Research

Massive comparative genomic analysis reveals convergent evolution of specialized bacteria

Vicky Merhej¹ , Manuela Royer-Carenzi² , Pierre Pontarotti² and Didier Raoult¹

¹  Unit for Research on Emergent and Tropical Infectious Diseases (URMITE), CNRS-IRD UMR 6236 IFR48, Faculty of Medicine, University of the Mediterranean, Marseilles, France

²  Evolutionary biology and modeling, LATP UMR CNRS 6632 FR 3098 IFR 48, University of Provence, Marseilles, France

author email corresponding author email

Biology Direct 2009, 4:13doi:10.1186/1745-6150-4-13

Published:	10 April 2009

Abstract

Background

Genome size and gene content in bacteria are associated with their lifestyles. Obligate intracellular bacteria (i.e., mutualists and parasites) have small genomes that derived from larger free-living bacterial ancestors; however, the different steps of bacterial specialization from free-living to intracellular lifestyle have not been studied comprehensively. The growing number of available sequenced genomes makes it possible to perform a statistical comparative analysis of 317 genomes from bacteria with different lifestyles.

Results

Compared to free-living bacteria, host-dependent bacteria exhibit fewer rRNA genes, more split rRNA operons and fewer transcriptional regulators, linked to slower growth rates. We found a function-dependent and non-random loss of the same 100 orthologous genes in all obligate intracellular bacteria. Thus, we showed that obligate intracellular bacteria from different phyla are converging according to their lifestyle. Their specialization is an irreversible phenomenon characterized by translation modification and massive gene loss, including the loss of transcriptional regulators. Although both mutualists and parasites converge by genome reduction, these obligate intracellular bacteria have lost distinct sets of genes in the context of their specific host associations: mutualists have significantly more genes that enable nutrient provisioning whereas parasites have genes that encode Types II, IV, and VI secretion pathways.

Conclusion

Our findings suggest that gene loss, rather than acquisition of virulence factors, has been a driving force in the adaptation of parasites to eukaryotic cells. This comparative genomic analysis helps to explore the strategies by which obligate intracellular genomes specialize to particular host-associations and contributes to advance our knowledge about the mechanisms of bacterial evolution.

Reviewers

This article was reviewed by Eugene V. Koonin, Nicolas Galtier, and Jeremy Selengut.