Phosphoproteome dynamics mediate revival of bacterial spores

BMC Biology

Volumn 13, Issue 1, 2015, Pages

  Rosenberg, Alex ^a   Soufi, Boumediene ^b   Ravikumar, Vaishnavi ^b   Soares, Nelson C ^b   Krug, Karsten ^b   Smith, Yoav ^c   Macek, Boris ^b   Ben Yehuda, Sigal ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c HEBREW UNIVERSITY   (Israel)

Author keywords

Bacillus subtilis; Germination; Phosphoproteome; Spore

Indexed keywords

BACTERIAL PROTEIN; PROTEOME;

BACILLUS SUBTILIS; BACTERIAL SPORE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; PHOSPHORYLATION; PROTEOME; SPORES, BACTERIAL;

EID: 84941654505     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-015-0184-7     Document Type: Article

References (75)

1. Setlow P. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol. 2006;101:514-25. doi: 10.1111/j.1365-2672.2005.02736.x .
2. Piggot PJ, Hilbert DW. Sporulation of Bacillus subtilis. Curr Opin Microbiol. 2004;7:579-86. doi: 10.1016/j.mib.2004.10.001 .
3. Higgins D, Dworkin J. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev. 2012;36:131-48. doi: 10.1111/j.1574-6976.2011.00310.x .
4. Driks A. Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol. 2002;10:251-4.
5. Beaman TC, Gerhardt P. Heat resistance of bacterial spores correlated with protoplast dehydration, mineralization, and thermal adaptation. Appl Environ Microbiol. 1986;52:1242-6.
6. Gerhardt P, Marquis R. Spore thermoresistance mechanisms. In: Smith I, Slepecky R, Setlow P, editors. Regulation of prokaryotic development. Washington, DC: American Society for Microbiology; 1989. p. 43-63.
7. McKenney PT, Driks A, Eichenberger P. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol. 2013;11:33-44. doi: 10.1038/nrmicro2921 .
8. Setlow P. Summer meeting 2013 - when the sleepers wake: the germination of spores of Bacillus species. J Appl Microbiol. 2013;115:1251-68. doi: 10.1111/jam.12343 .
9. Setlow P. Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function, and degradation. Annu Rev Microbiol. 1988;42:319-38. doi: 10.1146/annurev.mi.42.100188.001535 .
10. Mohr SC, Sokolov NV, He CM, Setlow P. Binding of small acid-soluble spore proteins from Bacillus subtilis changes the conformation of DNA from B to A. Proc Natl Acad Sci U S A. 1991;88:77-81.
11. Nicholson WL, Setlow B, Setlow P. Ultraviolet irradiation of DNA complexed with alpha/beta-type small, acid-soluble proteins from spores of Bacillus or Clostridium species makes spore photoproduct but not thymine dimers. Proc Natl Acad Sci U S A. 1991;88:8288-92.
12. Setlow B, Setlow P. Absence of transient elevated UV resistance during germination of Bacillus subtilis spores lacking small, acid-soluble spore proteins alpha and beta. J Bacteriol. 1988;170:2858-9.
13. Setlow P. I will survive: DNA protection in bacterial spores. Trends Microbiol. 2007;15:172-80. doi: 10.1016/j.tim.2007.02.004 .
14. Shah IM, Laaberki MH, Popham DL, Dworkin J. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell. 2008;135:486-96. doi: 10.1016/j.cell.2008.08.039 .
15. Sinai L, Rosenberg A, Smith Y, Segev E, Ben-Yehuda S. The molecular timeline of a reviving bacterial spore. Mol Cell. 2015;57:695-707. doi: 10.1016/j.molcel.2014.12.019 .
16. Paidhungat M, Setlow P. Spore germination and outgrowth. In: Hoch J, Losick R, Sonenshein A, editors. Bacillus subtilis and its relatives: from genes to cells. Washington, DC: ASM Press; 2002. p. 537-48.
17. Segev E, Rosenberg A, Mamou G, Sinai L, Ben-Yehuda S. Molecular kinetics of reviving bacterial spores. J Bacteriol. 2013;195:1875-82. doi: 10.1128/JB.00093-13 .
18. Campos SS, Ibarra-Rodriguez JR, Barajas-Ornelas RC, Ramirez-Guadiana FH, Obregon-Herrera A, Setlow P, et al. Interaction of apurinic/apyrimidinic endonucleases Nfo and ExoA with the DNA integrity scanning protein DisA in the processing of oxidative DNA damage during bacillus subtilis spore outgrowth. J Bacteriol. 2014;196:568-78. doi: 10.1128/JB.01259-13 .
19. Mehne FM, Schroder-Tittmann K, Eijlander RT, Herzberg C, Hewitt L, Kaever V, et al. Control of the diadenylate cyclase CdaS in Bacillus subtilis: an autoinhibitory domain limits cyclic di-AMP production. J Biol Chem. 2014;289:21098-107. doi: 10.1074/jbc.M114.562066 .
20. Setlow P, Kornberg A. Biochemical studies of bacterial sporulation and germination. XXII. Energy metabolism in early stages of germination of Bacillus megaterium spores. J Biol Chem. 1970;245:3637-44.
21. Setlow P, Kornberg A. Biochemical studies of bacterial sporulation and germination. 23. Nucleotide metabolism during spore germination. J Biol Chem. 1970;245:3645-52.
22. Setlow P, Primus G. Protein metabolism during germination of Bacillus megaterium spores. I. Protein synthesis and amino acid metabolism. J Biol Chem. 1975;250:623-30.
23. Kobir A, Shi L, Boskovic A, Grangeasse C, Franjevic D, Mijakovic I. Protein phosphorylation in bacterial signal transduction. Biochim Biophys Acta. 2011;1810:989-94. doi: 10.1016/j.bbagen.2011.01.006 .
24. Paleckova P, Kontrova F, Kofronova O, Bobek J, Benada O, Mikulik K. Effect of protein kinase inhibitors on protein phosphorylation and germination of aerial spores from Streptomyces coelicolor. Folia Microbiol (Praha). 2007;52:215-22.
25. Setlow P. Spore germination. Curr Opin Microbiol. 2003;6:550-6.
26. Kong L, Zhang P, Wang G, Yu J, Setlow P, Li YQ. Characterization of bacterial spore germination using phase-contrast and fluorescence microscopy, Raman spectroscopy and optical tweezers. Nat Protoc. 2011;6:625-39. doi: 10.1038/nprot.2011.307 .
27. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26:1367-72. doi: 10.1038/nbt.1511 .
28. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794-805. doi: 10.1021/pr101065j .
29. Macek B, Mijakovic I, Olsen JV, Gnad F, Kumar C, Jensen PR, et al. The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics. 2007;6:697-707. doi: 10.1074/mcp.M600464-MCP200 .
30. Ravikumar V, Shi L, Krug K, Derouiche A, Jers C, Cousin C, et al. Quantitative phosphoproteome analysis of Bacillus subtilis reveals novel substrates of the kinase PrkC and phosphatase PrpC. Mol Cell Proteomics. 2014;13:1965-78. doi: 10.1074/mcp.M113.035949 .
31. Elsholz AK, Turgay K, Michalik S, Hessling B, Gronau K, Oertel D, et al. Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc Natl Acad Sci U S A. 2012;109:7451-6. doi: 10.1073/pnas.1117483109 .
32. Schmidt A, Trentini DB, Spiess S, Fuhrmann J, Ammerer G, Mechtler K, et al. Quantitative phosphoproteomics reveals the role of protein arginine phosphorylation in the bacterial stress response. Mol Cell Proteomics. 2014;13:537-50. doi: 10.1074/mcp.M113.032292 .
33. Eymann C, Becher D, Bernhardt J, Gronau K, Klutzny A, Hecker M. Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. Proteomics. 2007;7:3509-26. doi: 10.1002/pmic.200700232 .
34. Soufi B, Kumar C, Gnad F, Mann M, Mijakovic I, Macek B. Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis. J Proteome Res. 2010;9:3638-46. doi: 10.1021/pr100150w .
35. Levine A, Vannier F, Absalon C, Kuhn L, Jackson P, Scrivener E, et al. Analysis of the dynamic Bacillus subtilis Ser/Thr/Tyr phosphoproteome implicated in a wide variety of cellular processes. Proteomics. 2006;6:2157-73. doi: 10.1002/pmic.200500352 .
36. Sharma K, D'Souza RC, Tyanova S, Schaab C, Wisniewski JR, Cox J, et al. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014;8:1583-94. doi: 10.1016/j.celrep.2014.07.036 .
37. Dephoure N, Gould KL, Gygi SP, Kellogg DR. Mapping and analysis of phosphorylation sites: a quick guide for cell biologists. Mol Biol Cell. 2013;24:535-42. doi: 10.1091/mbc.E12-09-0677 .
38. Arnaud M, Chastanet A, Debarbouille M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol. 2004;70:6887-91. doi: 10.1128/AEM.70.11.6887-6891.2004 .
39. Mason JM, Setlow P. Different small, acid-soluble proteins of the alpha/beta type have interchangeable roles in the heat and UV radiation resistance of Bacillus subtilis spores. J Bacteriol. 1987;169:3633-7.
40. Lee KS, Bumbaca D, Kosman J, Setlow P, Jedrzejas MJ. Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proc Natl Acad Sci U S A. 2008;105:2806-11. doi: 10.1073/pnas.0708244105 .
41. Mason JM, Setlow P. Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light. J Bacteriol. 1986;167:174-8.
42. Hayes CS, Setlow P. An alpha/beta-type, small, acid-soluble spore protein which has very high affinity for DNA prevents outgrowth of Bacillus subtilis spores. J Bacteriol. 2001;183:2662-6. doi: 10.1128/JB.183.8.2662-2666.2001 .
43. Kosman J, Setlow P. Effects of carboxy-terminal modifications and pH on binding of a Bacillus subtilis small, acid-soluble spore protein to DNA. J Bacteriol. 2003;185:6095-103.
44. Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell. 2000;102:615-23.
45. Wei Y, Bechhofer DH. Tetracycline induces stabilization of mRNA in Bacillus subtilis. J Bacteriol. 2002;184:889-94.
46. Akanuma G, Suzuki S, Yano K, Nanamiya H, Natori Y, Namba E, et al. Single mutations introduced in the essential ribosomal proteins L3 and S10 cause a sporulation defect in Bacillus subtilis. J Gen Appl Microbiol. 2013;59:105-17.
47. Deutscher J, Ake FM, Derkaoui M, Zebre AC, Cao TN, Bouraoui H, et al. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev. 2014;78:231-56. doi: 10.1128/MMBR.00001-14 .
48. Postma PW, Lengeler JW, Jacobson GR. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev. 1993;57:543-94.
49. Fujita Y, Miwa Y, Galinier A, Deutscher J. Specific recognition of the Bacillus subtilis gnt cis-acting catabolite-responsive element by a protein complex formed between CcpA and seryl-phosphorylated HPr. Mol Microbiol. 1995;17:953-60.
50. Pietack N, Becher D, Schmidl SR, Saier MH, Hecker M, Commichau FM, et al. In vitro phosphorylation of key metabolic enzymes from Bacillus subtilis: PrkC phosphorylates enzymes from different branches of basic metabolism. J Mol Microbiol Biotechnol. 2010;18:129-40. doi: 10.1159/000308512 .
51. Deutscher J, Reizer J, Fischer C, Galinier A, Saier Jr MH, Steinmetz M. Loss of protein kinase-catalyzed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J Bacteriol. 1994;176:3336-44.
52. Galinier A, Haiech J, Kilhoffer MC, Jaquinod M, Stulke J, Deutscher J, et al. The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression. Proc Natl Acad Sci U S A. 1997;94:8439-44.
53. Martin-Verstraete I, Deutscher J, Galinier A. Phosphorylation of HPr and Crh by HprK, early steps in the catabolite repression signalling pathway for the Bacillus subtilis levanase operon. J Bacteriol. 1999;181:2966-9.
54. Singh KD, Schmalisch MH, Stulke J, Gorke B. Carbon catabolite repression in Bacillus subtilis: quantitative analysis of repression exerted by different carbon sources. J Bacteriol. 2008;190:7275-84. doi: 10.1128/JB.00848-08 .
55. Stulke J, Hillen W. Regulation of carbon catabolism in Bacillus species. Annu Rev Microbiol. 2000;54:849-80. doi: 10.1146/annurev.micro.54.1.849 .
56. Bidnenko V, Shi L, Kobir A, Ventroux M, Pigeonneau N, Henry C, et al. Bacillus subtilis serine/threonine protein kinase YabT is involved in spore development via phosphorylation of a bacterial recombinase. Mol Microbiol. 2013;88:921-35. doi: 10.1111/mmi.12233 .
57. Schmidl SR, Gronau K, Pietack N, Hecker M, Becher D, Stulke J. The phosphoproteome of the minimal bacterium Mycoplasma pneumoniae: analysis of the complete known Ser/Thr kinome suggests the existence of novel kinases. Mol Cell Proteomics. 2010;9:1228-42. doi: 10.1074/mcp.M900267-MCP200 .
58. Hansen AM, Chaerkady R, Sharma J, Diaz-Mejia JJ, Tyagi N, Renuse S, et al. The Escherichia coli phosphotyrosine proteome relates to core pathways and virulence. PLoS Pathog. 2013;9:e1003403. doi: 10.1371/journal.ppat.1003403 .
59. Perego M, Hoch JA. Two-component systems, phosphorelays, and regulation of their activities by phosphatases. In: Sonenshein A, Hoch J, Losick R, editors. Bacillus subtilis and its closest relatives: from genes to cells. Washington, DC: ASM Press; 2002. p. 473-81.
60. Zu XL, Besant PG, Imhof A, Attwood PV. Mass spectrometric analysis of protein histidine phosphorylation. Amino Acids. 2007;32:347-57. doi: 10.1007/s00726-007-0493-4 .
61. Gould G. Germination. In: Gould G, Hurst A, editors. The bacterial spore. London: Academic Press; 1969. p. 397-444.
62. Halvorson HO, Vary JC, Steinberg W. Developmental changes during the formation and breaking of the dormant state in bacteria. Annu Rev Microbiol. 1966;20:169-88. doi: 10.1146/annurev.mi.20.100166.001125 .
63. Hayes CS, Alarcon-Hernandez E, Setlow P. N-terminal amino acid residues mediate protein-protein interactions between DNA-bound alpha/beta-type small, acid-soluble spore proteins from Bacillus species. J Biol Chem. 2001;276:2267-75. doi: 10.1074/jbc.M007858200 .
64. Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol. 2004;5:827-35. doi: 10.1038/nrm1488 .
65. Mikulik K, Bobek J, Zikova A, Smetakova M, Bezouskova S. Phosphorylation of ribosomal proteins influences subunit association and translation of poly (U) in Streptomyces coelicolor. Mol Biosyst. 2011;7:817-23. doi: 10.1039/c0mb00174k .
66. Keijser BJ, Ter Beek A, Rauwerda H, Schuren F, Montijn R, van der Spek H, et al. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J Bacteriol. 2007;189:3624-34. doi: 10.1128/JB.01736-06 .
67. Hageman JH, Shankweiler GW, Wall PR, Franich K, McCowan GW, Cauble SM, et al. Single, chemically defined sporulation medium for Bacillus subtilis: growth, sporulation, and extracellular protease production. J Bacteriol. 1984;160:438-41.
68. Pelczar PL, Igarashi T, Setlow B, Setlow P. Role of GerD in germination of Bacillus subtilis spores. J Bacteriol. 2007;189:1090-8. doi: 10.1128/JB.01606-06 .
69. Ishihama Y, Rappsilber J, Mann M. Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics. J Proteome Res. 2006;5:988-94. doi: 10.1021/pr050385q .
70. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, et al. Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics. 2008;7:299-307. doi: 10.1074/mcp.M700311-MCP200 .
71. Hahne H, Mader U, Otto A, Bonn F, Steil L, Bremer E, et al. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J Bacteriol. 2010;192:870-82. doi: 10.1128/JB.01106-09 .
72. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics. 2005;4:2010-21. doi: 10.1074/mcp.T500030-MCP200 .
73. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57. doi: 10.1038/nprot.2008.211 .
74. Michna RH, Commichau FM, Todter D, Zschiedrich CP, Stulke J. SubtiWiki-a database for the model organism Bacillus subtilis that links pathway, interaction and expression information. Nucleic Acids Res. 2014;42:D692-8. doi: 10.1093/nar/gkt1002 .
75. Vasantha N, Freese E. Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides. J Bacteriol. 1980;144:1119-25.