Comparative Genomics Reveals Three Genetic Groups of the Whitefly Obligate Endosymbiont Candidatus Portiera aleyrodidarum

SIMPLE SUMMARY: Many obligate endosymbionts colonize an invertebrate host and are directly transferred maternally to the host’s embryo. Consequently, the symbiotic bacteria from diverse host species evolve independently, reflecting the host’s phylogeny. Whiteflies, which consist of thousands of species, harbor obligate endosymbionts of the Portiera genus. The divergence status of these bacteria, after a long history of coevolution with their hosts, remains ambiguous. In the present study, we aim to unravel the divergence of obligate endosymbionts from different whitefly species through genome comparison. Our findings indicate that these endosymbionts have diverged into at least three disparate genetic groups. Such findings underscore the divergence of whitefly obligate endosymbionts and provide a cue for investigation into the co-divergence between obligate endosymbionts and their hosts. ABSTRACT: Maternally inherited obligate endosymbionts codiverge with their invertebrate hosts and reflect their host’s evolutionary history. Whiteflies (Hemiptera: Aleyrodidae) harbor one obligate endosymbiont, Candidatus Portiera aleyrodidarum (hereafter Portiera). Portiera was anciently acquired by whitefly and has been coevolving with its host ever since. Uncovering the divergence of endosymbionts provides a fundamental basis for inspecting the coevolutionary processes between the bacteria and their hosts. To illustrate the divergence of Portiera lineages across different whitefly species, we sequenced the Portiera genome from Aleyrodes shizuokensis and conducted a comparative analysis on the basic features and gene evolution with bacterial genomes from five whitefly genera, namely Aleurodicus, Aleyrodes, Bemisia, Pealius, and Trialeurodes. The results indicated that Portiera from Bemisia possessed significantly larger genomes, fewer coding sequences (CDSs), and a lower coding density. Their gene arrangement differed notably from those of other genera. The phylogeny of the nine Portiera lineages resembled that of their hosts. Moreover, the lineages were classified into three distinct genetic groups based on the genetic distance, one from Aleurodicus (Aleurodicinae), one from Bemisia (Aleyrodinae), and another from Aleyrodes, Pealius, and Trialeurrodes (Aleyrodinae). Synonymous and nonsynonymous rate analyses, parity rule 2 plot analyses, neutrality plot analyses, and effective number of codons analyses supported the distinction of the three genetic groups. Our results indicated that Portiera from distant hosts exhibit distinct genomic contents, implying codivergence between hosts and their endosymbionts. This work will enhance our understanding of coevolution between hosts and their endosymbionts.