The genome sequence of Rickettsia prowazekii and the origin of mitochondria

Abstract

We describe here the complete genome sequence (1,111,523 base pairs) of the obligate intracellular parasite Rickettsia prowazekii, the causative agent of epidemic typhus. This genome contains 834 protein-coding genes. The functional pro®les of these genes show similarities to those of mitochondrial genes: no genes required for anaerobic glycolysis are found in either R. prowazekii or mitochondrial genomes, but a complete set of genes encoding components of the tricarboxylic acid cycle and the respiratory-chain complex is found in R. prowazekii. In effect, ATP production in Rickettsia is the same as that in mitochondria. Many genes involved in the biosynthesis and regulation of biosynthesis of amino acids and nucleosides in free-living bacteria are absent from R. prowazekii and mitochondria. Such genes seem to have been replaced by homologues in the nuclear (host) genome. The R. prowazekii genome contains the highest proportion of non-coding DNA (24%) detected so far in a microbial genome. Such non-coding sequences may be degraded remnants of`neutralized' genes that await elimination from the genome. Phylogenetic analyses indicate that R. prowazekii is more closely related to mitochondria than is any other microbe studied so far.The Rickettsia are a-proteobacteria that multiply in eukaryotic cells only. R. prowazekii is the agent of epidemic, louse-borne typhus in humans. Three features of this endocellular parasite deserve our attention. First, R. prowazekii is estimated to have infected 20±30 million humans in the wake of the First World War and killed another few million following the Second World War (ref. 1). Because it is the descendent of free-living organisms 2±4 , its genome provides insight into adaptations to the obligate intracellular lifestyle, with probable practical value. Second, phylogenetic analyses based on sequences of ribosomal RNA and heat-shock proteins indicate that mitochondria may be derived from the aproteobacteria 5,6 . Indeed, the closest extant relatives of the ancestor to mitochondria seem to be the Rickettsia 7±10 . That modern Rickettsia favour an intracellular lifestyle identi®es these bacteria as the sort of organism that might have initiated the endosymbiotic scenario leading to modern mitochondria 11 . Finally, the genome of R. prowazekii is a small one, containing only 1,111,523 base pairs (bp). Its phylogenetic placement and many other characteristics identify it as a descendant of bacteria with substantially larger genomes 2±4 . Thus Rickettsia, like mitochondria, are good examples of highly derived genomes, the products of several types of reductive evolution.The genome sequence of R. prowazekii indicates that these three features may be related. For example, prokaryotic genomes evolving within a cell dominated by a much larger, eukaryote genome and constrained by bottle-necked population dynamics will tend to lose genetic information 12,13 . Predictable sets of expendable genes will tend to disappear from the prokaryotic genome when they are made redundant by the activit...

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

“…We classified W. glossinidia coding sequences into functional categories and compared them to the profiles of two other intracellular genomes, the obligate Buchnera and the parasite Rickettsia prowazekii 20 (Fig. 4).…”

Metabolic integration during the evolutionary origin of mitochondria

“…For example, cytochrome c is encoded in nuclear DNA but has features diagnostic of a-Proteobacteria, and specifically of the Rhodospirillaceae family of purple sulfur bacteria [23]. [24]. The branching sequence indicates that mitochondria diverged most recently from the intracellular parasite Rickettsia.…”

Duplication and Quadruplication of Arabidopsis thaliana Cysteinyl- and Asparaginyl-tRNA Synthetase Genes of Organellar Origin

“…6A) strongly suggest that SYNO ARATH derives from a plastid gene. Unlike cyanobacteria, bacteria close to the presumed ancestor of mitochondria [e.g., Rickettsia (Andersson et al 1998;Gray 1998)] lack an AsnRS and thus mitochondria probably also lacked an AsnRS to start with. This is not entirely certain, however, as the yeast mitochondrial AsnRS shows some similarity to bacterial enzymes and may be of mitochondrial origin.…”