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Anaerobic Growth of a “Strict Aerobe” (Bacillus Subtilis)

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Anaerobic Growth of a “Strict Aerobe” (Bacillus Subtilis) P1: ARS/ary P2: ARS/dat QC: ARS August 7, 1998 11:39 Annual Reviews AR063-06 Annu. Rev. Microbiol. 1998. 52:165–90 Copyright c 1998 by Annual Reviews. All rights reserved ANAEROBIC GROWTH OF A “STRICT AEROBE” (BACILLUS SUBTILIS) Michiko M. Nakano and Peter Zuber Department of Biochemistry and Molecular Biology, Louisiana State University Medical Center, Shreveport, Louisiana 71130-3932; e-mail: [email protected]; [email protected] KEY WORDS: anaerobiosis, nitrate respiration, fermentation, gene regulation ABSTRACT There was a long-held belief that the gram-positive soil bacterium Bacillus sub- tilis is a strict aerobe. But recent studies have shown that B. subtilis will grow anaerobically, either by using nitrate or nitrite as a terminal electron acceptor, or by fermentation. How B. subtilis alters its metabolic activity according to the availability of oxygen and alternative electron acceptors is but one focus of study. A two-component signal transduction system composed of a sensor kinase, ResE, and a response regulator, ResD, occupies an early stage in the regulatory pathway governing anaerobic respiration. One of the essential roles of ResD and ResE in anaerobic gene regulation is induction of fnr transcription upon oxygen limita- tion. FNR is a transcriptional activator for anaerobically induced genes, including those for respiratory nitrate reductase, narGHJI. B. subtilis has two distinct nitrate reductases, one for the assimilation of nitrate nitrogen and the other for nitrate by WIB6106 - University Munchen on 06/10/14. For personal use only. respiration. In contrast, one nitrite reductase functions both in nitrite nitrogen assimilation and nitrite respiration. Unlike many anaerobes, which use pyruvate Annu. Rev. Microbiol. 1998.52:165-190. Downloaded from www.annualreviews.org formate lyase, B. subtilis can carry out fermentation in the absence of exter- nal electron acceptors wherein pyruvate dehydrogenase is utilized to metabolize pyruvate. CONTENTS INTRODUCTION ...........................................................166 NITRATE RESPIRATION .....................................................167 165 0066-4227/98/1001-0165$08.00 P1: ARS/ary P2: ARS/dat QC: ARS August 7, 1998 11:39 Annual Reviews AR063-06 166 NAKANO & ZUBER Nitrate Reductase .........................................................168 NarK...................................................................171 FNR ...................................................................171 ResD-ResE Two-Component Signal Transduction System .........................172 NITRITE RESPIRATION .....................................................173 Nitrite Reductase .........................................................173 REGULATORY PATHWAYS IN NITRATE/NITRITE RESPIRATION .................175 ResD and ResE Are Required for Expression of Anaerobically Induced Genes .........175 Analysis of the fnr Promoter Region Required for ResDE-Dependent Activation .......176 Isolation and Analysis of a resE Suppressor Mutant..............................177 What Is the Specific Stimulus Affecting ResE Activity? ............................178 FNR Is an Anaerobic Regulator in Nitrate Respiration ...........................180 Nitrite-Dependent Induction of hmp Expression .................................181 FERMENTATION ...........................................................182 METABOLISM DURING ANAEROBIC GROWTH ................................183 Pyruvate Metabolism ......................................................183 Krebs Cycle .............................................................183 Components in the Electron Transfer Pathway ..................................184 Phospholipids ...........................................................184 OTHER FACTORS ...........................................................185 CONCLUDING REMARKS ...................................................185 Addition in Proof .........................................................186 INTRODUCTION Bacteria often encounter drastic changes in their environment, including fluc- tuations in the levels of external oxygen. Unlike strict aerobes or strict anaer- obes, which can survive only either in the presence or absence of oxygen, facultative anaerobes can cope with changes in environmental oxygen levels by sensing oxygen concentration and shifting cellular metabolism accordingly (28, 36, 37, 45, 76). The changes in metabolism in response to changes in oxy- gen availability include adjustments to the rate and route of carbon source utilization, to the pathways of electron flow to maintain an oxidation-reduction balance, and to the mechanisms of energy production and of certain biosyn- thetic reactions. These changes are achieved by modulating protein activity, by by WIB6106 - University Munchen on 06/10/14. For personal use only. regulating the expression of the appropriate genes, or both. As one approach to studying these differences in the pattern of gene expression, proteins whose Annu. Rev. Microbiol. 1998.52:165-190. Downloaded from www.annualreviews.org concentrations fluctuate in response to changes in oxygen levels have been identified by two-dimensional gel electrophoresis of extracts obtained from aerobically and anaerobically grown cultures of Escherichia coli (65, 71, 72) and Salmonella typhimurium (1). Another approach, using random gene fu- sions to a promoterless lacZ, also resulted in the identification of E. coli genes induced by oxygen limitation (8, 9, 87). Aerobically induced proteins include the enzymes of the pyruvate dehydrogenase complex, several tricarboxylic acid cycle enzymes, and superoxide dismutase (72). Anaerobically induced proteins include some glycolytic enzymes and pyruvate formate lyase (71), required for P1: ARS/ary P2: ARS/dat QC: ARS August 7, 1998 11:39 Annual Reviews AR063-06 ANAEROBIOSIS OF BACILLUS SUBTILIS 167 the anaerobic disposal of electrons in the form of formic acid. Most but not all of the aerobically induced genes were also induced under anaerobic conditions in the presence of nitrate, and the majority of anaerobically induced genes were repressed in the presence of alternative electron acceptors such as nitrate, and to a lesser extent by trimethylamine N-oxide (TMAO) and dimethylsulfoxide (DMSO). The repressive effect of the electron acceptors on some anaerobically induced genes reflects two anaerobic growth modes of E. coli, respiration and fermentation. In the absence of electron acceptors, E. coli carries out mixed- acid fermentation. In fermentative growth where NADH is not reoxidized by the electron transfer pathway that is coupled to ATP generation, NADH is reox- idized by conversion of pyruvate to various end products during which ATP is produced by substrate-level phosphorylation. Genes whose products function in this less energy-generating fermentation pathway are repressed when electron acceptors such as oxygen and nitrate are available to drive electron transfer. Microbiology textbooks have described the gram-positive bacterium Bacillus subtilis as a strict aerobe and this, until recently, has been the common under- standing among most investigators studying B. subtilis. That B. subtilis could grow under anaerobic conditions was stated for the first time, to our knowledge, by Priest in a review that appeared in 1993 (58), although membrane-bound nitrate reductase was isolated three decades ago from B. subtilis cultured under low aeration (7, 47a) (as described later, the enzyme is very likely respiratory nitrate reductase). The description by Priest prompted a fair number of inves- tigators to start to examine anaerobiosis in B. subtilis. The Bacillus genome sequencing project has contributed significantly to this study by identifying genes that show similarity to those known to function in anaerobic metabolism in E. coli. The natural habitat of E. coli is the large intestine of mammals, and a shift from an aerobic to an anaerobic environment is the usual result upon its entry into the host. B. subtilis is abundant in soil and is probably transferred from soil to other associated environments. Therefore, in the case of B. subtilis, fluctu- by WIB6106 - University Munchen on 06/10/14. For personal use only. ations in the availability of oxygen are not necessarily the result of changes in habitat, but instead are derived easily by changes in the soil’s water content. The Annu. Rev. Microbiol. 1998.52:165-190. Downloaded from www.annualreviews.org conditions under which E. coli and B. subtilis must grow and survive in nature may account for the differences in the way the two organisms control anaero- biosis. In this review, we summarize recent findings in this new area of study. NITRATE RESPIRATION Nitrate is the preferred terminal electron acceptor when oxygen is absent be- 0 cause of its high midpoint redox potential (E0 430 mV). Nitrate respira- tion and nitrite respiration (described in the next=+ section) are the only anaerobic P1: ARS/ary P2: ARS/dat QC: ARS August 7, 1998 11:39 Annual Reviews AR063-06 168 NAKANO & ZUBER Table 1 Genes involved in nitrate/nitrite respiration of B. subtilis and their predicted products Homolog in Gene Probable function of product Escherichia coli resD Response regulator; aerobic/anaerobic respiration resE Sensor kinase; aerobic/anaerobic respiration fnr Anaerobic regulator fnr narK Nitrite extrusion narK narG Subunit of nitrate reductase; molybdoprotein narG; narZ narH Subunit of nitrate reductase; iron-sulfur protein narH; narY narJ Assembly of nitrate reductase complex? narJ;
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