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Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function.

Tran HT, Krushkal J, Antommattei FM, Lovley DR, Weis RM - BMC Genomics (2008)

Bottom Line: Geobacter species are delta-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important.The genomes of G. sulfurreducens, G. metallireducens, and G. uraniireducens contain multiple (approximately 70) homologs of chemotaxis genes arranged in several major clusters (six, seven, and seven, respectively).The numerous chemoreceptors and chemotaxis-like gene clusters of Geobacter appear to be responsible for a diverse set of signaling functions in addition to chemotaxis, including gene regulation and biofilm formation, through functionally and spatially distinct signaling pathways.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Chemistry, University of Massachusetts, Amherst, MA 01003, USA. htt@chem.umass.edu

ABSTRACT

Background: Geobacter species are delta-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important. Their ability to remediate contaminated environments and produce electricity makes them attractive for further study. Cell motility, biofilm formation, and type IV pili all appear important for the growth of Geobacter in changing environments and for electricity production. Recent studies in other bacteria have demonstrated that signaling pathways homologous to the paradigm established for Escherichia coli chemotaxis can regulate type IV pili-dependent motility, the synthesis of flagella and type IV pili, the production of extracellular matrix material, and biofilm formation. The classification of these pathways by comparative genomics improves the ability to understand how Geobacter thrives in natural environments and better their use in microbial fuel cells.

Results: The genomes of G. sulfurreducens, G. metallireducens, and G. uraniireducens contain multiple (approximately 70) homologs of chemotaxis genes arranged in several major clusters (six, seven, and seven, respectively). Unlike the single gene cluster of E. coli, the Geobacter clusters are not all located near the flagellar genes. The probable functions of some Geobacter clusters are assignable by homology to known pathways; others appear to be unique to the Geobacter sp. and contain genes of unknown function. We identified large numbers of methyl-accepting chemotaxis protein (MCP) homologs that have diverse sensing domain architectures and generate a potential for sensing a great variety of environmental signals. We discuss mechanisms for class-specific segregation of the MCPs in the cell membrane, which serve to maintain pathway specificity and diminish crosstalk. Finally, the regulation of gene expression in Geobacter differs from E. coli. The sequences of predicted promoter elements suggest that the alternative sigma factors sigma28 and sigma54 play a role in regulating the Geobacter chemotaxis gene expression.

Conclusion: The numerous chemoreceptors and chemotaxis-like gene clusters of Geobacter appear to be responsible for a diverse set of signaling functions in addition to chemotaxis, including gene regulation and biofilm formation, through functionally and spatially distinct signaling pathways.

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Alignment of the beta-subdomain of Geobacter CheR homologs with E. coli and S. enterica CheR. Based on homology, the Geobacter CheRs were divided into three groups. Two groups (A and B) displayed significant identity with residues important for binding pentapeptide (highlighted in grey) and the third group (C) did not. Gene positioning provides further evidence that the group A and B homologs bind to MCPs containing the C-terminal pentapeptide: these homologs are located in che clusters with pentapeptide-containing MCPs (Figure 1). Group A consists of two CheR homologs that are located near two class-36 H MCPs. The consensus pentapeptide of the MCPs that are cognate to the Group B CheR homologs, EFEKF, is found in class-34 H MCPs.
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Figure 3: Alignment of the beta-subdomain of Geobacter CheR homologs with E. coli and S. enterica CheR. Based on homology, the Geobacter CheRs were divided into three groups. Two groups (A and B) displayed significant identity with residues important for binding pentapeptide (highlighted in grey) and the third group (C) did not. Gene positioning provides further evidence that the group A and B homologs bind to MCPs containing the C-terminal pentapeptide: these homologs are located in che clusters with pentapeptide-containing MCPs (Figure 1). Group A consists of two CheR homologs that are located near two class-36 H MCPs. The consensus pentapeptide of the MCPs that are cognate to the Group B CheR homologs, EFEKF, is found in class-34 H MCPs.

Mentions: To identify possible class-specific MCP-methyltransferase tethering interactions, we compared the aligned β-subdomain sequences of the Geobacter CheR homologs to the Salmonella and E. coli CheR sequences. The Salmonella CheR structure, co-crystallized with the NWETF pentapeptide has enabled the identification of residues in the β-subdomain that are involved in the peptide-CheR interaction (Q182, G188, R187, G190, G194 and R197, numbered according to Salmonella CheR, PDB# 1bc5) [75,77]. Figure 3 shows aligned sequences from the β-subdomain of all the Geobacter CheR homologs, together with the E. coli and Salmonella sequences (residues 166–199). Using this alignment, we divided the Geobacter CheRs into three groups. Two groups (A and B) displayed significant identity with residues important for binding a pentapeptide; the third and largest group (C) did not (Figure 3). Consequently, we concluded that the CheR homologs in Group C probably do not methylate MCPs by the E. coli mechanism.


Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function.

Tran HT, Krushkal J, Antommattei FM, Lovley DR, Weis RM - BMC Genomics (2008)

Alignment of the beta-subdomain of Geobacter CheR homologs with E. coli and S. enterica CheR. Based on homology, the Geobacter CheRs were divided into three groups. Two groups (A and B) displayed significant identity with residues important for binding pentapeptide (highlighted in grey) and the third group (C) did not. Gene positioning provides further evidence that the group A and B homologs bind to MCPs containing the C-terminal pentapeptide: these homologs are located in che clusters with pentapeptide-containing MCPs (Figure 1). Group A consists of two CheR homologs that are located near two class-36 H MCPs. The consensus pentapeptide of the MCPs that are cognate to the Group B CheR homologs, EFEKF, is found in class-34 H MCPs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2577667&req=5

Figure 3: Alignment of the beta-subdomain of Geobacter CheR homologs with E. coli and S. enterica CheR. Based on homology, the Geobacter CheRs were divided into three groups. Two groups (A and B) displayed significant identity with residues important for binding pentapeptide (highlighted in grey) and the third group (C) did not. Gene positioning provides further evidence that the group A and B homologs bind to MCPs containing the C-terminal pentapeptide: these homologs are located in che clusters with pentapeptide-containing MCPs (Figure 1). Group A consists of two CheR homologs that are located near two class-36 H MCPs. The consensus pentapeptide of the MCPs that are cognate to the Group B CheR homologs, EFEKF, is found in class-34 H MCPs.
Mentions: To identify possible class-specific MCP-methyltransferase tethering interactions, we compared the aligned β-subdomain sequences of the Geobacter CheR homologs to the Salmonella and E. coli CheR sequences. The Salmonella CheR structure, co-crystallized with the NWETF pentapeptide has enabled the identification of residues in the β-subdomain that are involved in the peptide-CheR interaction (Q182, G188, R187, G190, G194 and R197, numbered according to Salmonella CheR, PDB# 1bc5) [75,77]. Figure 3 shows aligned sequences from the β-subdomain of all the Geobacter CheR homologs, together with the E. coli and Salmonella sequences (residues 166–199). Using this alignment, we divided the Geobacter CheRs into three groups. Two groups (A and B) displayed significant identity with residues important for binding a pentapeptide; the third and largest group (C) did not (Figure 3). Consequently, we concluded that the CheR homologs in Group C probably do not methylate MCPs by the E. coli mechanism.

Bottom Line: Geobacter species are delta-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important.The genomes of G. sulfurreducens, G. metallireducens, and G. uraniireducens contain multiple (approximately 70) homologs of chemotaxis genes arranged in several major clusters (six, seven, and seven, respectively).The numerous chemoreceptors and chemotaxis-like gene clusters of Geobacter appear to be responsible for a diverse set of signaling functions in addition to chemotaxis, including gene regulation and biofilm formation, through functionally and spatially distinct signaling pathways.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Chemistry, University of Massachusetts, Amherst, MA 01003, USA. htt@chem.umass.edu

ABSTRACT

Background: Geobacter species are delta-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important. Their ability to remediate contaminated environments and produce electricity makes them attractive for further study. Cell motility, biofilm formation, and type IV pili all appear important for the growth of Geobacter in changing environments and for electricity production. Recent studies in other bacteria have demonstrated that signaling pathways homologous to the paradigm established for Escherichia coli chemotaxis can regulate type IV pili-dependent motility, the synthesis of flagella and type IV pili, the production of extracellular matrix material, and biofilm formation. The classification of these pathways by comparative genomics improves the ability to understand how Geobacter thrives in natural environments and better their use in microbial fuel cells.

Results: The genomes of G. sulfurreducens, G. metallireducens, and G. uraniireducens contain multiple (approximately 70) homologs of chemotaxis genes arranged in several major clusters (six, seven, and seven, respectively). Unlike the single gene cluster of E. coli, the Geobacter clusters are not all located near the flagellar genes. The probable functions of some Geobacter clusters are assignable by homology to known pathways; others appear to be unique to the Geobacter sp. and contain genes of unknown function. We identified large numbers of methyl-accepting chemotaxis protein (MCP) homologs that have diverse sensing domain architectures and generate a potential for sensing a great variety of environmental signals. We discuss mechanisms for class-specific segregation of the MCPs in the cell membrane, which serve to maintain pathway specificity and diminish crosstalk. Finally, the regulation of gene expression in Geobacter differs from E. coli. The sequences of predicted promoter elements suggest that the alternative sigma factors sigma28 and sigma54 play a role in regulating the Geobacter chemotaxis gene expression.

Conclusion: The numerous chemoreceptors and chemotaxis-like gene clusters of Geobacter appear to be responsible for a diverse set of signaling functions in addition to chemotaxis, including gene regulation and biofilm formation, through functionally and spatially distinct signaling pathways.

Show MeSH
Related in: MedlinePlus