A Rickettsia Genome Overrun by Mobile Genetic Elements Provides Insight into the Acquisition of Genes Characteristic of an Obligate Intracellular Lifestyle

Abstract

We present the draft genome for the Rickettsia endosymbiont of Ixodes scapularis (REIS), a symbiont of the deer tick vector of Lyme disease in North America. Among Rickettsia species (Alphaproteobacteria: Rickettsiales), REIS has the largest genome sequenced to date (>2 Mb) and contains 2,309 genes across the chromosome and four plasmids (pREIS1 to pREIS4). The most remarkable finding within the REIS genome is the extraordinary proliferation of mobile genetic elements (MGEs), which contributes to a limited synteny with other Rickettsia genomes. In particular, an integrative conjugative element named RAGE (for Rickettsiales amplified genetic element), previously identified in scrub typhus rickettsiae (Orientia tsutsugamushi) genomes, is present on both the REIS chromosome and plasmids. Unlike the pseudogene-laden RAGEs of O. tsutsugamushi, REIS encodes nine conserved RAGEs that include F-like type IV secretion systems similar to that of the tra genes encoded in the Rickettsia bellii and R. massiliae genomes. An unparalleled abundance of encoded transposases (>650) relative to genome size, together with the RAGEs and other MGEs, comprise ϳ35% of the total genome, making REIS one of the most plastic and repetitive bacterial genomes sequenced to date. We present evidence that conserved rickettsial genes associated with an intracellular lifestyle were acquired via MGEs, especially the RAGE, through a continuum of genomic invasions. Robust phylogeny estimation suggests REIS is ancestral to the virulent spotted fever group of rickettsiae. As REIS is not known to invade vertebrate cells and has no known pathogenic effects on I. scapularis, its genome sequence provides insight on the origin of mechanisms of rickettsial pathogenicity.

Small Regulatory RNAs of Rickettsia conorii

“…R. conorii genome harbors a single chromosome of 1268755 bp encoding for 1578 protein coding genes, 9 pseudogenes, 33 tRNAs, 2 rRNAs, and contains ~32% intergenic region910. This relatively high percentage of non-coding region in R. conorii and other rickettsial genomes has traditionally been considered to be the ‘junk DNA’ or defunct genes resulting from reductive evolution and pseudogenization711121314. However, recent advances in computational bioinformatics and bacterial molecular genetics have led to the appreciation that the intergenic regions, in addition to harboring transcription factor binding sites and mobile genetic elements, encode for small non-coding RNAs involved in the regulation of target genes.…”

Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts

“…5-40% of arthropod species (Goodacre et al, 2006;Weinert et al, 2007;Duron et al, 2008a;Zug and Hammerstein, 2012). The constitution of their genomes is dynamic, with flexible gene content and rampant intra-generic recombination, indicating accelerated rates of diversification and adaptability (Wu et al, 2004;Klasson et al, 2008;Felsheim et al, 2009;Klasson et al, 2009;Gillespie et al, 2012;Penz et al, 2012;Duplouy et al, 2013). Remarkably, mobile genetic elements represent substantial fractions of these genomes (Bordenstein and Reznikoff, 2005;Wernegreen, 2005;Moran et al, 2008) as exemplified with insertion sequences (ISs), a group of genetically compact transposable elements encoding no functions other than an enzyme that catalyzes their own transposition (Felsheim et al, 2009;Cerveau et al, 2011b).…”

Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-Like, Arsenophonus-Like, and Rickettsia-Like Symbionts

“…To date, a wide range of symbionts, such as Coxiella-like (13), Francisella-like (14), Wolbachia-like (15), Rickettsia-like (16), Arsenophonus-like (17), "Candidatus Midichloria mitochondrii" (18), and Rickettsia peacockii (19) symbionts, have been detected in several tick species. However, little attention has been given to coinfection with multiple symbionts of ticks.…”