The Transcriptional Program Underlying the Physiology of Clostridial Sporulation

Overview

Journal Genome Biol

Specialties Biology
Genetics

Date 2008 Jul 18

PMID 18631379

Citations 73

Authors

Shawn W Jones

Carlos J Paredes

Bryan Tracy

Nathan Cheng

Ryan Sillers

Ryan S Senger

Eleftherios T Papoutsakis

Affiliations

Soon will be listed here.

Abstract

Background: Clostridia are ancient soil organisms of major importance to human and animal health and physiology, cellulose degradation, and the production of biofuels from renewable resources. Elucidation of their sporulation program is critical for understanding important clostridial programs pertaining to their physiology and their industrial or environmental applications.

Results: Using a sensitive DNA-microarray platform and 25 sampling timepoints, we reveal the genome-scale transcriptional basis of the Clostridium acetobutylicum sporulation program carried deep into stationary phase. A significant fraction of the genes displayed temporal expression in six distinct clusters of expression, which were analyzed with assistance from ontological classifications in order to illuminate all known physiological observations and differentiation stages of this industrial organism. The dynamic orchestration of all known sporulation sigma factors was investigated, whereby in addition to their transcriptional profiles, both in terms of intensity and differential expression, their activity was assessed by the average transcriptional patterns of putative canonical genes of their regulon. All sigma factors of unknown function were investigated by combining transcriptional data with predicted promoter binding motifs and antisense-RNA downregulation to provide a preliminary assessment of their roles in sporulation. Downregulation of two of these sigma factors, CAC1766 and CAP0167, affected the developmental process of sporulation and are apparently novel sporulation-related sigma factors.

Conclusion: This is the first detailed roadmap of clostridial sporulation, the most detailed transcriptional study ever reported for a strict anaerobe and endospore former, and the first reported holistic effort to illuminate cellular physiology and differentiation of a lesser known organism.

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References

Perret S, Maamar H, Belaich J, Tardif C . Use of antisense RNA to modify the composition of cellulosomes produced by Clostridium cellulolyticum. Mol Microbiol. 2004; 51(2):599-607. DOI: 10.1046/j.1365-2958.2003.03860.x. View

Bourne N, FITZJAMES P, Aronson A . Structural and germination defects of Bacillus subtilis spores with altered contents of a spore coat protein. J Bacteriol. 1991; 173(20):6618-25. PMC: 209000. DOI: 10.1128/jb.173.20.6618-6625.1991. View

Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N . TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003; 34(2):374-8. DOI: 10.2144/03342mt01. View

Long S, Jones D, Woods D . Sporulation of Clostridium acetobutylicum P262 in a Defined Medium. Appl Environ Microbiol. 1983; 45(4):1389-93. PMC: 242467. DOI: 10.1128/aem.45.4.1389-1393.1983. View

Sands J, Montenecourt B . Effect of butanol on lipid composition and fluidity of Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol. 1984; 47(1):193-4. PMC: 239634. DOI: 10.1128/aem.47.1.193-194.1984. View

Green E, Boynton Z, Harris L, Rudolph F, Papoutsakis E, Bennett G . Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology (Reading). 1996; 142 ( Pt 8):2079-86. DOI: 10.1099/13500872-142-8-2079. View

Kodama T, Takamatsu H, Asai K, Kobayashi K, Ogasawara N, Watabe K . The Bacillus subtilis yaaH gene is transcribed by SigE RNA polymerase during sporulation, and its product is involved in germination of spores. J Bacteriol. 1999; 181(15):4584-91. PMC: 103590. DOI: 10.1128/JB.181.15.4584-4591.1999. View

Cornillot E, Nair R, Papoutsakis E, Soucaille P . 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. 1997; 179(17):5442-7. PMC: 179415. DOI: 10.1128/jb.179.17.5442-5447.1997. View

Wang S, Setlow B, Conlon E, Lyon J, Imamura D, Sato T . The forespore line of gene expression in Bacillus subtilis. J Mol Biol. 2006; 358(1):16-37. DOI: 10.1016/j.jmb.2006.01.059. View

10.

Frey M . Hydrogenases: hydrogen-activating enzymes. Chembiochem. 2002; 3(2-3):153-60. DOI: 10.1002/1439-7633(20020301)3:2/3<153::AID-CBIC153>3.0.CO;2-B. View

11.

Perego M, Spiegelman G, Hoch J . Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol Microbiol. 1988; 2(6):689-99. DOI: 10.1111/j.1365-2958.1988.tb00079.x. View

12.

Takamatsu H, Watabe K . Assembly and genetics of spore protective structures. Cell Mol Life Sci. 2002; 59(3):434-44. PMC: 11337453. DOI: 10.1007/s00018-002-8436-4. View

13.

Mansilla M, Cybulski L, Albanesi D, de Mendoza D . Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol. 2004; 186(20):6681-8. PMC: 522199. DOI: 10.1128/JB.186.20.6681-6688.2004. View

14.

Makino S, Moriyama R . Hydrolysis of cortex peptidoglycan during bacterial spore germination. Med Sci Monit. 2002; 8(6):RA119-27. View

15.

Tummala S, Junne S, Papoutsakis E . Antisense RNA downregulation of coenzyme A transferase combined with alcohol-aldehyde dehydrogenase overexpression leads to predominantly alcohologenic Clostridium acetobutylicum fermentations. J Bacteriol. 2003; 185(12):3644-53. PMC: 156216. DOI: 10.1128/JB.185.12.3644-3653.2003. View

16.

Kaan T, Homuth G, Mader U, Bandow J, Schweder T . Genome-wide transcriptional profiling of the Bacillus subtilis cold-shock response. Microbiology (Reading). 2002; 148(Pt 11):3441-3455. DOI: 10.1099/00221287-148-11-3441. View

17.

Paredes C, Rigoutsos I, Terry Papoutsakis E . Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res. 2004; 32(6):1973-81. PMC: 390361. DOI: 10.1093/nar/gkh509. View

18.

Baer S, Blaschek H, Smith T . Effect of Butanol Challenge and Temperature on Lipid Composition and Membrane Fluidity of Butanol-Tolerant Clostridium acetobutylicum. Appl Environ Microbiol. 1987; 53(12):2854-61. PMC: 204212. DOI: 10.1128/aem.53.12.2854-2861.1987. View

19.

Alsaker K, Spitzer T, Papoutsakis E . Transcriptional analysis of spo0A overexpression in Clostridium acetobutylicum and its effect on the cell's response to butanol stress. J Bacteriol. 2004; 186(7):1959-71. PMC: 374416. DOI: 10.1128/JB.186.7.1959-1971.2004. View

20.

Peguin S, Soucaille P . Modulation of Carbon and Electron Flow in Clostridium acetobutylicum by Iron Limitation and Methyl Viologen Addition. Appl Environ Microbiol. 1995; 61(1):403-5. PMC: 1388339. DOI: 10.1128/aem.61.1.403-405.1995. View