To B or not to B: Arsenophonus as a source of B-vitamins in whiteflies.
1Insect lineages feeding on nutritionally restricted diets such as phloem, xylem, or blood, were able to diversify by acquiring bacterial species that complemented the missing nutrients. These bacteria, considered obligate/primary endosymbionts, share a long evolutionary history with their hosts. In some cases, however, these endosymbionts are not able to fulfill all the nutritional requirements of their host, driving the acquisition of additional symbiotic species. Whiteflies, which feed on phloem, established an obligate relationship with Candidatus Portiera aleyrodidarum, who provides essential amino acids and carotenoids to the host. As many Whiteflies species harbor additional endosymbionts, they could provide their hosts with missing nutrients. To test this hypothesis, genomes of several endosymbionts from the whiteflies Aleurodicus dispersus, A. floccissimus and Trialeurodes vaporariorum were sequenced and analyzed. All three species were found to harbor an endosymbiont from the genus Arsenophonus, and the two former also host Wolbachia. A comparative analysis of the three Arsenophonus genomes revealed that although all of them are capable of synthesizing B-vitamins and cofactors, such as pyridoxal, riboflavin, or folate, their genomes and phylogenetic relationship vary greatly. Arsenophonus of A. floccissimus and T. vaporariorum belong to the same clade and display characteristics of facultative endosymbionts, such as large genomes (3 Mb) with thousands of genes, many pseudogenes, intermediate GC content, and mobile genetic elements (MGEs). In contrast, Arsenophonus of A. dispersus belongs to a different lineage and displays the characteristics of a primary endosymbiont, such as a reduced genome (670 kb) with 400 genes, 32% GC content, and no MGEs. However, the presence of 274 pseudogenes suggests that this symbiotic association is more recent than other reported hemipterans primary endosymbionts. Arsenophonus of A. dispersus gene repertoire is completely integrated in the symbiotic consortia, and the biosynthesis of most vitamins occurs in shared pathways with its host. In addition, Wolbachia have also retained the ability to produce riboflavin, FAD, and folate, and may have a nutritional contribution. Taken together, our results show that Arsenophonus have a pivotal place in whiteflies nutrition by their ability to produce B-vitamins, even if they diverge and/or go through a genome reduction process.