Sequence of a Coxiella Endosymbiont of the Tick Amblyomma nuttalli Suggests a Pattern of Convergent Genome Reduction in the Coxiella Genus

Abstract

Ticks require bacterial symbionts for the provision of necessary compounds that are absent in their hematophagous diet. Such symbionts are frequently vertically transmitted and, most commonly, belong to the Coxiella genus, which also includes the human pathogen Coxiella burnetii. This genus can be divided in four main clades, presenting partial but incomplete cocladogenesis with the tick hosts. Here, we report the genome sequence of a novel Coxiella, endosymbiont of the African tick Amblyomma nuttalli, and the ensuing comparative analyses. Its size (∼1 Mb) is intermediate between symbionts of Rhipicephalus species and other Amblyomma species. Phylogenetic analyses show that the novel sequence is the first genome of the B clade, the only one for which no genomes were previously available. Accordingly, it allows to draw an enhanced scenario of the evolution of the genus, one of parallel genome reduction of different endosymbiont lineages, which are now at different stages of reduction from a more versatile ancestor. Gene content comparison allows to infer that the ancestor could be reminiscent of C. burnetii. Interestingly, the convergent loss of mismatch repair could have been a major driver of such reductive evolution. Predicted metabolic profiles are rather homogenous among Coxiella endosymbionts, in particular vitamin biosynthesis, consistently with a host-supportive role. Concurrently, similarities among Coxiella endosymbionts according to host genus and despite phylogenetic unrelatedness hint at possible host-dependent effects.

Keywords: Amblyomma nuttalli; Coxiella-like endosymbiont; comparative genomics; genome reduction; phylogeny; symbiont evolution.

Fig. 1

(A) Maximum likelihood MLST phylogenetic tree of Coxiella and other Legionellales, and (B) maximum likelihood phylogenomic tree of Coxiellaceae. In (A, B), the four major Coxiella clades are evidenced by different colors, numbers on branches stand for bootstrap support after 1,000 pseudoreplicates, CE stands for Coxiella endosymbiont, and respective host organisms are indicated. In (A), symbionts with available genomes are highlighted. In (B), scale bar stands for estimated proportional sequence divergence, and the bar plot on the right shows the respective coding (blue) and noncoding (red) genome sizes.