Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function

Hoa T Tran,Robert M Weis,Frances M Antommattei,Julia Krushkal,Derek R Lovley

doi:10.1186/1471-2164-9-471

Abstract

BackgroundGeobacter species are δ-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.ResultsThe genomes of G. sulfurreducens, G. metallireducens, and G. uraniireducens contain multiple (~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 σ28 and σ54 play a role in regulating the Geobacter chemotaxis gene expression.ConclusionThe 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.

Highlights

Geobacter species are δ-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important
Geobacter Chemotaxis Genes: Numbers and Organization BLAST analysis of the G. sulfurreducens, G. metallireducens, and G. uraniireducens genomes identified multiple copies of the chemotaxis genes; over 60 genes in each species were homologous to the known che and mcp genes in E. coli, B. subtilis and T. maritima (Table 1)
Homologs of all the che genes from E. coli were present in the Geobacter species, except cheZ, which is found much more frequently in genomes of β- and γ-proteobacteria in comparison to the genomes of α, ε, and especially δ-proteobacteria [54]

Summary

Introduction

Geobacter species are δ-Proteobacteria and are often the predominant species in a variety of sedimentary environments where Fe(III) reduction is important. 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. Adaptation to stimuli, mediated by the reversible methylation of MCPs in the process catalyzed by CheR and CheB, allows cells to remain sensitive to small changes in chemoeffector concentration over a large range [7,8]

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