Abstract
Ticks (order Ixodida) vector pathogenic bacteria that cause diseases in humans and other mammals. They also contain bacteria that are closely related to pathogens but function as endosymbionts that provide nutrients that are missing from mammalian blood—their sole food source. For instance, mammalian pathogens such as Coxiella burnetii and Francisella tularensis, as well as Coxiella-like and Francisella-like endosymbionts (CLEs and FLEs, respectively) occur in ticks worldwide. However, it is not clear whether the pathogens evolved from symbionts or symbionts from pathogens. Recent studies have indicated that C. burnetii likely originated from a tick-associated ancestor, but the origins of FLEs are not clear. In this study, we sequenced the genome of an FLE, termed FLE-Am, present in the Gulf Coast tick, Amblyomma maculatum. We show that FLE-Am likely evolved from a pathogenic strain of Francisella, indicating that tick endosymbionts can evolve from mammalian pathogens. Although the genome of FLE-Am is almost the same size as the genomes of pathogenic Francisella strains, about one-third of its protein-coding genes contain inactivating mutations. The relatively low coding capacity and extensive metabolic capabilities indicate that FLE-Am transitioned recently to its current endosymbiotic lifestyle and likely replaced an ancient endosymbiont with degraded functionality.
Highlights
To identify the evolutionary relationship between pathogenic Francisella and FLE-Am, we examined the FLE-Am genome for the presence of virulence genes described in F. tularensis and F. novicida[13,14]
We discovered that FLE-Am contained pseudogenized versions of several virulence genes, including genes for a Type VI Secretion System present on a pathogenicity island in F. tularensis and for Type 4 pili that are critical to mammalian infection (Fig. 2, Supplementary Table S2)
In long-term endosymbionts such as a CLE in A. americanum (CLEAA)[3], and the presence of large number of pseudogenes imply that the bacterium is in the initial stages of reductive evolution, as superfluous genes are first pseudogenized and deleted from the genome when a bacterium shifts from a free-living to a host-associated lifestyle
Summary
We analyzed the A. maculatum microbiome and discovered that FLE-Am dominates the tick microbiome. Out of the 4,603 (>1 kb) contigs assembled from the sequencing reads, a vast majority was of host origin. 48 contigs were of bacterial origin, and out of those 46 belonged to Francisellacae (Supplementary Table S1). FLE-Am has been previously shown to be the major bacterium present in A. maculatum[8], and FLEs are maternally transmitted[10], indicating that it is essential to the normal development of A. maculatum. We estimated the phylogenetic position of FLE-Am using 442 orthologous proteins present in 44 fully sequenced Francisella genomes. FLE-Am shares a recent common ancestor with Francisella species that are pathogenic to mammals, with the exclusion of aquatic Francisella species. F. noatunensis orientalis LADL-07-285A F. noatunensis orientalis FNO190 F. noatunensis orientalis Toba 04 F. noatunensis orientalis FNO01 F. noatunensis orientalis FNO24 F. noatunensis orientalis FNO12 F. philomiragia philomiragia GA01-2794 F. philomiragia philomiragia ATCC 25015 O#319L F. philomiragia philomiragia GA01-2801 F. philomiragia philomiragia O#319-036 [FSC 153] F. philomiragia philomiragia ATCC 25017 F. philomiragia philomiragia O#319-067 F. philomiragia philomiragia O#319-029
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