for preserving caves with prehistoric paintings. Curr Microbiol. 59:321–5. doi:10.1007/s00284-009-9437-4. PMID:19536596.
   PubMed Web of Science ®Google Scholar
• Sánchez-Román M, Vasconcelos C, Schmid T, Dittrich M, McKenzie JA, Zenobi R. 2008. Aerobic microbial dolomite at the nanometer scale: implications for the geologic record. Geology. 36:879–82. doi:10.1130/G25013A.1.
   Web of Science ®Google Scholar
• Sanchez-Moral S, Portillo MC, Janices I, Cuezva S, Fernández-Cortés A, Cañaveras JC, Gonzalez JM. 2012. The role of microorganisms in the formation of calcitic moonmilk deposits and speleothems in Altamira Cave. Geomorphology. 139–140:285–92. doi:10.1016/j.geomorph.2011.10.030.
   Web of Science ®Google Scholar
• Sharma YR. 1989. Elementary organic spectroscopy: principles and chemical applications. New Delhi (India): S. Chand Publisher. p. 294.
   Google Scholar
• Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Bio Evol. 24:1596–99.
   Google Scholar
• Thrailkill, JV. 1964. Origin of cave popcorn [abs.]: Bulletin of the National Speleological Society. 27, p. 59.
   Google Scholar
• Urzì C, De Leo F, Bruno L, Albertano P. 2010. Microbial diversity in Paleolithic caves: a study case on the phototrophic biofilms of the Cave of Bats (Zuheros, Spain). Microbial Ecol. 60:116–29. doi:10.1007/s00248-010-9710-x.
   PubMed Web of Science ®Google Scholar
• Vaishampayan P, Miyashita M, Ohnishi A, Satomi M, Rooney A, et al. 2009. Description of Rummeliibacillus stabekisii gen. nov., sp. nov. and reclassification of Bacillus pycnus Nakamura et al., 2002 as Rummeliibacillus pycnus comb.nov. Int J Syst Evol Microbiol. 59:1094–99. doi:10.1099/ijs.0.006098-0. PMID:19406799.
   PubMed Web of Science ®Google Scholar
• Vasconcelos C, McKenzie JA, Bernasconi S, Grujic D, Tien AJ. 1995. Microbial mediation as a possible mechanism for natural dolomite formation at low temperatures. Nature. 377:220–2. doi:10.1038/377220a0.
   Web of Science ®Google Scholar
• Warthmann R, van Lith Y, Vasconcelos C, McKenzie JA, Marpoff AM. 2000. Bacterially induced dolomite precipitation in anoxic culture experiments. Geology. 32:277–80.
   Google Scholar
• Zhou J, Gu Y, Zou C, Mo M. 2007. Phylogenetic diversity of bacteria in an earth-cave in Guizhou Province, Southwest of China. J Microbiol. 45:105–12. PMID:17483794.
   PubMed Web of Science ®Google Scholar