Evolutionary origin of insect– Wolbachia nutritional mutualism

Abstract

Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitaminmanipulated blood meals via an artificial feeding system, demonstrated that wCle certainly synthesizes biotin, and the wCleprovisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.

Extensive Mitochondrial Heteroplasmy in Natural Populations of a Resurging Human Pest, the Bed Bug (Hemiptera: Cimicidae)

“…The ease of maintaining bed bugs in laboratory cultures, and the availability of isolated populations and museum specimens makes C. lectularius an excellent model organism for the study of the origins and maintenance of mitochondrial heteroplasmy. C. lectularius may also contribute to a better understanding of the roles of environmental factors (e.g., temperature, starvation, Wolbachia infection; Nikoh et al 2014] in facilitating, maintaining, and purging paternal mtDNA. Fig.…”

Small genome symbiont underlies cuticle hardness in beetles

“…Histological analyses were conducted as described (28,71). Symbiont genome sequencing and annotation were performed as described (72)(73)(74)(75). Transcriptomic data of the host bacteriomes were obtained by RNA sequencing using TruSeq RNA Sample Preparation Kit v2 (Illumina) and HiSeq2000 sequencer (Illumina), and analyzed using the program Trinity (76) implemented in the MASER pipeline (cell-innovation.nig.ac.jp/).…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…Two examples that have caught the attention of evolutionary biologists involve the bedbug Cimex lectularius (Hosokawa et al, 2010;Nikoh et al, 2014) and the parasitic wasp Asobara tabida (Dedeine et al, 2001). In the bedbug C. lectularius, Wolbachia fullfils a role of dietary provisioner of vitamin B (Hosokawa et al, 2010) and biotin (Nikoh et al, 2014). Hosokawa and colleagues found that reduction or elimination of Wolbachia through antibiotic treatment rendered animals incapable of producing normally developing eggs, which could be restored by dietary supplementation of vitamin B.…”

“…Such sexual asymmetry in favor of females is similar in principle to that between mitochondrial and nuclear genomes, where mitochondrial DNA (mtDNA) mutations can be maintained when favorable in females, even if they are harmful in males (Gemmell et al, 2004). Wolbachia-host associations therefore provide an opportunity to explore the coevolutionary processes that concur with intracellular lifestyles (Sicard et al, 2014) with new knowledge of Wolbachia biology coming from bacterial genome analysis (e.g., Wu et al, 2004;Ellegaard et al, 2013;Nikoh et al, 2014;Ramírez-Puebla et al, 2015).…”