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Open Access Research article

Comparative analyses imply that the enigmatic sigma factor 54 is a central controller of the bacterial exterior

Christof Francke1246*, Tom Groot Kormelink1236, Yanick Hagemeijer6, Lex Overmars136, Vincent Sluijter6, Roy Moezelaar15 and Roland J Siezen1246

Author affiliations

1 TI Food and Nutrition, P.O.Box 557, 6700AN Wageningen, The Netherlands

2 Kluyver Centre for Genomics of Industrial Fermentation, Julianalaan 67 2628 BC Delft, The Netherlands

3 Wageningen University and Research Center, Laboratory of Microbiology, Dreijenplein 10, 6703 HB Wageningen, the Netherlands

4 Netherlands Bioinformatics Centre, Geert Grooteplein 28 6525 GA Nijmegen, The Netherlands

5 Wageningen University and Research Center, Food and Biobased Research, PO Box 17, 6700 AA The Netherlands

6 Center for Molecular and Biomolecular Informatics (260), NCMLS, Radboud University Nijmegen Medical Center, P.O.Box 9101, 6500HB Nijmegen, The Netherlands

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Citation and License

BMC Genomics 2011, 12:385  doi:10.1186/1471-2164-12-385

Published: 1 August 2011

Abstract

Background

Sigma-54 is a central regulator in many pathogenic bacteria and has been linked to a multitude of cellular processes like nitrogen assimilation and important functional traits such as motility, virulence, and biofilm formation. Until now it has remained obscure whether these phenomena and the control by Sigma-54 share an underlying theme.

Results

We have uncovered the commonality by performing a range of comparative genome analyses. A) The presence of Sigma-54 and its associated activators was determined for all sequenced prokaryotes. We observed a phylum-dependent distribution that is suggestive of an evolutionary relationship between Sigma-54 and lipopolysaccharide and flagellar biosynthesis. B) All Sigma-54 activators were identified and annotated. The relation with phosphotransfer-mediated signaling (TCS and PTS) and the transport and assimilation of carboxylates and nitrogen containing metabolites was substantiated. C) The function annotations, that were represented within the genomic context of all genes encoding Sigma-54, its activators and its promoters, were analyzed for intra-phylum representation and inter-phylum conservation. Promoters were localized using a straightforward scoring strategy that was formulated to identify similar motifs. We found clear highly-represented and conserved genetic associations with genes that concern the transport and biosynthesis of the metabolic intermediates of exopolysaccharides, flagella, lipids, lipopolysaccharides, lipoproteins and peptidoglycan.

Conclusion

Our analyses directly implicate Sigma-54 as a central player in the control over the processes that involve the physical interaction of an organism with its environment like in the colonization of a host (virulence) or the formation of biofilm.

Keywords:
biofilm; enhancer binding protein; exopolysaccharide; lipopolysaccharide; nitrogen assimilation; motility; peptidoglycan