Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed γ-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the γ-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.B vitamins | bacteriome | Cimex lectularius | nutritional mutualism
The smallest reported bacterial genome belongs to Tremblaya princeps, a symbiont of Planococcus citri mealybugs (PCIT). Tremblaya PCIT not only has a 139 kb genome, but possesses its own bacterial endosymbiont, Moranella endobia. Genome and transcriptome sequencing, including genome sequencing from a Tremblaya lineage lacking intracellular bacteria, reveals that the extreme genomic degeneracy of Tremblaya PCIT likely resulted from acquiring Moranella as an endosymbiont. In addition, at least 22 expressed horizontally transferred genes from multiple diverse bacteria to the mealybug genome likely complement missing symbiont genes. However, none of these horizontally transferred genes are from Tremblaya, showing that genome reduction in this symbiont has not been enabled by gene transfer to the host nucleus. Our results thus indicate that the functioning of this three-way symbiosis is dependent on genes from at least six lineages of organisms and reveal a path to intimate endosymbiosis distinct from that followed by organelles.
Ecological studies on three bacterial lineages symbiotic in aphids have shown that they impose a variety of effects on their hosts, including resistance to parasitoids and tolerance to heat stress. Phylogenetic analyses of partial sequences of gyrB and recA are consistent with previous analyses limited to 16S rRNA gene sequences and yield improved confidence of the evolutionary relationships of these symbionts. All three symbionts are in the Enterobacteriaceae. One of the symbionts, here given the provisional designation "Candidatus Serratia symbiotica," is a Serratia species that has acquired a symbiotic lifestyle. The other two symbionts, here designated "Candidatus Hamiltonella defensa" and "Candidatus Regiella insecticola," are sister groups to one another and together show a relationship to species of Photorhabdus.Recent genomic and phylogenetic studies suggest that associations with arthropods have played a role in the evolution of the Enterobacteriaceae (see, e.g., Duchaud et al. [11]). Aphids, psyllids, scale insects, whiteflies, weevils, and other insects all harbor various maternally transmitted Enterobacteriaceae, distributed sporadically or ubiquitously within a particular host species (5,20,28,29,36,37,39). To date, very few of these symbionts have been successfully cultured and characterized outside of hosts, with the exceptions of Arsenophonus nasoniae, the facultative symbiont of a parasitoid wasp (15), and Sodalis glossinidius, the secondary symbiont of tsetse, a blood-feeding fly that vectors trypanosomes (6). ("Secondary" symbionts are so named because they coexist with a "primary" symbiont that appears to represent a more ancient infection of the same host lineage.) These symbiotic lineages represent a number of independent infections of arthropod hosts, with each cluster occurring in several diverse insect groups. For example, phylogenies derived from 16S rRNA gene sequences indicate that the closest known relatives of Sodalis are the primary symbionts of grain weevils in the genus Sitophilus, followed by facultative symbionts of sap-feeding insects (28). Likewise, the cluster corresponding to the genus Arsenophonus has representatives in parasitoid hymenopterans (A. nasoniae) and also in a wide variety of hemipterans such as assassin bugs, aphids, psyllids, and whiteflies (15,17,28,31,34,37,39,46).Aphids provide the best-studied instance in which Enterobacteriaceae form heritable symbioses that are facultative for the host insects. Almost all aphids contain a primary symbiont, Buchnera aphidicola, and many also contain secondary symbionts from one of three groups of Enterobacteriaceae, with members of each group showing near-identity of 16S rRNA gene sequences (29). All three types of symbiont are known from the pea aphid, Acyrthosiphon pisum, as well as from a wide variety of different species and subfamilies of aphids (16,28,29,40), with a few records from other insect hosts. Although the mechanisms of transfer in nature are not known, the symbionts can be cured or transferred among hosts...
Almost all aphids harbour an endosymbiotic bacterium, Buchnera aphidicola, in bacteriocytes. Buchnera synthesizes essential nutrients and supports growth and reproduction of the host. Over the long history of endosymbiosis, many essential genes have been lost from the Buchnera genome, resulting in drastic genome reduction and the inability to live outside the host cells. In turn, when deprived of Buchnera, the host aphid suffers retarded growth and sterility. Buchnera and the host aphid are often referred to as highly integrated almost inseparable mutualistic partners. However, we discovered that, even after complete elimination of Buchnera, infection with a facultative endosymbiotic gamma-proteobacterium called pea aphid secondary symbiont (PASS) enabled survival and reproduction of the pea aphid. In the Buchnera-free aphid, PASS infected the cytoplasms of bacteriocytes that normally harbour Buchnera, establishing a novel endosymbiotic system. These results indicate that PASS can compensate for the essential role of Buchnera by physiologically and cytologically taking over the symbiotic niche. By contrast, PASS negatively affected the growth and reproduction of normal host aphids by suppressing the essential symbiont Buchnera. These findings illuminate complex symbiont-symbiont and host-symbiont interactions in an endosymbiotic system, and suggest a possible evolutionary route to novel obligate endosymbiosis by way of facultative endosymbiotic associations.
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