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Open Access Highly Accessed Research article

On the nature of fur evolution: A phylogenetic approach in Actinobacteria

Catarina L Santos12*, João Vieira1, Fernando Tavares12, David R Benson3, Louis S Tisa4, Alison M Berry5, Pedro Moradas-Ferreira16 and Philippe Normand7

Author Affiliations

1 IBMC – Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua do Campo Alegre, 823, 4150-180 Porto, Portugal

2 Faculdade de Ciências da Universidade do Porto, Departamento de Botânica, Rua do Campo Alegre 1191, 4150-181 Porto, Portugal

3 Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06279, USA

4 Department of Microbiology, University of New Hampshire, Durham, NH, 03824, USA

5 Department of Plant Sciences, Mail Stop 1, PES Building, University of California, Davis, CA 95616, USA

6 Instituto de Ciências Biomédicas Abel Salazar, Lg. Prof. Abel Salazar, 4099-003 Porto, Portugal

7 UMR 5557 CNRS Ecologie Microbienne, IFR41 Bio-Environnement et Santé, Université Lyon 1, 43 Bd du 11 novembre 1918, 69622 Villeurbanne Cedex, France

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BMC Evolutionary Biology 2008, 8:185  doi:10.1186/1471-2148-8-185

Published: 25 June 2008

Abstract

Background

An understanding of the evolution of global transcription regulators is essential for comprehending the complex networks of cellular metabolism that have developed among related organisms. The fur gene encodes one of those regulators – the ferric uptake regulator Fur – widely distributed among bacteria and known to regulate different genes committed to varied metabolic pathways. On the other hand, members of the Actinobacteria comprise an ecologically diverse group of bacteria able to inhabit various natural environments, and for which relatively little is currently understood concerning transcriptional regulation.

Results

BLAST analyses revealed the presence of more than one fur homologue in most members of the Actinobacteria whose genomes have been fully sequenced. We propose a model to explain the evolutionary history of fur within this well-known bacterial phylum: the postulated scenario includes one duplication event from a primitive regulator, which probably had a broad range of co-factors and DNA-binding sites. This duplication predated the appearance of the last common ancestor of the Actinobacteria, while six other duplications occurred later within specific groups of organisms, particularly in two genera: Frankia and Streptomyces. The resulting paralogues maintained main biochemical properties, but became specialised for regulating specific functions, coordinating different metal ions and binding to unique DNA sequences. The presence of syntenic regions surrounding the different fur orthologues supports the proposed model, as do the evolutionary distances and topology of phylogenetic trees built using both Neighbor-Joining and Maximum-Likelihood methods.

Conclusion

The proposed fur evolutionary model, which includes one general duplication and two in-genus duplications followed by divergence and specialization, explains the presence and diversity of fur genes within the Actinobacteria. Although a few rare horizontal gene transfer events have been reported, the model is consistent with the view of gene duplication as a main force of microbial genomes evolution. The parallel study of Fur phylogeny across diverse organisms offers a solid base to guide functional studies and allows the comparison between response mechanisms in relation with the surrounding environment. The survey of regulators among related genomes provides a relevant tool for understanding the evolution of one of the first lines of cellular adaptability, control of DNA transcription.