Changes in Bacillus spore small molecules, rRNA, germination, and outgrowth after extended sublethal exposure to various temperatures: Evidence that protein synthesis is not essential for spore germination

Journal of Bacteriology

Volumn 198, Issue 24, 2016, Pages 3254-3264

  Korza, George ^a   Setlow, Barbara ^a   Rao, Lei ^a   Li, Qiao ^a   Setlow, Peter ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE TRIPHOSPHATE; PHOSPHORUS; PROTEIN; RIBONUCLEASE; RIBONUCLEASE Y; RIBOSOME RNA; RNA 16S; RNA 23S; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACILLUS MEGATERIUM; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIAL STRAIN; CONTROLLED STUDY; EXPOSURE; HIGH TEMPERATURE; INCUBATION TIME; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN HYDROLYSIS; PROTEIN SYNTHESIS; RNA DEGRADATION; RNA PURIFICATION; SPORE GERMINATION; VEGETATIVE GROWTH; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TEMPERATURE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN BIOSYNTHESIS; RNA, RIBOSOMAL; SPORES, BACTERIAL; TEMPERATURE;

EID: 84996773886     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00583-16     Document Type: Article

References (52)

1. Setlow P, Johnson EA. 2012. Spores and their significance, p 45-79. In Doyle MP, Buchanan R (ed), Food microbiology: fundamentals and frontiers, 4th edition. ASM Press, Washington, DC
2. Setlow P. 2016. Spore resistance properties, p 201-216. In Eichenberger P, Driks A (ed), The bacterial spore. ASM Press, Washington, DC
3. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101:514-525. http://dx .doi.org/10.1111/j.1365-2672.2005.02736.x
4. Setlow P. 2013. When the sleepers wake: the germination of spores of Bacillus species. J Appl Microbiol 115:1251-1268. http://dx.doi.org/10 .1111/jam.12343
5. Setlow P. 2014. The germination of spores of Bacillus species: what we know and do not know. J Bacteriol 196:1297-1305. http://dx.doi.org/10 .1128/JB.01455-13
6. Setlow P, Kornberg A. 1970. Biochemical studies of bacterial sporulation and germination. XXII. Energy metabolism in early stages of germination of Bacillus megaterium spores. J Biol Chem 245:3637-3644
7. Scott IR, Ellar DJ. 1978. Metabolism and the triggering of germination of Bacillus megaterium. Concentrations of amino acids, organic acids, adenine nucleotides and nicotinamide nucleotides during germination. Biochem J 174:627-634
8. Scott IR, Ellar DJ. 1978. Metabolism and the triggering of germination of Bacillus megaterium. Use of L-[3H]alanine and tritiated water to detect metabolism. Biochem J 174:635-640
9. Vary JC. 1978. Glucose-initiated germination in Bacillus megaterium spores, p 104-108. In Chambliss G, Vary JC (ed), Spores VII. American Society for Microbiology, Washington, DC
10. Magge A, Setlow B, Cowan AE, Setlow P. 2009. Analysis of dye binding by and membrane potential in spores of Bacillus species. J Appl Microbiol 106:814-821. http://dx.doi.org/10.1111/j.1365-2672.2008.04048.x
11. 31P-NMR of lowmolecular-weight compounds. J Bacteriol 197:992-1001. http://dx.doi .org/10.1128/JB.02520-14
12. Segev E, Smith Y, Ben-Yehuda S. 2012. RNA dynamics in aging bacterial spores. Cell 148:139-149. http://dx.doi.org/10.1016/j.cell.2011.11.059
13. Sinai L, Rosenberg A, Smith Y, Segev E, Ben-Yehuda S. 2015. The molecular timeline of a reviving bacterial spore. Mol Cell 57:695-707. http://dx.doi.org/10.1016/j.molcel.2014.12.019
14. Setlow B, Setlow P. 1996. Role of DNA repair in Bacillus subtilis spore resistance. J Bacteriol 178:3486-3495
15. Paidhungat M, Setlow P. 2000. Role of Ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. J Bacteriol 182:2513-2519. http://dx.doi.org/10.1128/JB.182.9.2513-2519.2000
16. Commichau FM, Rothe FM, Herzberg C, Wagner E, Hellwig D, Lehnik-Habrink M, Hammer E, Völker U, Stülke J. 2009. Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8:1350-1360. http://dx.doi.org/10.1074/mcp.M800546-MCP200
17. Nicholson WL, Setlow P. 1990. Sporulation, germination and outgrowth, p 391-450. In Harwood CR, Cutting SM (ed), Molecular biological methods for Bacillus. John Wiley & Sons, Chichester, United Kingdom
18. Gupta S, Ustok FI, Johnson CL, Bailey DMD, Lowe CR, Christie G. 2013. Investigating the functional hierarchy of Bacillus megaterium PV361 spore germinant receptors. J Bacteriol 195:3045-3053. http://dx.doi.org/10.1128/JB.00325-13
19. Coleman WH, Zhang P, Li YQ, Setlow P. 2010. Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Lett Appl Microbiol 50:507-514. http://dx.doi.org/10.1111/j.1472-765X.2010.02827.x
20. Coleman WH, Chen D, Li YQ, Cowan AE, Setlow P. 2007. How moist heat kills spores of Bacillus subtilis. J Bacteriol 189:8458-8466. http://dx .doi.org/10.1128/JB.01242-07
21. Paidhungat M, Setlow B, Driks A, Setlow P. 2000. Characterization of spores of Bacillus subtilis which lack dipicolinic acid. J Bacteriol 182:5505-5512. http://dx.doi.org/10.1128/JB.182.19.5505-5512.2000
22. Yi X, Setlow P. 2010. Studies of the commitment step in the germination of spores of Bacillus species. J Bacteriol 192:3424-3433. http://dx.doi.org/10.1128/JB.00326-10
23. Luu S, Cruz-Mora J, Setlow B, Feeherry FE, Doona CJ, Setlow P. 2015. The effects of heat activation on Bacillus spore germination with nutrients or under high pressure, with or without various germination proteins. Appl Environ Microbiol 81:2927-2938. http://dx.doi.org/10.1128/AEM.00193-15
24. Setlow B, Melly E, Setlow P. 2001. Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. J Bacteriol 183: 4894-4899. http://dx.doi.org/10.1128/JB.183.16.4894-4899.2001
25. Moeller R, Hornek G, Rettberg G, Mollenkopf H-J, Stackebrandt E, Nicholson WL. 2006. A method for extracting RNA from dormant and germinating Bacillus subtilis strain 168 endospores. Curr Microbiol 53: 227-231. http://dx.doi.org/10.1007/s00284-006-0099-1
26. Rump VL, Asamoah B, Gonzalez-Escalona N. 2010. Comparison of commercial RNA extraction kits for preparation of DNA-free total RNA from Salmonella cells. BMC Res Notes 3:211. http://dx.doi.org/10.1186/1756-0500-3-211
27. Knaysi G. 1965. Maximal temperatures of the two stages of germination in several mesophilic members of the genus Bacillus. Appl Microbiol 13: 500-501
28. Nelson DL, Kornberg A. 1970. Biochemical studies of bacterial sporulation and germination. XIX. Phosphate metabolism during sporulation. J Biol Chem 245:1137-1145
29. Wang G, Paredes-Sabja D, Sarker MR, Green C, Setlow P, Li YQ. 2012. Effects of wet heat-treatment on the germination of individual spores of Clostridium perfringens. J Appl Microbiol 113:824-836. http://dx.doi.org/10.1111/j.1365-2672.2012.05387.x
30. Hyatt MT, Levinson HS. 1961. Interaction of heat, glucose, L-alanine, and potassium nitrate in spore germination of Bacillus megaterium. J Bacteriol 81:204-211
31. Setlow P, Primus G. 1975. Protein metabolism during germination of Bacillus megaterium spores. I. Protein synthesis and amino acid metabolism. J Biol Chem 250:623-630
32. Rodenberg S, Steinberg W, Piper J, Nickerson K, Vary J, Epstein R, HalvorsonHO.1968. Relationship between protein and ribonucleic acid synthesis during outgrowth of spores of Bacillus cereus. J Bacteriol 96:492-500
33. Armstrong RL, Sueoka N. 1968. Phase transitions in ribonucleic acid synthesis during germination of Bacillus subtilis spores. Proc Natl Acad Sci U S A 59:153-160. http://dx.doi.org/10.1073/pnas.59.1.153
34. Albertini AM, Galizzi A. 1975. Mutant of Bacillus subtilis with a temperature-sensitive lesion in ribonucleic acid synthesis during germination. J Bacteriol 124:14-25
35. Busta FF. 1978. Introduction to injury and repair of microbial cells. Adv Appl Microbiol 23:195-201
36. Hurst A. 1977. Bacterial injury: a review. Can J Microbiol 23:935-944. http://dx.doi.org/10.1139/m77-139
37. Feeherry FE, Munsey DT, Rowley DN. 1987. Thermal inactivation and injury of Bacillus stearothermophilus spores. Appl Environ Microbiol 53: 365-370
38. Gerhardt P, Marquis RE. 1989. Spore thermoresistance mechanisms, p 43-63. In Smith I, Slepecky RA, Setlow P (ed), Regulation of prokaryotic development. American Society for Microbiology, Washington, DC
39. 2H NMR. Biophys J 105:2016-2023. http://dx .doi.org/10.1016/j.bpj.2013.09.022
40. Sunde EP, Setlow P, Hederstedt L, Halle B. 2009. The physical state of water in bacterial spores. Proc Natl Acad Sci U S A 106:19334-19339. http://dx.doi.org/10.1073/pnas.0908712106
41. Sulthana S, Basturea GN, Deutscher MP. 2016. Elucidation of pathways of ribosomal RNA degradation: an essential role for RNase E. RNA 22: 1163-1171. http://dx.doi.org/10.1261/rna.056275.116
42. MaiväliÜ Paier A, Tenson T. 2013. When stable RNA becomes unstable: the degradation of ribosomes in bacteria and beyond. Biol Chem 394:845-855. http://dx.doi.org/10.1515/hsz-2013-0133
43. Cowan AE, Koppel DE, Setlow B, Setlow. 2003. A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proc Natl Acad Sci U S A 100:4209-4214. http://dx.doi.org/10.1073/pnas.0636762100
44. Kaga E, Nakagomi O, Uesugi S. 1992. Thermal degradation of RNARNA hybrids during hybridization in solution. Mol Cell Probes 6:261-264. http://dx.doi.org/10.1016/0890-8508(92)90026-T
45. Tenhunen J. 1989. Hydrolysis of single-stranded RNA in aqueous solutions-effect on quantitative hybridizations. Mol Cell Probes 3:391-396. http://dx.doi.org/10.1016/0890-8508(89)90018-2
46. Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu Rev Biochem 80:501-526. http://dx.doi.org/10.1146/annurev-biochem-062608-160432
47. Wang G, Zhang P, Setlow P, Li YQ. 2011. Kinetics of germination of wet-heat-treated individual spores of Bacillus species, monitored by Raman spectroscopy and differential interference contrast microscopy. Appl Environ Microbiol 77:3368-3379. http://dx.doi.org/10 .1128/AEM.00046-11
48. Atrih A, Foster SJ. 2001. In vivo roles of the germination-specific lytic enzymes of Bacillus subtilis. Microbiology 147:2925-2932. http://dx.doi .org/10.1099/00221287-147-11-2925
49. Peng L, Chen D, Setlow P, Li YQ. 2009. Elastic and inelastic light scattering from single bacterial spores in an optical trap allows the monitoring of spore germination dynamics. Anal Chem 81:4035-4042. http://dx.doi.org/10.1021/ac900250x
50. Bergman NH, Anderson EC, Swenson EE, Niemeyer MW, Miyoshi AD, Hanna PC. 2006. Transcriptional profiling of the Bacillus anthracis life cycle in vitro and an implied model for regulation of spore formation. J Bacteriol 188:6092-6100. http://dx.doi.org/10.1128/JB.00723-06
51. Keijser BJF, Ter Beek A, Rauwerda H, Schuren F, Montijn R, van der Spek H, Brul S. 2007. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J Bacteriol 189:3624-3634. http://dx.doi.org/10.1128/JB.01736-06
52. Bettegowda C, Huang X, Lin J, Cheong I, Kohli M, Szabo SA, Zhang X, Diaz LA, Jr, Velculescu VE, Parmigiani G, Kinzler KW, Vogelstein B, Zhou S. 2006. The genome and transcriptomes of the anti-tumor agent Clostridium novyi-NT. Nat Biotechnol 24:1573-1580. http://dx.doi.org/10.1038/nbt1256