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Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses.

Gao H, Wang X, Yang ZK, Palzkill T, Zhou J - BMC Genomics (2008)

Bottom Line: To further determine genes regulated by the Arc system, an ArcA recognition weight matrix from DNA-binding data and bioinformatics analysis was generated and used to produce an ArcA sequence affinity map.By combining both techniques, we identified an ArcA regulon of at least 50 operons, of which only 6 were found to be directly controlled by ArcA in E. coli.These results indicate that the Arc system in S. oneidensis differs from that in E. coli substantially in terms of its physiological function and regulon while their binding motif are strikingly similar.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Environmental Genomics and Department of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 73019, USA. haichun@ou.edu

ABSTRACT

Background: The Arc two-component system is a global regulator controlling many genes involved in aerobic/anaerobic respiration and fermentative metabolism in Escherichia coli. Shewanella oneidensis MR-1 contains a gene encoding a putative ArcA homolog with ~81% amino acid sequence identity to the E. coli ArcA protein but not a full-length arcB gene.

Results: To understand the role of ArcA in S. oneidensis, an arcA deletion strain was constructed and subjected to both physiological characterization and microarray analysis. Compared to the wild-type MR-1, the mutant exhibited impaired aerobic growth and a defect in utilizing DMSO in the absence of O2. Microarray analyses on cells grown aerobically and anaerobically on fumarate revealed that expression of 1009 genes was significantly affected (p < 0.05) by the mutation. In contrast to E. coli ArcA, the protein appears to be dispensable in regulation of the TCA cycle in S. oneidensis. To further determine genes regulated by the Arc system, an ArcA recognition weight matrix from DNA-binding data and bioinformatics analysis was generated and used to produce an ArcA sequence affinity map. By combining both techniques, we identified an ArcA regulon of at least 50 operons, of which only 6 were found to be directly controlled by ArcA in E. coli.

Conclusion: These results indicate that the Arc system in S. oneidensis differs from that in E. coli substantially in terms of its physiological function and regulon while their binding motif are strikingly similar.

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Differentially expressed genes grouped by functional classification according to the TIGR S. oneidensis genome database. A, Amino acid biosynthesis; B, Biosynthesis of cofactors, prosthetic groups, and carriers; C, Cell envelope; D. Cellular processes; E, Central intermediary metabolism; F, Disrupted reading frame; G, DNA metabolism; H, Energy metabolism; I, Fatty acid and phospholipid metabolism; J, Hypothetical proteins; K, Mobile and extrachromosomal element functions; L, Protein fate; M, Protein synthesis; N, Purines, pyrimidines, nucleosides, and nucleotides; O, Regulatory functions; P, Signal transduction; Q, Transcription; R, Transport and binding proteins; S, Unclassified; T, Unknown function. Bars in black are the genes that showed decreased expression in the presence of ArcA; bars in gray are the genes that showed increased expression in the presence of ArcA.
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Figure 2: Differentially expressed genes grouped by functional classification according to the TIGR S. oneidensis genome database. A, Amino acid biosynthesis; B, Biosynthesis of cofactors, prosthetic groups, and carriers; C, Cell envelope; D. Cellular processes; E, Central intermediary metabolism; F, Disrupted reading frame; G, DNA metabolism; H, Energy metabolism; I, Fatty acid and phospholipid metabolism; J, Hypothetical proteins; K, Mobile and extrachromosomal element functions; L, Protein fate; M, Protein synthesis; N, Purines, pyrimidines, nucleosides, and nucleotides; O, Regulatory functions; P, Signal transduction; Q, Transcription; R, Transport and binding proteins; S, Unclassified; T, Unknown function. Bars in black are the genes that showed decreased expression in the presence of ArcA; bars in gray are the genes that showed increased expression in the presence of ArcA.

Mentions: In total, 1009 genes passed ANOVA statistical analysis (p < 0.05) with Benjamini and Hochberg False Discovery Rate multiple testing correction in at least one of two hybridizations between JZ3988K and MR-1, representing approximately 21.7% of the 4,648 ORFs spotted on the array (Table S1 in additional file 2). Interestingly, only 12 genes responded oppositely under aerobic and anaerobic conditions while the majority of 1009 genes responded to the arcA mutation are irrespective to the availability of oxygen. The functional class distribution of these 1009 genes is shown in Fig. 2. Genes displaying significant differences in expression due to an arcA mutation under either aerobic or anaerobic conditions were observed in almost every category. The wide distribution of putative functional roles attributed to the differentially expressed genes indicates that ArcA has a global effect on gene expression in S. oneidensis. While up to 54% of the genes showed increased expression in the absence of ArcA under aerobic conditions, the percentage of this type of genes under anaerobic conditions increased to 60%. The most noticeable differences in gene numbers between tested conditions were observed in the categories of protein synthesis (M) and nucleotide synthesis (N). Under aerobic conditions, nearly all of genes in these two categories showed reduced expression in the absence of ArcA but very few genes in these categories were affected under anaerobic conditions.


Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses.

Gao H, Wang X, Yang ZK, Palzkill T, Zhou J - BMC Genomics (2008)

Differentially expressed genes grouped by functional classification according to the TIGR S. oneidensis genome database. A, Amino acid biosynthesis; B, Biosynthesis of cofactors, prosthetic groups, and carriers; C, Cell envelope; D. Cellular processes; E, Central intermediary metabolism; F, Disrupted reading frame; G, DNA metabolism; H, Energy metabolism; I, Fatty acid and phospholipid metabolism; J, Hypothetical proteins; K, Mobile and extrachromosomal element functions; L, Protein fate; M, Protein synthesis; N, Purines, pyrimidines, nucleosides, and nucleotides; O, Regulatory functions; P, Signal transduction; Q, Transcription; R, Transport and binding proteins; S, Unclassified; T, Unknown function. Bars in black are the genes that showed decreased expression in the presence of ArcA; bars in gray are the genes that showed increased expression in the presence of ArcA.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2262068&req=5

Figure 2: Differentially expressed genes grouped by functional classification according to the TIGR S. oneidensis genome database. A, Amino acid biosynthesis; B, Biosynthesis of cofactors, prosthetic groups, and carriers; C, Cell envelope; D. Cellular processes; E, Central intermediary metabolism; F, Disrupted reading frame; G, DNA metabolism; H, Energy metabolism; I, Fatty acid and phospholipid metabolism; J, Hypothetical proteins; K, Mobile and extrachromosomal element functions; L, Protein fate; M, Protein synthesis; N, Purines, pyrimidines, nucleosides, and nucleotides; O, Regulatory functions; P, Signal transduction; Q, Transcription; R, Transport and binding proteins; S, Unclassified; T, Unknown function. Bars in black are the genes that showed decreased expression in the presence of ArcA; bars in gray are the genes that showed increased expression in the presence of ArcA.
Mentions: In total, 1009 genes passed ANOVA statistical analysis (p < 0.05) with Benjamini and Hochberg False Discovery Rate multiple testing correction in at least one of two hybridizations between JZ3988K and MR-1, representing approximately 21.7% of the 4,648 ORFs spotted on the array (Table S1 in additional file 2). Interestingly, only 12 genes responded oppositely under aerobic and anaerobic conditions while the majority of 1009 genes responded to the arcA mutation are irrespective to the availability of oxygen. The functional class distribution of these 1009 genes is shown in Fig. 2. Genes displaying significant differences in expression due to an arcA mutation under either aerobic or anaerobic conditions were observed in almost every category. The wide distribution of putative functional roles attributed to the differentially expressed genes indicates that ArcA has a global effect on gene expression in S. oneidensis. While up to 54% of the genes showed increased expression in the absence of ArcA under aerobic conditions, the percentage of this type of genes under anaerobic conditions increased to 60%. The most noticeable differences in gene numbers between tested conditions were observed in the categories of protein synthesis (M) and nucleotide synthesis (N). Under aerobic conditions, nearly all of genes in these two categories showed reduced expression in the absence of ArcA but very few genes in these categories were affected under anaerobic conditions.

Bottom Line: To further determine genes regulated by the Arc system, an ArcA recognition weight matrix from DNA-binding data and bioinformatics analysis was generated and used to produce an ArcA sequence affinity map.By combining both techniques, we identified an ArcA regulon of at least 50 operons, of which only 6 were found to be directly controlled by ArcA in E. coli.These results indicate that the Arc system in S. oneidensis differs from that in E. coli substantially in terms of its physiological function and regulon while their binding motif are strikingly similar.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Environmental Genomics and Department of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 73019, USA. haichun@ou.edu

ABSTRACT

Background: The Arc two-component system is a global regulator controlling many genes involved in aerobic/anaerobic respiration and fermentative metabolism in Escherichia coli. Shewanella oneidensis MR-1 contains a gene encoding a putative ArcA homolog with ~81% amino acid sequence identity to the E. coli ArcA protein but not a full-length arcB gene.

Results: To understand the role of ArcA in S. oneidensis, an arcA deletion strain was constructed and subjected to both physiological characterization and microarray analysis. Compared to the wild-type MR-1, the mutant exhibited impaired aerobic growth and a defect in utilizing DMSO in the absence of O2. Microarray analyses on cells grown aerobically and anaerobically on fumarate revealed that expression of 1009 genes was significantly affected (p < 0.05) by the mutation. In contrast to E. coli ArcA, the protein appears to be dispensable in regulation of the TCA cycle in S. oneidensis. To further determine genes regulated by the Arc system, an ArcA recognition weight matrix from DNA-binding data and bioinformatics analysis was generated and used to produce an ArcA sequence affinity map. By combining both techniques, we identified an ArcA regulon of at least 50 operons, of which only 6 were found to be directly controlled by ArcA in E. coli.

Conclusion: These results indicate that the Arc system in S. oneidensis differs from that in E. coli substantially in terms of its physiological function and regulon while their binding motif are strikingly similar.

Show MeSH
Related in: MedlinePlus