The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in Gram‐positive bacteria

Grundy, Frank J.; Henkin, Tina M.

doi:10.1046/j.1365-2958.1998.01105.x

Cited by 268 publications

(319 citation statements)

References 27 publications

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“…For 20 of the 37 genes, additional regulation by secondary regulators has already been proven by previous studies. These 20 genes are: bioB, bmrR, purK, radA, yacK, yacM, ydaF, ykrT, yocL, ypuD, yraA, ysnF, ywhH, yxjG and the operon yceC-yceD-yceE-yceF-yceG-yceH (Au et al, 2005;Banse et al, 2008;Baranova et al, 1999;Bower et al, 1996; Cao et al, 2002;Chu et al, 2006;Chumsakul et al, 2011;Comella & Grossman, 2005;Derré et al, 1999;Drzewiecki et al, 1998;Ebbole & Zalkin, 1987;Eiamphungporn & Helmann, 2008;Erwin et al, 2005;Grundy & Henkin, 1998; Höper et al, 2005;Jervis et al, 2007;Kearns et al, 2005; Krüger et al, 1996;Kumaraswami et al, 2010;Leelakriangsak et al, 2007;Lei et al, 2009;Marvasi et al, 2010;Nakano et al, 2003;Nguyen et al, 2009;Perkins et al, 1996; Petersohn et al, 2001;Sekowska & Danchin, 2002;Wang et al, 2006;Weng et al, 1995; You et al, 2008). Details about their secondary regulators are included in Supplementary Table S4.…”

Section: Integrating the Two Rf-based Predictionsmentioning

confidence: 99%

Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification

et al. 2012

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The structure of the SigB-dependent general stress regulon of Bacillus subtilis has previously been characterized by proteomics approaches as well as DNA array-based expression studies. However, comparing the SigB targets published in three previous major transcriptional profiling studies it is obvious that although each of them identified well above 100 target genes, only 67 were identified in all three studies. These substantial differences can likely be attributed to the different strains, growth conditions, microarray platforms and experimental setups used in the studies. In order to gain a better understanding of the structure of this important regulon, a targeted DNA microarray analysis covering most of the known SigB-inducing conditions was performed, and the changes in expression kinetics of 252 potential members of the SigB regulon and appropriate control genes were recorded. Transcriptional data for the B. subtilis wild-type strain 168 and its isogenic sigB mutant BSM29 were analysed using random forest, a machine learning algorithm, by incorporating the knowledge from previous studies. This analysis revealed a strictly SigB-dependent expression pattern for 166 genes following ethanol, butanol, osmotic and oxidative stress, low-temperature growth and heat shock, as well as limitation of oxygen or glucose. Kinetic analysis of the data for the wild-type strain identified 30 additional members of the SigB regulon, which were also subject to control by additional transcriptional regulators, thus displaying atypical SigB-independent induction patterns in the mutant strain under some of the conditions tested. For 19 of these 30 SigB regulon members, published reports support control by secondary regulators along with SigB. Thus, this microarray-based study assigns a total of 196 genes to the SigB-dependent general stress regulon of B. subtilis. INTRODUCTIONAs an organism living in the upper layer of soil, Bacillus subtilis is exposed to a wide range of transitory stress and starvation conditions, and many of these activate the alternative sigma factor SigB. The collection of SigBactivating stress conditions includes sudden environmental stresses such as heat, acid, ethanol, butanol and osmotic stress, Mn 2+ , nitric oxide (NO), sodium nitroprusside (SNP) and blue light; energy stresses such as starvation for glucose, phosphate and oxygen; inhibitors that collectively trigger a decrease in the ATP pool [azide, carbonyl cyanide m-chlorophenylhydrazone (CCCP), mycophenolic acid], addition of antibiotics such as vancomycin and bacitracin; as well as growth at extreme temperatures, both high and low (Hecker et al., 2007;Price, 2000Price, , 2002Price, , 2011. The increased expression of the SigB regulon provides B. subtilis cells with a non-specific, multiple stress resistance against a wide range of stresses (Gaidenko & Price, 1998; Höper et al., 2005; Völker et al., 1999). SigB-dependent gene Abbreviations: ANOVA, analysis of variance; OOB, out-of-bag; RF, random forest.The complete microarray dataset discussed...

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Section: Integrating the Two Rf-based Predictionsmentioning

confidence: 99%

Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification

et al. 2012

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“…11,[30][31][32][33][34] These riboswitches are located upstream of genes involved in the metabolism, biosynthesis and transport of methionine or SAM. 11,35 The SAM riboswitch class is one of the most abundant, 36 especially in Gram-positive organisms, and is unique in that six distinct SAM riboswitch families have been reported to date that bind SAM in diverse ways. 3,11,24,36 The large diversity of SAM riboswitches likely reflects the importance of regulating SAM-related metabolic pathways.…”

Section: S-adenosylmethionine (Sam) Riboswitchesmentioning

confidence: 99%

Folding of the SAM-I riboswitch

et al. 2012

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“…Grundy and Henkin (11) found that at least 11 transcription units in Bacillus subtilis that are mostly involved in Cys and Met synthesis possess a leader element that includes an intrinsic transcription terminator, competing antiterminator, and a conserved element (S-box) that functions as an anti-antiterminator. Based on their genetic and physiological studies, the authors postulated that the S-box serves as a target for repression during growth in the presence of Met (11,12).…”

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The riboswitch-mediated control of sulfur metabolism in bacteria

Epshtein

Mironov

Nudler

2003

Proc. Natl. Acad. Sci. U.S.A.

235

164

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Many operons in Gram-positive bacteria that are involved in methionine (Met) and cysteine (Cys) biosynthesis possess an evolutionarily conserved regulatory leader sequence (S-box) that positively controls these genes in response to methionine starvation. Here, we demonstrate that a feed-back regulation mechanism utilizes S-adenosyl-methionine as an effector. S-adenosyl-methionine directly and specifically binds to the nascent S-box RNA, causing an intrinsic terminator to form and interrupt transcription prematurely. The S-box leader RNA thus expands the family of newly discovered riboswitches, i.e., natural regulatory RNA aptamers that seem to sense small molecules ranging from amino acid derivatives to vitamins.M odulation of the structures of leader transcripts is a common mode of regulation of synthetic and metabolic operons in prokaryotes. Switching between two alternative RNA structures, with one causing transcription termination, is made in response to some external event, e.g., ribosome pausing (in Gram-negative bacteria), binding of a regulatory protein, or tRNA (in Gram-positive bacteria) (reviewed in ref. 1). Recently, three regulons responsible for vitamin biosynthesis have been shown to use flavinmononucleotide, thiamin pyrophosphate (TPP), and adenosyl-cobalamin to directly bind their cognate leader RNAs, changing their structures and functions (2-5). Such leader RNA aptamers were called riboswitches to reflect their unique ability to switch between two conformations in response to binding of a small molecule without the help of proteins (3, 5, 6). The evolutionarily conserved sequences encoding vitamin-sensing riboswitches have been found in the genomes of many Gram-positive and Gram-negative bacteria (7-10), and also in some archaea (10), fungi, and plant species (A.S.M. and E.N., unpublished observations). In this work, we tested the hypothesis that riboswitches are not just a peculiar attribute of vitamin biosynthetic operons but are more common in nature and are also involved in control of amino acid biosynthesis.Grundy and Henkin (11) found that at least 11 transcription units in Bacillus subtilis that are mostly involved in Cys and Met synthesis possess a leader element that includes an intrinsic transcription terminator, competing antiterminator, and a conserved element (S-box) that functions as an anti-antiterminator. Based on their genetic and physiological studies, the authors postulated that the S-box serves as a target for repression during growth in the presence of Met (11,12). Northern blot experiments substantiated a model of S-box gene regulation by transcription antitermination in response to Met (13). It has also been shown that overexpression of S-adenosyl-methionine (SAM) synthase leads to Met auxotrophy in B. subtilis, suggesting that SAM is an effector of Met biosynthesis in this bacteria (14). This notion was corroborated recently. The transcription profile of S-box genes in several Met auxotroph strains of B. subtilis was analyzed by using DNA arrays. The results argued that...

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The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in Gram‐positive bacteria

Cited by 268 publications

References 27 publications

Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification

Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification

Folding of the SAM-I riboswitch

The riboswitch-mediated control of sulfur metabolism in bacteria

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