σK of clostridium acetobutylicum is the first known sporulation-: Specific sigma factor with two developmentally separated roles, one early and one late in sporulation

Journal of Bacteriology

Volumn 196, Issue 2, 2014, Pages 287-299

  Jones, Mohab A Al Hinai ^a,b   Papoutsakis, Eleftherios T ^a,c  

^a UNIVERSITY OF DELAWARE   (United States)

^b SULTAN QABOOS UNIVERSITY   (Oman)

^c Elcriton Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MUTANT PROTEIN; SIGMA FACTOR;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; GROWTH CURVE; HUMAN; MICROBIAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPOROGENESIS; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84890906688     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01103-13     Document Type: Article

References (63)

1. Nolling J, Breton G, Omelchenko MV, Makarova KS, Zeng QD, Gibson R, Lee HM, Dubois J, Qiu DY, Hitti J, GTC Sequencing Center Production, Finishing, and Bioinformatics Teams, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR. 2001. Genome sequence and comparative analysis of the solventproducing bacterium Clostridium acetobutylicum. J. Bacteriol. 183:4823- 4838. http://dx.doi.org/10.1128/JB.183.16.4823-4838.2001.
2. Papoutsakis ET. 2008. Engineering solventogenic clostridia. Curr. Opin. Biotechnol. 19:420-429. http://dx.doi.org/10.1016/j.copbio.2008.08.003.
3. Lee SY, Park JH, Jang SH, Nielsen LK, Kim J, Jung KS. 2008. Fermentative butanol production by clostridia. Biotechnol. Bioeng. 101:209-228. http://dx.doi.org/10.1002/bit.22003.
4. Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET. 2012. Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr. Opin. Biotechnol. 23:364-381. http://dx.doi.org/10.1016/j.copbio.2011.10.008.
5. Steiner E, Dago AE, Young DI, Heap JT, Minton NP, Hoch JA, Young M. 2011. Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. Mol. Microbiol. 80:641-654. http://dx.doi.org/10.1111/j.1365 -2958.2011.07608.x.
6. Tracy BP, Jones SW, Papoutsakis ET. 2011. Inactivation of sigma(E) and sigma(G) in Clostridium acetobutylicum illuminates their roles in clostridial-cell-form biogenesis, granulose synthesis, solventogenesis, and spore morphogenesis. J. Bacteriol. 193:1414-1426. http://dx.doi.org/10.1128/JB.01380-10.
7. Bi CH, Jones SW, Hess DR, Tracy BP, Papoutsakis ET. 2011. SpoIIE is necessary for asymmetric division, sporulation, and expression of sigma(F), sigma(E), and sigma(G) but does not control solvent production in Clostridium acetobutylicum ATCC 824. J. Bacteriol. 193:5130-5137. http://dx.doi.org/10.1128/JB.05474-11.
8. Jones SW, Tracy BP, Gaida SM, Papoutsakis ET. 2011. Inactivation of sigma(F) in Clostridium acetobutylicum ATCC 824 blocks sporulation prior to asymmetric division and abolishes sigma(E) and sigma(G) protein expression but does not block solvent formation. J. Bacteriol. 193: 2429-2440. http://dx.doi.org/10.1128/JB.00088-11.
9. Jones SW, Paredes CJ, Tracy B, Cheng N, Sillers R, Senger RS, Papoutsakis ET. 2008. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol. 9:R114. http://dx.doi.org/10.1186 /gb-2008-9-7-r114.
10. Piggot PJ, Hilbert DW. 2004. Sporulation of Bacillus subtilis. Curr. Opin. Microbiol. 7:579-586. http://dx.doi.org/10.1016/j.mib.2004.10.001.
11. Paredes CJ, Alsaker KV, Papoutsakis ET. 2005. A comparative genomic view of clostridial sporulation and physiology. Nat. Rev. Microbiol. 3:969-978. http://dx.doi.org/10.1038/nrmicro1288.
12. Harry KH, Zhou R, Kroos L, Melville SB. 2009. Sporulation and enterotoxin (CPE) synthesis are controlled by the sporulation-specific sigma factors SigE and SigK in Clostridium perfringens. J. Bacteriol. 191:2728- 2742. http://dx.doi.org/10.1128/JB.01839-08.
13. Kirk DG, Dahlsten E, Zhang Z, Korkeala H, Lindstrom M. 2012. Involvement of Clostridium botulinum ATCC 3502 sigma factor K in early-stage sporulation. Appl. Environ. Microbiol. 78:4590-4596. http: //dx.doi.org/10.1128/AEM.00304-12.
14. Dürre P, Bohringer M, Nakotte S, Schaffer S, Thormann K, Zickner B. 2002. Transcriptional regulation of solventogenesis in Clostridium acetobutylicum. J. Mol. Microbiol. Biotechnol. 4:295-300.
15. Harris LM, Welker NE, Papoutsakis ET. 2002. Northern, morphological, and fermentation analysis of spo0A inactivation and overexpression in Clostridium acetobutylicum ATCC 824. J. Bacteriol. 184:3586-3597. http://dx.doi.org/10.1128/JB.184.13.3586-3597.2002.
16. Ravagnani A, Jennert KCB, Steiner E, Grunberg R, Jefferies JR, Wilkinson SR, Young DI, Tidswell EC, Brown DP, Youngman P, Morris JG, Young M. 2000. Spo0A directly controls the switch from acid to solvent production in solvent-forming clostridia. Mol. Microbiol. 37:1172-1185. http://dx.doi.org/10.1046/j.1365-2958.2000.02071.x.
17. Siranosian KJ, Grossman AD. 1994. Activation of spo0A transcription by sigma H is necessary for sporulation but not for competence in Bacillus subtilis. J. Bacteriol. 176:3812-3815.
18. Haldenwang WG. 1995. The sigma factors of Bacillus subtilis. Microbiol. Rev. 59:1-30.
19. de Hoon MJL, Eichenberger P, Vitkup D. 2010. Hierarchical evolution of the bacterial sporulation network. Curr. Biol. 20:R735-R745. http://dx.doi.org/10.1016/j.cub.2010.06.031.
20. Feucht A, Evans L, Errington J. 2003. Identification of sporulation genes by genome-wide analysis of the sigma(E) regulon of Bacillus subtilis. Microbiology 149:3023-3034. http://dx.doi.org/10.1099/mic.0.26413-0.
21. Li ZS, Di Donato F, Piggot PJ. 2004. Compartmentalization of gene expression during sporulation of Bacillus subtilis is compromised in mutants blocked at stage III of sporulation. J. Bacteriol. 186:2221-2223. http: //dx.doi.org/10.1128/JB.186.7.2221-2223.2003.
22. Illing N, Errington J. 1991. Genetic regulation of morphogenesis in Bacillus subtilis-roles of sigma E and sigma F in prespore engulfment. J. Bacteriol. 173:3159 -3169.
23. Kroos L, Kunkel B, Losick R. 1989. Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science 243:526-529. http://dx.doi.org/10.1126/science.2492118.
24. Cutting S, Oke V, Driks A, Losick R, Lu S, Kroos L. 1990. A forespore checkpoint for mother cell gene expression during development in B. subtilis. Cell 62:239-250. http://dx.doi.org/10.1016/0092-8674(90)90362-I.
25. Karmazyn-Campelli C, Bonamy C, Savelli B, Stragier P. 1989. Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis. Genes Dev. 3:150-157. http://dx.doi.org/10.1101/gad.3.2.150.
26. Li J, McClane BA. 2010. Evaluating the involvement of alternative sigma factors SigF and SigG in Clostridium perfringens sporulation and enterotoxin synthesis. Infect. Immun. 78:4286-4293. http://dx.doi.org/10.1128 /IAI.00528-10.
27. Farquhar R, Yudkin MD. 1988. Phenotypic and genetic characterization of mutations in the spoIVC locus of Bacillus subtilis. J. Gen. Microbiol. 134:9-17.
28. Fimlaid KA, Bond JP, Schutz KC, Putnam EE, Leung JM, Lawley TD, Shen A. 2013. Global analysis of the sporulation pathway of Clostridium difficile. PLoS Genet. 9:e1003660. http://dx.doi.org/10.1371/journal.pgen.1003660.
29. Yutin N, Galperin MY. 2013. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ. Microbiol. 15:2631-2641. http://dx.doi.org/10.1111/1462-2920.12173.
30. Al-Hinai MA, Fast AG, Papoutsakis ET. 2012. Novel system for efficient isolation of Clostridium double-crossover allelic exchange mutants enabling markerless chromosomal gene deletions and DNA integration. Appl. Environ. Microbiol. 78:8112-8121. http://dx.doi.org/10.1128/AEM.02214-12.
31. Desai RP, Papoutsakis ET. 1999. Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl. Environ. Microbiol. 65:936-945.
32. Mermelstein LD, Papoutsakis ET. 1993. In vivo methylation in Escherichia coli by the Bacillus subtilis phage phi 3T I methyltransferase to protect plasmids from restriction upon transformation of Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 59:1077-1081.
33. Mermelstein LD, Welker NE, Bennett GN, Papoutsakis ET. 1992. Expression of cloned homologous fermentative genes in Clostridium acetobutylicum ATCC 824. Biotechnology (NY) 10:190-195. http://dx.doi.org /10.1038/nbt0292-190.
34. Sillers R, Al-Hinai MA, Papoutsakis ET. 2009. Aldehyde-alcohol dehydrogenase and/or thiolase overexpression coupled with CoA transferase downregulation lead to higher alcohol titers and selectivity in Clostridium acetobutylicum fermentations. Biotechnol. Bioeng. 102:38-49. http://dx.doi.org/10.1002/bit.22058.
35. Alsaker KV, Paredes CJ, Papoutsakis ET. 2005. Design, optimization and validation of genomic DNA microarrays for examining the Clostridium acetobutylicum transcriptome. Biotechnol. Bioprocess Eng. 10:432-443. http://dx.doi.org/10.1007/BF02989826.
36. Schaeffer AB, Fulton MD. 1933. A simplified method of staining endospores. Science 77:194. http://dx.doi.org/10.1126/science.77.1990.194.
37. Tomas CA, Welker NE, Papoutsakis ET. 2003. Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell's transcriptional program. Appl. Environ. Microbiol. 69:4951-4965. http://dx.doi.org/10.1128/AEM.69.8.4951-4965.2003.
38. Paredes CJ, Senger RS, Spath IS, Borden JR, Sillers R, Papoutsakis ET. 2007. A general framework for designing and validating oligomer-based DNA microarrays and its application to Clostridium acetobutylicum. Appl. Environ. Microbiol. 73:4631-4638. http://dx.doi.org/10.1128/AEM.00144-07.
39. Smyth GK. 2005. Limma: linear models for microarray data, p 397-420. In Gentleman R, Carey V, Dudoit S, Irizarry RA, HuberW(ed), Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, NY.
40. Yang YH, Dudoit S, Luu P, Speed TP. 2001. Normalization for cDNA microarray data, p 141-152. In Bittner ML, Chen Y, Dorsel AN, Dougherty ER (ed), Proceedings of SPIE, vol 4266. Microarrays: optical technologies and informatics. SPIE, Bellingham, WA.
41. Maddox IS, Steiner E, Hirsch S, Wessner S, Gutierrez NA, Gapes JR, Schuster KC. 2000. The cause of "acid-crash" and "acidogenic fermentations" during the batch acetone-butanol-ethanol (ABE-) fermentation process. J. Mol. Microbiol. Biotechnol. 2:95-100.
42. Wu JJ, Howard MG, Piggot PJ. 1989. Regulation of transcription of the Bacillus subtilis spoIIA locus. J. Bacteriol. 171:692-698.
43. Saujet L, Monot M, Dupuy B, Soutourina O, Martin-Verstraete I. 2011. The key sigma factor of transition phase, SigH, controls sporulation, metabolism, and virulence factor expression in Clostridium difficile. J. Bacteriol. 193:3186-3196. http://dx.doi.org/10.1128/JB.00272-11.
44. Fujita M, Gonzalez-Pastor JE, Losick R. 2005. High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J. Bacteriol. 187:1357- 1368. http://dx.doi.org/10.1128/JB.187.4.1357-1368.2005.
45. Tomas CA, Alsaker KV, Bonarius HPJ, Hendriksen WT, Yang H, Beamish JA, Paredes CJ, Papoutsakis ET. 2003. DNA array-based transcriptional analysis ofasporogenous,nonsolventogenic Clostridium acetobutylicum strains SKO1 and M5. J. Bacteriol. 185:4539-4547. http://dx.doi.org/10.1128/JB.185.15.4539-4547.2003.
46. Dürre P. 2005. Handbook on clostridia. Taylor&Francis, Boca Raton, FL.
47. Fischer RJ, Helms J, Durre P. 1993. Cloning, sequencing, and molecular analysis of the sol operon of Clostridium acetobutylicum, a chromosomal locus involved in solventogenesis. J. Bacteriol. 175:6959 - 6969.
48. Petersen DJ, Cary JW, Vanderleyden J, Bennett GN. 1993. Sequence and arrangement of genes encoding enzymes of the acetone-production pathway of Clostridium acetobutylicum ATCC824. Gene 123:93-97. http://dx.doi.org/10.1016/0378-1119(93)90545-E.
49. Nair RV, Bennett GN, Papoutsakis ET. 1994. Molecular characterization of an aldehyde/alcohol dehydrogenase gene from Clostridium acetobutylicum ATCC-824. J. Bacteriol. 176:871-885.
50. Nair RV, Papoutsakis ET. 1994. Expression of plasmid-encoded Aad in Clostridium acetobutylicum M5 restores vigorous butanol production. J. Bacteriol. 176:5843-5846.
51. Jones SW. 2011. Elucidating the transcriptional regulation of sporulation in Clostridium acetobutylicum. Ph.D. thesis. Northwestern University, Evanston, IL.
52. Tummala SB, Welker NE, Papoutsakis ET. 1999. Development and characterization of a gene expression reporter system for Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 65:3793-3799.
53. Cornillot E, Nair RV, Papoutsakis ET, Soucaille P. 1997. The genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 reside on a large plasmid whose loss leads to degeneration of the strain. J. Bacteriol. 179:5442-5447.
54. Alsaker KV, Spitzer TR, Papoutsakis ET. 2004. Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. J. Bacteriol. 186:1959-1971. http://dx.doi.org/10.1128/JB.186.7.1959-1971.2004.
55. Takamatsu H, Chikahiro Y, Kodama T, Koide H, Kozuka S, Tochikubo K, Watabe K. 1998. A spore coat protein, CotS, of Bacillus subtilis is synthesized under the regulation of sigma(K) and GerE during development and is located in the inner coat layer of spores. J. Bacteriol. 180: 2968-2974.
56. Takamatsu H, Kodama T, Imamura A, Asai K, Kobayashi K, Nakayama T, Ogasawara N, Watabe K. 2000. The Bacillus subtilis yabG gene is transcribed by SigK RNA polymerase during sporulation, and yabG mutant spores have altered coat protein composition. J. Bacteriol. 182:1883- 1888. http://dx.doi.org/10.1128/JB.182.7.1883-1888.2000.
57. Santangelo JD, Kuhn A, Treuner-Lange A, Durre P. 1998. Sporulation and time course expression of sigma-factor homologous genes in Clostridium acetobutylicum. FEMS Microbiol. Lett. 161:157-164. http://dx.doi.org/10.1111/j.1574-6968.1998.tb12943.x.
58. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeno-Tarrraga AM, Wang HW, Holden MTG, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrugresistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38:779-786. http://dx.doi.org/10.1038/ng1830.
59. Veening JW, Smits WK, Kuipers OP. 2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62:193-210. http://dx.doi.org/10.1146/annurev.micro.62.081307.163002.
60. Veening JW, Stewart EJ, Berngruber TW, Taddei F, Kuipers OP, Hamoen LW. 2008. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl. Acad. Sci. U. S. A. 105:4393-4398. http://dx.doi.org/10.1073/pnas.0700463105.
61. Chary VK, Meloni M, Hilbert DW, Piggot PJ. 2005. Control of the expression and compartmentalization of sigma(G) activity during sporulation of Bacillus subtilis by regulators of sigma(F) and sigma(E). J. Bacteriol. 187: 6832-6840. http://dx.doi.org/10.1128/JB.187.19.6832-6840.2005.
62. Tracy BP, Gaida SM, Papoutsakis ET. 2008. Development and application of flow-cytometric techniques for analyzing and sorting endosporeforming clostridia. Appl. Environ. Microbiol. 74:7497-7506. http://dx.doi.org/10.1128/AEM.01626-08.
63. Ferrell JE. 2002. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr. Opin. Cell Biol. 14:140-148. http://dx.doi.org/10.1016/S0955-0674(02)00314-9.