Evolution ofWolbachiamutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas

Abstract

Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae, wCfeT and wCfeJ, found co-infecting cat fleas (Ctenocephalides felis) of the Elward Laboratory colony (Soquel, CA, USA). wCfeT is basal to nearly all described Wolbachia supergroups, while wCfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of Wolbachia host associations. wCfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the Wolbachia tree, indicating parallel evolution towards mutualism. Alternately, wCfeJ harbors a toxin-antidote operon analogous to the wPip cinAB operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies. wCfeJ cinB and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain Wolbachia strains and Rickettsia species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the C. felis genome itself contains two CI-like antidote genes, divergent from wCfeJ cinA, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (wCfeT/wCfeJ) amongst C. felis colonies, though fleas in wild populations mostly harbor wCfeT alone. Collectively, genomes of wCfeT, wCfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism.

Prevalence and relationship of endosymbiotic Wolbachia in the butterfly genus Erebia

“…Branch length in coalescence units, with terminal branches arbitrarily set at the default value 10. Capital letters depict Wolbachia supergroups (taken from [ 56 ]) …”

“…The included genomes covered five of the 16 known Wolbachia supergroups (i.e. groups A, B, E, F and L; [ 56 ]). We identified all single copy orthologs across all Wolbachia genomes with OrthoFinder [ 57 ].…”

Unpacking the intricacies of Rickettsia–vector interactions

“…[83]. Like the common louse endosymbiont (Candidatus Riesia), wolbachiae are known to provide essential biosynthetic pathways lacking in the blood meal, such as B vitamins, to its insect host [84,85]. Furthermore, Wolbachia spp.…”

“…Furthermore, Wolbachia spp. manipulate insect reproductive fitness, potentially influencing disease ecology [80,85]. While the interaction between competitive, vertically transmitted wolbachiae and rickettsiae has recently been examined in parasitoid wasps [86], the interaction remains understudied in fleas.…”

Horizontal gene transfer-mediated bacterial strain variation affects host fitness in Drosophila

“…The most prominent may be the acquisition of vitamin B7 (biotin) and vitamin B2 (riboflavin) synthesis by planthopper-associated Wolbachia [ 73 ]. Similarly, bed bug-associated Wolbachia [ 74 ] and cat flea-associated Wolbachia seem to have gained the ability to produce biotin via HGT [ 75 ]. In ticks, pabA (and possibly pabB ) required for the synthesis of folic acid was acquired by a Coxiella -like symbiont through horizontal gene transfer (HGT) from an Alphaproteobacterium [ 76 ] and is thought to affect tick fitness.…”