Gene gain and loss events in Rickettsia and Orientiaspecies

Vicky Merhej,Khalid El Karkouri,Pierre Pontarotti,Didier Raoult,Kalliopi Georgiades

doi:10.1186/1745-6150-6-6

Abstract

BackgroundGenome degradation is an ongoing process in all members of the Rickettsiales order, which makes these bacterial species an excellent model for studying reductive evolution through interspecies variation in genome size and gene content. In this study, we evaluated the degree to which gene loss shaped the content of some Rickettsiales genomes. We shed light on the role played by horizontal gene transfers in the genome evolution of Rickettsiales.ResultsOur phylogenomic tree, based on whole-genome content, presented a topology distinct from that of the whole core gene concatenated phylogenetic tree, suggesting that the gene repertoires involved have different evolutionary histories. Indeed, we present evidence for 3 possible horizontal gene transfer events from various organisms to Orientia and 6 to Rickettsia spp., while we also identified 3 possible horizontal gene transfer events from Rickettsia and Orientia to other bacteria. We found 17 putative genes in Rickettsia spp. that are probably the result of de novo gene creation; 2 of these genes appear to be functional. On the basis of these results, we were able to reconstruct the gene repertoires of "proto-Rickettsiales" and "proto-Rickettsiaceae", which correspond to the ancestors of Rickettsiales and Rickettsiaceae, respectively. Finally, we found that 2,135 genes were lost during the evolution of the Rickettsiaceae to an intracellular lifestyle.ConclusionsOur phylogenetic analysis allowed us to track the gene gain and loss events occurring in bacterial genomes during their evolution from a free-living to an intracellular lifestyle. We have shown that the primary mechanism of evolution and specialization in strictly intracellular bacteria is gene loss. Despite the intracellular habitat, we found several horizontal gene transfers between Rickettsiales species and various prokaryotic, viral and eukaryotic species.Open peer reviewReviewed by Arcady Mushegian, Eugene V. Koonin and Patrick Forterre. For the full reviews please go to the Reviewers' comments section.

Highlights

Genome degradation is an ongoing process in all members of the Rickettsiales order, which makes these bacterial species an excellent model for studying reductive evolution through interspecies variation in genome size and gene content
After identifying true gene loss and horizontal gene transfer (HGT), we reconstructed the ancestral gene sets of alpha-proteobacteria, proto-Rickettsiales, proto-Rickettsiaceae and proto-Rickettsia, which helped us to predict the number of genes lost during the passage from a free-living to an intracellular lifestyle (See Additional File 1: Figure S1)
We found that 701 COG found only in Rickettsia (riCOG) (COGs found only in Rickettsia spp.) were common to the 11 rickettsial species in our study, 995 riCOGs were absent from at least 1 of the 11 rickettsial species and 1,954 open reading frames (ORFs) were specific to 1 of the 11 species (See Additional File 1: Table S1)

Summary

Introduction

Genome degradation is an ongoing process in all members of the Rickettsiales order, which makes these bacterial species an excellent model for studying reductive evolution through interspecies variation in genome size and gene content. The rickettsial species associated with arthropods are split into 2 major groups: the spotted fever group (SFG), which is associated with ticks, fleas and mites, and the often considered to be the result of its loss in that genome [11]. Given the genetic isolation of Rickettsiales, alternative mechanisms for gene gain seemed impossible until the discovery of horizontal gene transfer (HGT) events in rickettsial genomes [9,17,18,19,20]. These findings made it acceptable to regard microbial genomes as dynamic entities that evolve by both losing and acquiring genes [21]. When comparing closely related genomes, the relative absence of a given gene in one genome could potentially reflect gene gain in another genome

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