Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas.

Timothy P Driscoll,John F Beckmann,Mariah Plumer,Spiridon E Sevdalis,Victoria I Verhoeve,Darin L Shrewsberry,Abdu F Azad,Laura M Krueger,Joseph J Gillespie,Kevin R Macaluso,Cassia Brockway

doi:10.7717/peerj.10646

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.

Highlights

Wolbachiae (Alphaproteobacteria: Rickettsiales: Anaplasmataceae) comprise Gramnegative, obligate intracellular bacteria that infect over half the world’s described insect species as well as certain parasitic nematodes (Hilgenboecker et al, 2008)
While riboflavin biosynthesis genes are highly conserved in wolbachiae (Newton & Rice, 2020), biotin biosynthesis genes are rare and likely originated via lateral gene transfer (LGT) with taxonomically divergent intracellular bacteria (Gillespie et al, 2012)
Wolbachia genes underpinning cytoplasmic incompatibility (CI) and male killing have been characterized (Chen et al, 2019; Beckmann et al, 2019; LePage et al, 2017; Beckmann, Ronau & Hochstrasser, 2017; Beckmann & Fallon, 2013; Perlmutter et al, 2019) and occur predominantly in the eukaryotic association module (EAM) of Wolbachia prophage genomes (Bordenstein & Bordenstein, 2016). These genes highlight the role of LGT in providing wolbachiae with factors facilitating mutualism or reproductive parasitism (RP), both of which are highly successful strategies for increasing infection frequency in invertebrate host populations

Summary

Introduction

Wolbachiae (Alphaproteobacteria: Rickettsiales: Anaplasmataceae) comprise Gramnegative, obligate intracellular bacteria that infect over half the world’s described insect species as well as certain parasitic nematodes (Hilgenboecker et al, 2008). Like other obligate intracellular microbes, wolbachiae are metabolic parasites that complement a generally reduced metabolism with pilfering of host metabolites (Driscoll et al, 2017; Jiménez et al, 2019) Their ability to survive and flourish is heavily influenced by the acquisition of key functions through lateral gene transfer (LGT). Wolbachia genes underpinning CI and male killing have been characterized (Chen et al, 2019; Beckmann et al, 2019; LePage et al, 2017; Beckmann, Ronau & Hochstrasser, 2017; Beckmann & Fallon, 2013; Perlmutter et al, 2019) and occur predominantly in the eukaryotic association module (EAM) of Wolbachia prophage genomes (Bordenstein & Bordenstein, 2016) These genes highlight the role of LGT in providing wolbachiae with factors facilitating mutualism or RP, both of which are highly successful strategies for increasing infection frequency in invertebrate host populations

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Conclusion