Calcium carbonate precipitation by heterotrophic bacteria isolated from biofilms formed on deteriorated ignimbrite stones: influence of calcium on EPS production and biofilm formation by these isolates

Biofouling

Volumn 30, Issue 5, 2014, Pages 547-560

  López Moreno, Angélica ^a   Sepúlveda Sánchez, José David ^b   Mercedes Alonso Guzmán, Elia Mercedes ^c   Le Borgne, Sylvie ^d  

^a UNIVERSIDAD AUTÓNOMA METROPOLITANA   (Mexico)

^b DEPARTAMENTO DE QUÍMICA   (Mexico)

^c UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO   (Mexico)

^d DEPARTAMENTO DE PROCESOS Y TECNOLOGÍA   (Mexico)

Author keywords

biofilm formation; calcium effect; EPS production; heterotrophic bacteria; ignimbrite stones

Indexed keywords

BACTERIUM; BIOFILM; CALCITE; CALCIUM CARBONATE; COLONIZATION; IGNIMBRITE; ISOLATED POPULATION; VATERITE;

MEXICO [NORTH AMERICA]; MICHOACAN; MORELIA;

BACILLUS (BACTERIUM); BACILLUS SP.; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ENTEROBACTER; ENTEROBACTER CANCEROGENUS;

CALCIUM CARBONATE;

BACILLUS; BIOFILM; CHEMISTRY; ENTEROBACTER; GENETICS; HETEROTROPHY; ISOLATION AND PURIFICATION; METABOLISM; MEXICO; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PRECIPITATION; SURFACE PROPERTY;

BACILLUS; BIOFILMS; CALCIUM CARBONATE; CHEMICAL PRECIPITATION; ENTEROBACTER; HETEROTROPHIC PROCESSES; MEXICO; MOLECULAR SEQUENCE DATA; PHYLOGENY; SURFACE PROPERTIES;

EID: 84900022666     PISSN: 08927014     EISSN: 10292454     Source Type: Journal    
DOI: 10.1080/08927014.2014.888715     Document Type: Article

References (76)

1. Achal V, Pan X. 2011. Characterization of urease and carbonic anhydrase producing bacteria and their role in calcite precipitation. Curr Microbiol. 62:894-902.
2. Achal V, Abhijit M, Reddy MS. 2010. Characterization of two urease-producing and calcifying Bacillus spp. isolated from cement. J Microbiol Biotechnol. 20:1571-1576.
3. Allen MM. 1968. Simple conditions for growth of unicellular blue-green algae on plates. J Phycol. 4:1-4.
4. Allsopp D, Seal KJ, Gaylarde CC. 2004. Introduction to biodeterioration. 2nd ed. Cambridge: Cambridge University Press.
5. Alonso E, Martínez L. 2003. The role of environmental sulfur on degradation of ignimbrites of the Cathedral in Morelia, Mexico. Build Environ. 38:861-867.
6. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
7. Bachmeier KL, Williams AE, Warmington JR, Bang SS. 2002. Urease activity in microbiologically-induced calcite precipitation. J Biotechnol. 93:171-181.
8. Baker GC, Smith JJ, Cowan DA. 2003. Review and re-analysis of domain-specific 16S primers. J Microbiol Methods. 55:541-555.
9. Barabesi C, Galizzi A, Mastromei G, Rossi M, Tamburini E, Perito B. 2007. Bacillus subtilis gene cluster involved in calcium carbonate biomineralization. J Bacteriol. 189:228-235.
10. 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.
11. Braissant O, Cailleau G, Dupraz C, Verrecchia EP. 2003. Bacterially induced mineralization of calcium carbonate in terrestrial environments: the role of exopolysaccharides and amino acids. J Sediment Res. 73:485-490.
12. 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. 20:85-98.
13. Dakal TC, Cameotra SS. 2012. Microbially induced deterioration of architectural heritages: routes and mechanisms involved. Environ Sci Europe. 24:36.
14. De Belie N. 2010. Microorganisms versus stony materials: a love-hate relationship. Mater Struct. 43:1191-1202.
15. De Muynck W, De Belie N, Verstraete W. 2010. Microbial carbonate precipitation in construction materials: a review. Ecol Eng. 36:118-136.
16. Dick J, De Windt W, De Graef B, Saveyn H, Van der Meere P, De Belie N, Verstraete W. 2006. Bio-deposition of a calcium carbonate layer on degraded limestone by Bacillus species. Biodegradation. 17:357-367.
17. Ercole C, Bozzelli P, Altieri F, Cacchio P, Del Gallo M. 2012. Calcium carbonate mineralization: involvement of extracellular polymeric materials isolated from calcifying bacteria. Microsc Microanal. 18:829-839.
18. Fernandes P. 2006. Applied microbiology and biotechnology in the conservation of stone cultural heritage materials. Appl Microbiol Biotechnol. 73:291-296.
19. 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.
20. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiology. 8:623-633.
21. Fortin D, Ferris FG, Beveridge TJ. 1997. Surface-mediated mineral development by bacteria. Rev Mineral. 35:161-180.
22. Friedman LE, de Rossi BN, Messina MT, Franco MA. 2001. Phenotype evaluation of Bordetella bronchiseptica cultures by urease activity and Congo red affinity. Lett Appl Microbiol. 33:285-290.
23. Gaylarde P, Gaylarde C. 2004. Deterioration of siliceous stone monuments in Latin America: microorganisms and mechanisms. Corros Rev. 22:395-416.
24. Geesey GG, Wigglesworth-Cooksey B, Cooksey KE. 2000. Influence of calcium and other cations on surface adhesion of bacteria and diatoms: a review. Biofouling. 15:195-205.
25. Gerhardt P, Murray RGE, Wood WA, Krieg NR. 1994. Methods for general and molecular bacteriology. Washington (DC): American Society for Microbiology Press.
26. Gorbushina AA. 2007. Life on the rocks. Environ Microbiol. 9:1613-1631.
27. Gundlapally SR, Garcia-Pichel F. 2006. The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol. 52:345-357.
28. Hammes F, Verstraete W. 2002. Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev Environ Sci Biotechnol. 1:3-7.
29. Hammes F, Boon N, De Villiers J, Verstraete W, Douglas SS. 2003. Strain-specific ureolytic microbial calcium carbonate precipitation. Appl Environ Microbiol. 69:4901-4909.
30. Hernández-Mariné M, Roldán Molina M. 2012. Biofilms on rocks. In D Muñoz Torrero, D. Haro, J. Vallès, editors. Recent Advances in Pharmaceutical Sciences II. Kerala: Transworld Research Network; p. 1-13 [e-book].
31. Herzberg M, Kang S, Elimelech M. 2009. Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. Environ Sci Technol. 43:4393-4398.
32. Jansson C, Northen T. 2010. Calcifying cyanobacteria-the potential of biomineralization for carbon capture and storage. Curr Opin Biotechnol. 21:365-371.
33. Jimenez-Lopez C, Rodriguez-Navarro C, Piñar G, Carillo-Rosúa FJ, Rodriguez-Gallego M, Gonzalez-Muñoz MT. 2007. Consolidation of degraded ornamental porous limestone stone by calcium carbonate precipitation induced by the microbiota inhabiting the stone. Chemosphere. 68:1929-1936.
34. Johnson JL. 1994. Similarity analysis of rRNAs. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR, editors. Methods for general and molecular microbiology. Washington (DC): American Society for Microbiology; p. 683-700.
35. 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.
36. Keefe WE. 1976. Formation of crystalline deposits by several genera of the family Enterobacteriaceae. Infect Immun. 14:590-592.
37. Knorre H, Krumbein WE. 2000. Bacterial calcification. In: Riding RE, Awramik SM, editors. Microbial sediments. Berlin: Springer-Verlag; p. 25-31.
38. Laiz L, Miller AZ, Jurado V, Akatova E, Sanchez-Moral S, Gonzalez JM, Dionísio A, Macedo MF. 2009. Isolation of five Rubrobacter strains from biodeteriorated monuments. Naturwissenschaften. 96:71-79.
39. McNamara CJ, Perry IVTD, Bearce KA, Hernandez-Duque G, Mitchell R. 2006. Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microb Ecol. 51:51-64.
40. Miller AZ, Laiz L, Gonzalez JM, Dionísio A, Macedo MF, Saiz-Jimenez C. 2008. Reproducing stone monuments photosynthetic-based colonization under laboratory conditions. Sci Total Environ. 405:278-285.
41. Miller AZ, Sanmartín P, Pereira-Pardo L, Dionísio A, Saiz-Jimenez C, Macedo MF, Prieto B. 2012. Bioreceptivity of building stones: a review. Sci Total Environ. 426:1-12.
42. Morse JW, Mackenzie FT. 1990. Geochemistry of sedimentary carbonates. Amsterdam: Elsevier.
43. Natarajan KR. 1995. Kinetic study of the enzyme urease from Dolichos biflorus. J Chem Educ. 72:556-557.
44. Nehrke G, Van Cappellen P, van der Weijden CH. 2006. Framboidal vaterite aggregates and their transformation into calcite. A morphological study. J Cryst Growth. 287:528-530.
45. Ortega-Morales BO, Hernández-Duque G, Borges-Gómez L, Guezennec J. 1999. Characterization of epilithic microbial communities associated with Mayan stone monuments in Yucatan, Mexico. Geomicrobiol J. 16:221-232.
46. Ortega-Morales BO, Gaylarde CC, Englert GE, Gaylarde PM. 2005. Analysis of salt-containing biofilms on limestone buildings of the Mayan culture at Edzna, Mexico. Geomicrobiol J. 22:261-268.
47. Patrauchan MA, Sarkisova S, Sauer K, Franklin MJ. 2005. Calcium influences cellular and extracellular product formation during biofilm-associated growth of a marine Pseudoalteromonas sp. Microbiology. 151:2885-2897.
48. Perito B, Mastromei G. 2011. Molecular basis of bacterial calcium carbonate precipitation. Prog Mol Subcell Biol. 52:113-139.
49. Phillips AJ, Gerlach R, Lauchnor E, Mitchell AC, Cunningham AB, Spangler L. 2013. Engineered applications of ureolytic biomineralization: a review. Biofouling. 29:715-733.
50. 2 leakage reduction through biofilm-induced calcium carbonate precipitation. Environ Sci Technol. 47:142-149.
51. Portillo MC, Gonzalez MJ. 2011. Microbial community diversity and the complexity of preserving cultural heritage. In: Charola AE, McNamara C, Koestler RJ. editors. Biocolonization of stone: control and preventive methods. Smithsonian contributions to museum conservation. Washington (DC): Smithsonian Institution Scholarly Press. Number 2 p. 19-28.
52. Ramirez M, Hernandez-Marine M, Novelo E, Roldan M. 2010. Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling. 26:399-409.
53. Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR. 2007. Methods for general and molecular microbiology. 3rd ed. Washington (DC): American Society for Microbiology Press.
54. Rivadeneyra MA, Ramos-Cormenzana A, García-Cervigón A. 1983. Bacterial formation of struvite. Geomicrobiol J. 3:151-163.
55. Rivadeneyra MA, Delgado G, Ramos-Cormenzana A, Delgado R. 1998. Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities: crystal formation sequence. Res Microbiol. 149:277-287.
56. Rodriguez-Navarro C, Rodriguez-Gallego M, Ben Chekroun K, Gonzalez-Muñoz MT. 2003. Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Appl Environ Microbiol. 69:2182-2193.
57. Rodriguez-Navarro C, Jroundi F, Schiro M, Ruiz-Agudo E, González-Muñoz MT. 2012. Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environ Microbiol. 78:4017-4029.
58. Rossi F, Micheletti E, Bruno L, Adhikary SP, Albertano P, Philippis RD. 2012. Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monuments. Biofouling. 28:215-224.
59. Rusznyák A, Akob DM, Nietzsche S, Eusterhues K, Totsche KU, Neu TR, Frosch T, Popp J, Keiner R, Geletneky J, et al. 2012. Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg Cave. Appl Environ Microbiol. 78:1157-1167.
60. Sánchez-Román M, Rivadeneyra MA, Vasconcelos C, McKenzie JA. 2007. Biomineralization of carbonate and phosphate by moderately halophilic bacteria. FEMS Microbiol Ecol. 61:273-284.
61. Scheerer S, Ortega-Morales O, Gaylarde C. 2009. Microbial deterioration of stone monuments - an updated overview. Advances Appl Microbiol. 66:97-139.
62. Scholl MA, Mills AL, Herman JS, Hornmerger GM. 1990. The influence of mineralogy and solution chemistry on the attachment of bacteria to representative aquifer materials. J Cont Hydrol. 6:321-336.
63. Shirakawa MA, Beech IB, Tapper R, Cincotto MA, Gambale W. 2003. The development of a method to evaluate bioreceptivity of indoor mortar plastering to fungal growth. Int Biodeter Biodegr. 51:83-92.
64. Shirakawa MA, Cincotto MA, Atencio D, Gaylarde CC, Vanderley MJ. 2011. Effect of culture medium on biocalcification by Pseudomonas putida, Lysinibacillus sphaericus and Bacillus subtilis. Braz J Microbiol. 42:499-507.
65. Smalley JW, Birss AJ, McKee AS, Marsh PD. 1995. Congo red binding by Porphyromonas gingivalis is mediated by a 66 kDa outer-membrane protein. Microbiology. 141:205-211.
66. Sondi I, Matijevic E. 2001. Homogeneous precipitation of calcium carbonate by enzyme catalyzed reaction. J Colloid Interface Sci. 238:208-214.
67. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
68. 3 morphology and polymorphism. Chem Geol. 262:138-146.
69. Urzi C, Garcia-Valles M, Vendrell M, Pernice A. 1999. Biomineralization processes on rock and monument surfaces observed in field and in laboratory conditions. Geomicrobiol J. 16:39-54.
70. Videla HA. 1996. Manual of biocorrosion. Boca Raton (FL): CRC Lewis Publishers, 1-11.
71. Videla HA, Guiamet PS, De Saravia SG. 2000. Biodeterioration of Mayan archaeological sites in the Yucatan Peninsula, Mexico. Int Biodeterior Biodegr. 46:335-341.
72. Warscheid T, Braams J. 2000. Biodeterioration of stone: a review. Int Biodeterior Biodegr. 46:343-368.
73. Weatherburn MW. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal Chem. 39:971-974.
74. Wierzchos J, Davila AF, Artieda O, Cámara-Gallego B, Asunción de los Ríos, Nealson KH, Valea S, García-González MT, Ascaso C. 2013. Ignimbrite as a substrate for endolithic life in the hyper-arid Atacama Desert: implications for the search for life on Mars. Icarus. 224:334-346.
75. Zamarreño DV, Inkpen R, May E. 2009. Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl Environ Microbiol. 75:5981-5990.
76. Zammit G, Sánchez-Moral S, Albertano P. 2011. Bacterially mediated mineralisation processes lead to biodeterioration of artworks in Maltese catacombs. Sci Total Environ. 409:2773-2782.