Systematic investigation of germination responses of Bacillus subtilis spores in different high-salinity environments

FEMS Microbiology Ecology

Volumn 91, Issue 5, 2015, Pages

  Nagler, Katja ^a   Moeller, Ralf ^a  

^a GERMAN AEROSPACE CENTER DLR   (Germany)

Author keywords

Ions; Metals; Osmotic stress; Salt stress; Salt dependent germination inhibition; Spore germination

Indexed keywords

BACTERIUM; CONCENTRATION (COMPOSITION); ENVIRONMENTAL STRESS; INHIBITION; ION; LIFE CYCLE; METAL; MICROBIAL ECOLOGY; OSMOREGULATION; SALINITY TOLERANCE; SODIUM CHLORIDE; SOIL MICROORGANISM; SPORE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

INORGANIC SALT; SODIUM CHLORIDE; SOIL; WATER;

BACILLUS SUBTILIS; BACTERIAL SPORE; CHEMISTRY; DESICCATION; DRUG EFFECTS; MICROBIOLOGY; OSMOSIS; OSMOTIC PRESSURE; PHYSIOLOGY; SALINITY; SOIL;

BACILLUS SUBTILIS; DESICCATION; OSMOSIS; OSMOTIC PRESSURE; SALINITY; SALTS; SODIUM CHLORIDE; SOIL; SOIL MICROBIOLOGY; SPORES, BACTERIAL; WATER;

EID: 84940785953     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiv023     Document Type: Article

References (57)

1. Arias ME, González-Pérez JA, Gonález-Vila FJ, et al. Soil health-a new challenge for microbiologists and chemists. Int Microbiol 2005;8:13-21.
2. Atluri S, Ragkousi K, Cortezzo DE, et al. Cooperativity between different nutrient receptors in germination of spores of Bacillus subtilis and reduction of this cooperativity by alterations in the GerB receptor. J Bacteriol 2006;188:28-36.
3. Bremer E. Adaptation to changing osmolarity. In: Hoch JA, Losick R, Sonenshein AL (eds). Bacillus Subtilis and Its Closest relatives: From Genes to Cells.Washington, DC: ASM Press, 2002, 385-91.
4. Cabezali CB, Baldini MD, Burgos MA, et al. Relationship of physical factors and salinity with indicator bacteria in Bahiá Blanca estuary waters, Argentina. Rev Argent Microbiol 1994;26:59-64.
5. Chung L., Rajan KS, Merdinger E, et al. Coordinative binding of divalent cations with ligand related to bacterial spores. Equilibrium studies. Biophys J 1971;11:469-82.
6. Datta KK, de Jong C. Adverse effect of waterlogging and soil salinity on crop and land productivity in northwest region of Haryana, India. Agr Water Manage 2002;57:223-38.
7. Davila AF, Duport LG, Melchiorri R, et al. Hygroscopic salts and the potential of life on Mars. Astrobiology 2010;10:617-28.
8. de Souza Silva AMM, Fay EF. Effect of salinity on soilmicroorganisms. In: Hernandez-Soriano MC (ed). Soil Health and Land Use Management. Rijeka, Croatia: InTech Europe, 2012, 177-98.
9. Duda VI, Danilevich VN, Suzina NE, et al. Changes in thefine structure of microbial cells induced by chaotropic salts. Microbiology 2004;73:341-9.
10. Earl AM, Losick R, Kolter R. Ecology and genomics of Bacillus subtilis. Trends Microbiol 2008;16:269-75.
11. European Commission, DG Health and Consumers, Food and Feed Safety. Food Additives Database, 2013. http://www.ec.europa.eu/food/food/fAEF/additives/lists authorised fA en. htm (30 May 2013, date last accessed).
12. Falkowski PG, Fenchel T, Delong EF. The microbial engines that drive Earth's biogeochemical cycles. Science 2008;320:1034-9.
13. Fleming HP, Ordal ZJ. Responses of Bacillus subtilis spores to ionic environments during sporulation and germination. J Bacteriol 1964;88:1529-37.
14. Francis CA, Tebo BM. Marine Bacillus spores as catalysts for oxidative precipitation and sorption of metals. J Mol Microbiol Biotechnol 1999;1:71-8.
15. Frische T, Höper H. Soil microbial parameters and luminescent bacteria assays as indicators for in situ bioremediation of TNT-contaminated soils. Chemosphere 2003;50:415-27.
16. Gest H, Mandelstam J. Longevity of microorganisms in natural environments. Microbiol Sci 1987;4:69-71.
17. Griffiths KK, Zhang J, Cowan AE, et al. Germination proteins in the inner membrane of dormant Bacillus subtilis spores colocalize in a discrete cluster. Mol Microbiol 2011;81:1061-77.
18. He LM, Tebo BM. Surface charge properties of and Cu(II) adsorption by spores of the marine Bacillus sp. strain SG-1. Appl Environ Microb 1998;64:1123-9.
19. Hudson KD, Corfe BM, Kemp EH, et al. Localization of GerAA and GerAC germination proteins in the Bacillus subtilis spore. J Bacteriol 2001;183:4317-22.
20. Ishikawa S, Yamane K, Sekiguchi J. Regulation and characterization of a newly deduced cell wall hydrolase gene (cwlJ) which affects germination of Bacillus subtilis spores. J Bacteriol 1998;180:1375-80.
21. Ju XT, Kou CL, Christie P, et al. Changes in the soil environment from excessive application of fertilizers and manures to two contrasting intensive cropping systems on the North China Plain. Environ Pollut 2007;145:497-506.
22. Keijser BJF, Ter Beek A, Rauwerda H, et al. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J Bacteriol 2007;189:3624-34.
23. Kloepper JW, Ryu C-M, Zhang S. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 2004;94:1259-66.
24. Li Y, Davis A, Korza G, et al. Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis. J Bacteriol 2012;194:1875-84.
25. Lucho-Constantino CA, Aĺvarez-Suárez M, Beltrán-Hernández RI, et al. Amultivariate analysis of the accumulation and fractionation of major and trace elements in agricultural soils in Hidalgo State, Mecixo irrigated with raw wastewater. Environ Int 2005;31:313-23.
26. Marles-Wright J, Lewis RJ. Stress responses of bacteria. Curr Opin Struct Biol 2007;17:755-60.
27. Metternicht GI, Zinck JA. Remote sensing of soil salinity: potentials and constrains. Remote Sens Environ 2003;85:1-20.
28. Miller KJ, Wood JM. Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 1996;50:101-36.
29. Nagler K, Setlow P, Li YQ, et al. High salinity alters the germination behavior of Bacillus subtilis spores with nutrient and nonnutrient germinants. Appl Environ Microb 2014;80:1314-21.
30. Nicholson WL. Roles of Bacillus endospores in the environment. Cell Mol Life Sci 2002;59:410-6.
31. NicholsonWL, Munakata N, Horneck G, et al. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol R 2000;64:548-72.
32. Nicholson WL, Schuerger AC, Race MS. Migrating microbes and planetary protection. Trends Microbiol 2009;17:389-92.
33. Nicholson WL, Setlow P. Sporulation, germination, and outgrowth. In: Harwood CR, Cutting SM (eds). Molecular Biological Methods for Bacillus. Sussex, UK: John Wiley & Sons, 1990, 391-450.
34. Paidhungat M, Setlow P. Role of Ger proteins in nutrient and nonnutrient triggering of spore germination. J Bacteriol 2000;182:2513-9.
35. Paidhungat M, Setlow P. Localization of a germinant receptor protein (GerBA) to the inner membrane of Bacillus subtilis spores. J Bacteriol 2001;183:3982-90.
36. Paredes-Sabja D, Setlow P, Sarker MR. Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol 2010;19:85-94.
37. Priest FG. Systematics and ecology of Bacillus. In: Sonenshein AL, Hoch JA, Losick R (eds). Bacillus Subtilis and Other Gram- Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. Washington, DC: American Society for Microbiology, 1993, 3-16.
38. Rusan MJM, Hinnawi S, Rousan L. Long term effect ofwastewater irrigation of forage crops on soil and plant quality parameters. Desalination 2007;215:143-52.
39. Sass AM,McKew BA, Sass H, et al. Diversity of Bacillus-like organisms isolated from deep-sea hypersaline anoxic sediments. Saline Systems 2008;4:8.
40. Sawyer WH, Puckridge J. The dissociation of proteins by chaotropic salts. J Biol Chem 1973;248:8429-33.
41. Schaeffer P, Millet J, Aubert JP. Catabolic repression of bacterial sporulation. P Natl Acad Sci USA 1965;54:704-11.
42. Schoenholtz SH, Van Miegroet H, Burger JA. A review of chemical and physical properties as indicators of forest soil quality: challenges and opportunities. Forest Ecol Manag 2000;138:335-56.
43. Setlow B, Melly E, Setlow P. Properties of spores of Bacillus subtilis blocked at an intermediate stage of spore germination. J Bacteriol 2001;183:4894-9.
44. Setlow P. Spore germination. Curr Opin Microbiol 2003;6:550-6.
45. Setlow P. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 2006;101:514-25.
46. SetlowP. Iwill survive:DNA protection in bacterial spores. Trends Microbiol 2007;15:172-80.
47. Sunde EP, Setlow P, Hederstedt L, et al. The physical state of water in bacterial spores. P Natl Acad Sci USA 2009;106: 19334-9.
48. Swerdlow BM, Setlow B, Setlow P. Levels of H+ and other monovalent cations in dormant and germinating spores of Bacillus megaterium. J Bacteriol 1981;148:20-9.
49. Vepachedu VR, Setlow P. Localization of SpoVAD to the inner membrane of spores of Bacillus subtilis. J Bacteriol 2005;187:5677-82.
50. Vepachedu VR, Setlow P. Role of SpoVA proteins in release of dipicolinic acid during germination of Bacillus subtilis spores triggered by dodecylamine or lysozyme. J Bacteriol 2007;189:1565-72.
51. Yastrebova OV, Plotnikova EG, Anan'ina LN, et al. Aerobic sporeforming bacteria from the region of salt mining. Russ J Ecol 2009;40:516-21.
52. Yi X, Bond C, Sarker MR, et al. Efficient inhibition of germination of coat-deficient bacterial spores by multivalent metal cations, including terbium (Tb3+). Appl Environ Microb 2011;77:5536-9.
53. Yi X, Setlow P. Studies of the commitment step in the germination of spores of Bacillus species. J Bacteriol 2010;192:3424-33.
54. Zhang W, Li F, Nie L. Integrating multiple 'omics' analysis for microbial biology: application and methodologies. Micobiology 2010;156:287-301.
55. Zhang Y, Cremer PS. Interactions between marcomoleculaes and ions: the Hofmeister series. Curr Opin Chem Biol 2006;10:658-63.
56. Zhang Y, Cremer PS. Chemistry of Hofmeister anions and osmolytes. Annu Rev Phys Chem 2010;61:63-83.
57. Zorzano MP, Mateo-Martí E, Prieto-Ballesteros O, et al. Stability of liquid saline water on present day Mars. Geophys Res Lett 2009;36:L20201.