Abstract
Insect lineages feeding on nutritionally restricted diets such as phloem sap, xylem sap, or blood, were able to diversify by acquiring bacterial species that complement lacking 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 of their host's nutritional requirements, driving the acquisition of additional symbiotic species. Phloem-feeding members of the insect family Aleyrodidae (whiteflies) established an obligate relationship with Candidatus Portiera aleyrodidarum, which provides its hots with essential amino acids and carotenoids. In addition, many whitefly species harbor additional endosymbionts which may potentially further supplement their host's diet. To test this hypothesis, genomes of several endosymbionts of the whiteflies Aleurodicus dispersus, Aleurodicus floccissimus and Trialeurodes vaporariorum were analyzed. In addition to Portiera, all three species were found to harbor one Arsenophonus and one Wolbachia endosymbiont. A comparative analysis of Arsenophonus genomes revealed that although all three 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 and pseudogenes, intermediate GC content, and mobile genetic elements. In contrast, Arsenophonus of A. dispersus belongs to a different lineage and displays the characteristics of a primary endosymbiont—a reduced genome (670 kb) with ~400 genes, 32% GC content, and no mobile genetic elements. However, the presence of 274 pseudogenes suggests that this symbiotic association is more recent than other reported primary endosymbionts of hemipterans. The gene repertoire of Arsenophonus of A. dispersus is completely integrated in the symbiotic consortia, and the biosynthesis of most vitamins occurs in shared pathways with its host. In addition, Wolbachia endosymbionts have also retained the ability to produce riboflavin, flavin adenine dinucleotide, and folate, and may make a nutritional contribution. Taken together, our results show that Arsenophonus hold a pivotal place in whitefly nutrition by their ability to produce B vitamins.
Highlights
Mutualistic, commensal, or parasitic relationships have been described in a diverse array of eukaryotes that are allied with bacterial symbionts (Moya et al, 2008)
A total of five endosymbiont metagenomeassembled genomes (MAGs) were recovered from the three studied whitefly species: Arsenophonus from A. dispersus (ARAD), A. floccissimus (ARAF) and T. vaporariorum (ARTV), and Wolbachia from A. dispersus (WBAD) and A. floccissimus (WBAF) (Figure 1 and Table 1)
Wolbachia had been previously detected by PCR in T. vaporariorum (SantosGarcia et al, 2015), its genome was impossible to assemble and analyze due to the low amount of recovered reads (Table S3)
Summary
Mutualistic, commensal, or parasitic relationships have been described in a diverse array of eukaryotes that are allied with bacterial symbionts (Moya et al, 2008). The class Insecta provides examples of mutualistic associations, and several lineages are known to have lived in intimate relationships with obligate symbionts for millions of years. Such symbionts are usually harbored inside specialized cells, termed bacteriocytes (sometimes organized as a bacteriome), and are vertically transmitted from the mother to her offspring. These bacterial symbionts, living inside cells and transmitted throughout long evolutionary periods, have been denoted primary (or obligatory) endosymbionts. When these requirements become vital, a secondary endosymbiont might become primary, resulting in a consortium of primary endosymbionts (Lamelas et al, 2011)
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