Bacteriome-associatedWolbachiaof the parthenogenetic termiteCavitermes tuberosus

Abstract

One sentence summary: The parthenogenetic termite Cavitermes tuberosus and the reproductive parasite Wolbachia are partners that likely engage in an intimate insect-bacteria nutritional partnership. † These authors contributed equally to this study. ‡ Simon Hellemans, http://orcid.org/0000-0003-1266-9134 § Nicolas Kaczmarek, ABSTRACTWolbachia has deeply shaped the ecology and evolution of many arthropods, and interactions between the two partners are a continuum ranging from parasitism to mutualism. Non-dispersing queens of the termite Cavitermes tuberosus are parthenogenetically produced through gamete duplication, a mode of ploidy restoration generally induced by Wolbachia. These queens display a bacteriome-like structure in the anterior part of the mesenteron. Our study explores the possibility of a nutritional mutualistic, rather than a parasitic, association between Wolbachia and C. tuberosus. We found a unique strain (wCtub), nested in the supergroup F, in 28 nests collected in French Guiana, the island of Trinidad and the state of Paraíba, Brazil (over 3500 km). wCtub infects individuals regardless of caste, sex or reproductive (sexual versus parthenogenetic) origin. qPCR assays reveal that Wolbachia densities are higher in the bacteriome-like structure and in the surrounding gut compared to other somatic tissues. High-throughput 16S rRNA gene amplicon sequencing reveals that Wolbachia represents over 97% of bacterial reads present in the bacteriome structure. BLAST analyses of 16S rRNA, bioA (a gene of the biosynthetic pathway of B vitamins) and five multilocus sequence typing genes indicated that wCtub shares 99% identity with wCle, an obligate nutritional mutualist of the bedbug Cimex lectularius.

The Jekyll and Hyde Symbiont: Could Wolbachia Be a Nutritional Mutualist?

“…In the literature, several metabolic pathways in the host have been speculated to be supplemented or modulated by Wolbachia (15,23,(27)(28)(29)(30)(31)(32), from B vitamins to nucleotides. Comparative genomics is a first step to identifying metabolic capabilities across Wolbachia strains that could be involved in nutritional mutualism.…”

“…Wolbachia is also bacteriocyte associated in the termite, infected by the related strain wCtub; this localization suggests that these specific symbionts may be nutritional mutualists. Interestingly, the bioA gene was amplified from the wCtub symbionts, suggesting that they may also harbor the biotin biosynthesis operon (30). This operon was unique to the F clade symbionts until the Wolbachia strains that infect Nomada bees (wNfla/wNleu) were sequenced (28).…”

Comparative screening of endosymbiotic bacteria associated with the asexual and sexual lineages of the termiteGlyptotermes nakajimai

“…Termites are diploid and typically have an XY sex determination system [11]. Notably, four of six examined termite species with facultative parthenogenesis do not appear to harbour endosymbiotic bacteria [12,13]. These results suggest that endosymbiotic bacteria are unlikely to be the inducers of parthenogenesis in termites.…”

Asexual Queen Succession in Termites

“…The evolution of AQS requires both the capacity to reproduce parthenogenetically (tychoparthenogenesis) and the developmental propensity of parthenogens to develop into neotenic queens (Nozaki et al 2018). In termites, evidence points towards queens to be intrinsically able to reproduce parthenogenetically, rather than induced by intracellular Asexual queen succession in termites (A29115) 9 endosymbiotic bacteria (Matsuura et al 2004;Yashiro and Lo 2019;Hellemans et al 2019c).…”