The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution.

Christoph Kneip,Uwe G Maier,Peter J Lockhart,Christine Voβ

doi:10.1186/1471-2148-8-30

Abstract

BackgroundBacteria occur in facultative association and intracellular symbiosis with a diversity of eukaryotic hosts. Recently, we have helped to characterise an intracellular nitrogen fixing bacterium, the so-called spheroid body, located within the diatom Rhopalodia gibba. Spheroid bodies are of cyanobacterial origin and exhibit features that suggest physiological adaptation to their intracellular life style. To investigate the genome modifications that have accompanied the process of endosymbiosis, here we compare gene structure, content and organisation in spheroid body and cyanobacterial genomes.ResultsComparison of the spheroid body's genome sequence with corresponding regions of near free-living relatives indicates that multiple modifications have occurred in the endosymbiont's genome. These include localised changes that have led to elimination of some genes. This gene loss has been accompanied either by deletion of the respective DNA region or replacement with non-coding DNA that is AT rich in composition. In addition, genome modifications have led to the fusion and truncation of genes. We also report that in the spheroid body's genome there is an accumulation of deleterious mutations in genes for cell wall biosynthesis and processes controlled by transposases. Interestingly, the formation of pseudogenes in the spheroid body has occurred in the presence of intact, and presumably functional, recA and recF genes. This is in contrast to the situation in most investigated obligate intracellular bacterium-eukaryote symbioses, where at least either recA or recF has been eliminated.ConclusionOur analyses suggest highly specific targeting/loss of individual genes during the process of genome reduction and establishment of a cyanobacterial endosymbiont inside a eukaryotic cell. Our findings confirm, at the genome level, earlier speculation on the obligate intracellular status of the spheroid body in Rhopalodia gibba. This association is the first example of an obligate cyanobacterial symbiosis involving nitrogen fixation for which genomic data are available. It represents a new model system to study molecular adaptations of genome evolution that accompany a switch from free-living to intracellular existence.

Highlights

Bacteria occur in facultative association and intracellular symbiosis with a diversity of eukaryotic hosts
A diverse range of genetic modifications have occurred in the genome of R. gibba spheroid bodies and these would compromise the ability of the endosymbiont to exist as a free-living cyanobacterium, thereby confirming their suspected obligate status
Our findings provide insight into the genome evolution of a nitrogen-fixing endosymbiontic cyanobacterium living within a unicellular eukaryotic host

Summary

Introduction

Bacteria occur in facultative association and intracellular symbiosis with a diversity of eukaryotic hosts. The genomes of obligate intracellular bacteria often show an accumulation of deleterious mutations and a higher AT-ratio, accompanied with reduction in genome size when compared to their free-living relatives [6]. The dimension of these processes can be as extreme as seen in the reduced genome of Buchnera sp., an endosymbiont of aphids with a genome size of 641 kbp [7,8] and Carsonella, a γ-proteobacterial symbiont of phloem sapfeeding insects with a genome size of only 160 kbp [9]. Unlike the genomes of Buchnera and Carsonella, the genomes of these endosymbionts do not exhibit unusually high AT content

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