Sunday, January 21, 2007

 

Reductive Genome Evolution from the Mother of Rickettsia

Excerpts from an open access PLoS Genetics article:

Summary

Genome downsizing and fast sequence divergence are frequently observed in bacteria living exclusively within the cells of higher eukaryotes. However, the driving forces and contributions of these processes to the genome diversity of the microorganisms remain poorly understood. The genus Rickettsia, a group of small obligate intracellular pathogens of humans, provides a fascinating model to study the genome downsizing process. In this article, we used seven Rickettsia genomes to reconstruct the genome of their ancestor and inferred the origin and fate of the genes found in today's species. We identify the process of gene loss as the main cause of genome diversification within the genus and show that the rate of gene loss, sequence divergence, and genome rearrangements are highly variable across the various Rickettsia lineages. This heterogeneity likely reflects the intricate effects of specialization to distinct arthropod hosts and critical alterations of the gene repertoire, such as the losses of DNA repair genes and the amplification of mobile genes. In contrast, we did not find evidence for the role of reduced population sizes on the long-term acceleration of sequence evolution. Overall, the data presented in this article shed new light on the fundamental evolutionary processes that drive the evolution of obligate intracellular bacteria.

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Abstract

The Rickettsia genus is a group of obligate intracellular alpha-proteobacteria representing a paradigm of reductive evolution. Here, we investigate the evolutionary processes that shaped the genomes of the genus. The reconstruction of ancestral genomes indicates that their last common ancestor contained more genes, but already possessed most traits associated with cellular parasitism. The differences in gene repertoires across modern Rickettsia are mainly the result of differential gene losses from the ancestor. We demonstrate using computer simulation that the propensity of loss was variable across genes during this process. We also analyzed the ratio of nonsynonymous to synonymous changes (Ka/Ks) calculated as an average over large sets of genes to assay the strength of selection acting on the genomes of Rickettsia, Anaplasmataceae, and free-living gamma-proteobacteria. As a general trend, Ka/Ks were found to decrease with increasing divergence between genomes. The high Ka/Ks for closely related genomes are probably due to a lag in the removal of slightly deleterious nonsynonymous mutations by natural selection. Interestingly, we also observed a decrease of the rate of gene loss with increasing divergence, suggesting a similar lag in the removal of slightly deleterious pseudogene alleles. For larger divergence (Ks greater than 0.2), Ka/Ks converge toward similar values indicating that the levels of selection are roughly equivalent between intracellular alpha-proteobacteria and their free-living relatives. This contrasts with the view that obligate endocellular microorganisms tend to evolve faster as a consequence of reduced effectiveness of selection, and suggests a major role of enhanced background mutation rates on the fast protein divergence in the obligate intracellular alpha-proteobacteria.

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Introduction

Intracellular bacteria that are strictly associated with multicellular eukaryotes possess small genomes, typically in the range of 1 Mb or less. This feature is a consequence of the reduction of originally larger genomes invariably accompanying the adaptation to parasitic/symbiotic lifestyles. The transition from a free-living existence to a close relationship with eukaryotic cells is a frequent theme in bacterial evolution and has been documented in mycoplasmas, phytoplasmas, chlamydias, and the alpha- and gamma-proteobacteria. The Rickettsia genus is a group of obligate intracellular, small, rod-shaped, alpha-proteobacteria that possess highly reduced genomes compared to those of their free-living relatives. Known Rickettsia are parasites of arthropods such as ticks and insects (lice and fleas), in which they are presumably stably maintained in the population and can be vertically transmitted. Through bites or feces of the vectors, they can infect mammals that can become sources for the next lines of infected vectors. Many members of this genus cause mild to fatal diseases in humans.

The Rickettsia genus provides an excellent model to investigate the process of reductive evolution. Their genomes present substantial inter-species variations in size (1.1-1.5 Mb) and gene content (about 900-1,500 genes) as a consequence of the recent and ongoing genome degradation process. However, they exhibit few recent gene transfers and genome rearrangements, which help a fine reconstruction of genome evolution history. Complete genome sequences are publicly available for five Rickettsia species covering the three major genus sub-groups: the typhus group (TG), including Rickettsia prowazekii (the agent of epidemic typhus transmitted by louse) and Rickettsia typhi (the agent endemic typhus transmitted by flea); the spotted fever group (SFG), including Rickettsia conorii (the agent of Mediterranean spotted fever transmitted by tick) and Rickettsia felis (the agent of flea-borne spotted fever); and the last group currently represented by a sole species, Rickettsia bellii, associated with ticks. The availability of these five Rickettsia genome sequences, as well as two new SFG Rickettsia genome sequences determined in our laboratory (i.e., Rickettsia africae, the agent of African tick bite fever and Rickettsia massiliae, the agent of a tick-borne spotted fever in Europe) prompted us to carry out a comparative genomics analysis to investigate how genome reduction and other evolutionary processes have contributed to the diversity of the genus. In this study, we identified the genes conserved in seven Rickettsia, inferred the gene content of their ancestors, and investigated the evolutionary dynamics of genome changes that occurred during the evolution of the genus.

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Full article citation:

Blanc G, Ogata H, Robert C, Audic S, Suhre K, et al. (2007) Reductive Genome Evolution from the Mother of Rickettsia. PLoS Genet 3(1): e14 doi:10.1371/journal.pgen.0030014

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