Home LiteratureArticle Details
PMID: 9352926 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Characterization of anaerobic fermentative growth of Bacillus subtilis: identification of fermentation end products and genes required for growth.

Journal of bacteriology ·Vol. 179 ·No. 21 ·1997-11-00 ·Pages 6749-55

Nakano MM, Dailly YP, Zuber P, Clark DP

Abstract

Bacillus subtilis can grow anaerobically by respiration with nitrate as a terminal electron acceptor. In the absence of external electron acceptors, it grows by fermentation. Identification of fermentation products by using in vivo nuclear magnetic resonance scans of whole cultures indicated that B. subtilis grows by mixed acid-butanediol fermentation but that no formate is produced. An ace mutant that lacks pyruvate dehydrogenase (PDH) activity was unable to grow anaerobically and produced hardly any fermentation product. These results suggest that PDH is involved in most or all acetyl coenzyme A production in B. subtilis under anaerobic conditions, unlike Escherichia coli, which uses pyruvate formate lyase. Nitrate respiration was previously shown to require the ResDE two-component signal transduction system and an anaerobic gene regulator, FNR. Also required are respiratory nitrate reductase, encoded by the narGHJI operon, and moaA, involved in biosynthesis of a molybdopterin cofactor of nitrate reductase. The resD and resDE mutations were shown to moderately affect fermentation, but nitrate reductase activity and fnr are dispensable for fermentative growth. A search for genes involved in fermentation indicated that ftsH is required, and is also needed to a lesser extent for nitrate respiration. These results show that nitrate respiration and fermentation of B. subtilis are governed by divergent regulatory pathways.

MeSH Terms
ATP-Dependent Proteases Acetates/analysis Amino Acids/metabolism Anaerobiosis Bacillus subtilis/genetics,growth & development,metabolism Bacterial Proteins/genetics Electron Transport Escherichia coli Proteins Ethanol/analysis Fermentation Gene Expression Regulation, Bacterial Glucose/metabolism Lactates/analysis Magnetic Resonance Spectroscopy Membrane Proteins/genetics Mutation Nitrate Reductase Nitrate Reductases/genetics Nitrates/metabolism Pyruvic Acid/metabolism
Chemicals
Acetates Amino Acids Bacterial Proteins Escherichia coli Proteins Lactates Membrane Proteins Nitrates Ethanol Pyruvic Acid Nitrate Reductases Nitrate Reductase ATP-Dependent Proteases FtsH protein, E coli Glucose
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Nakano M M
Department of Biochemistry and Molecular Biology, Louisiana State University Medical Center, Shreveport 71130-3932, USA. [email protected]
Dailly Y P
Zuber P
Clark D P
References (30)
30 references, click to expand
  1. Oxygen-controlled regulation of the flavohemoglobin gene in Bacillus subtilis.
    J Bacteriol. 1996 Jul;178(13):3803-8 PMID: 8682784
  2. Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis.
    J Bacteriol. 1996 Jul;178(13):3796-802 PMID: 8682783
  3. Characterization of the ftsH gene of Bacillus subtilis.
    Microbiology. 1997 Mar;143 ( Pt 3):971-8 PMID: 9084181
  4. Regulation of pyruvate dehydrogenase activity in Escherichia coli K12.
    Biochim Biophys Acta. 1966 Aug 10;122(2):355-8 PMID: 4291045
  5. Growth and sporulation of Bacillus subtilis mutants blocked in the pyruvate dehydrogenase complex.
    J Bacteriol. 1969 Sep;99(3):745-56 PMID: 4984174
  6. Role of pyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme during growth and sporulation of Bacillus subtilis.
    J Biol Chem. 1973 Sep 10;248(17):6062-70 PMID: 4146915
  7. Proton correlation nuclear magnetic resonance study of anaerobic metabolism of Escherichia coli.
    Biochemistry. 1978 Oct 31;17(22):4742-5 PMID: 365221
  8. Proton correlation nuclear magnetic resonance study of metabolic regulations and pyruvate transport in anaerobic Escherichia coli cells.
    Biochemistry. 1980 Aug 5;19(16):3684-91 PMID: 6996710
  9. Mutants of Escherichia coli K12 with defects in anaerobic pyruvate metabolism.
    J Gen Microbiol. 1981 May;124(1):35-42 PMID: 7033467
  10. Homology between CAP and Fnr, a regulator of anaerobic respiration in Escherichia coli.
    J Mol Biol. 1983 May 15;166(2):241-7 PMID: 6343617
  11. Wild-type and mutant forms of the pyruvate dehydrogenase multienzyme complex from Bacillus subtilis.
    Biochem J. 1983 May 1;211(2):463-72 PMID: 6409095
  12. Anaerobic fermentation balance of Escherichia coli as observed by in vivo nuclear magnetic resonance spectroscopy.
    J Bacteriol. 1989 Nov;171(11):6213-7 PMID: 2681156
  13. The fermentation pathways of Escherichia coli.
    FEMS Microbiol Rev. 1989 Sep;5(3):223-34 PMID: 2698228
  14. Effect of positive redox potentials (greater than +400 mV) on the expression of anaerobic respiratory enzymes in Escherichia coli.
    Mol Microbiol. 1990 Feb;4(2):315-9 PMID: 2187148
  15. Involvement of pyruvate dehydrogenase in product formation in pyruvate-limited anaerobic chemostat cultures of Enterococcus faecalis NCTC 775.
    Arch Microbiol. 1990;154(1):50-5 PMID: 2118752
  16. Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria.
    Annu Rev Genet. 1991;25:361-87 PMID: 1812811
  17. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression.
    J Bacteriol. 1993 Mar;175(5):1344-51 PMID: 8444796
  18. Topology and subcellular localization of FtsH protein in Escherichia coli.
    J Bacteriol. 1993 Mar;175(5):1352-7 PMID: 8444797
  19. Properties of FNR proteins substituted at each of the five cysteine residues.
    Mol Microbiol. 1993 Apr;8(1):61-8 PMID: 8497198
  20. Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon.
    J Bacteriol. 1993 Aug;175(15):4605-14 PMID: 8335620
  21. A role for iron in transcriptional activation by FNR.
    FEBS Lett. 1993 Aug 23;329(1-2):55-8 PMID: 8354409
  22. Molecular genetic analysis of the moa operon of Escherichia coli K-12 required for molybdenum cofactor biosynthesis.
    Mol Microbiol. 1993 Jun;8(6):1071-81 PMID: 8361352
  23. Pyruvate formate-lyase is not essential for nitrate respiration by Escherichia coli.
    FEMS Microbiol Lett. 1994 Apr 1;117(2):163-8 PMID: 8181719
  24. Identification and isolation of a gene required for nitrate assimilation and anaerobic growth of Bacillus subtilis.
    J Bacteriol. 1995 Feb;177(4):1112-5 PMID: 7860592
  25. The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshift.
    J Bacteriol. 1995 Jul;177(14):4105-12 PMID: 7608085
  26. The anaerobic life of Bacillus subtilis: cloning of the genes encoding the respiratory nitrate reductase system.
    FEMS Microbiol Lett. 1995 Sep 1;131(2):219-25 PMID: 7557333
  27. Systematic sequencing of the 180 kilobase region of the Bacillus subtilis chromosome containing the replication origin.
    DNA Res. 1994;1(1):1-14 PMID: 7584024
  28. Anaerobic transcription activation in Bacillus subtilis: identification of distinct FNR-dependent and -independent regulatory mechanisms.
    EMBO J. 1995 Dec 1;14(23):5984-94 PMID: 8846791
  29. Regulators of aerobic and anaerobic respiration in Bacillus subtilis.
    J Bacteriol. 1996 Mar;178(5):1374-85 PMID: 8631715
  30. The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion.
    Mol Microbiol. 1997 Mar;23(5):921-33 PMID: 9076729
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1997-11-00
Pages
6749-55
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC179605
Subset
IM
Grants
NIGMS NIH HHS · GM45898 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]