Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci

Abstract

BackgroundThe whitefly Bemisia tabaci is an important agricultural pest with global distribution. This phloem-sap feeder harbors a primary symbiont, “Candidatus Portiera aleyrodidarum”, which compensates for the deficient nutritional composition of its food sources, and a variety of secondary symbionts. Interestingly, all of these secondary symbionts are found in co-localization with the primary symbiont within the same bacteriocytes, which should favor the evolution of strong interactions between symbionts.ResultsIn this paper, we analyzed the genome sequences of the primary symbiont Portiera and of the secondary symbiont Hamiltonella in the B. tabaci Mediterranean (MED) species in order to gain insight into the metabolic role of each symbiont in the biology of their host. The genome sequences of the uncultured symbionts Portiera and Hamiltonella were obtained from one single bacteriocyte of MED B. tabaci. As already reported, the genome of Portiera is highly reduced (357 kb), but has kept a number of genes encoding most essential amino-acids and carotenoids. On the other hand, Portiera lacks almost all the genes involved in the synthesis of vitamins and cofactors. Moreover, some pathways are incomplete, notably those involved in the synthesis of some essential amino-acids. Interestingly, the genome of Hamiltonella revealed that this secondary symbiont can not only provide vitamins and cofactors, but also complete the missing steps of some of the pathways of Portiera. In addition, some critical amino-acid biosynthetic genes are missing in the two symbiotic genomes, but analysis of whitefly transcriptome suggests that the missing steps may be performed by the whitefly itself or its microbiota.ConclusionsThese data suggest that Portiera and Hamiltonella are not only complementary but could also be mutually dependent to provide a full complement of nutrients to their host. Altogether, these results illustrate how functional redundancies can lead to gene losses in the genomes of the different symbiotic partners, reinforcing their inter-dependency.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1379-6) contains supplementary material, which is available to authorized users.

Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica

“…Finally, within-pathway complementation might exist between AqS1 and AqS2, as has also been reported in other (non-sponge) symbionts (Wu et al, 2006;Rao et al, 2015). For example, enzyme-encoding genes that participate in the production of aromatic amino acids are present in the AqS1, but not in the AqS2, genome, suggesting that each symbiont could synthesize particular amino acids provided that the metabolism of the other supplies the intermediate substrates.…”

“…For example, enzyme-encoding genes that participate in the production of aromatic amino acids are present in the AqS1, but not in the AqS2, genome, suggesting that each symbiont could synthesize particular amino acids provided that the metabolism of the other supplies the intermediate substrates. It has been postulated that metabolic redundancies existing within symbiotic partners upon host initial acquisition might be lost over time, resulting in mutual dependence to produce compounds essential to their host (Wu et al, 2006;Rao et al, 2015). Alternatively, the function of the missing genes could be performed by other genes encoded in their respective genomes, either by a novel enzyme, or by an already-known enzyme that would have changed or extended its prior function by co-option (Charles et al, 2011;Sloan and Moran, 2012;Rao et al, 2015).…”

“…In non-sponge host-symbiont systems, the temporal stability of associations involving two or more unrelated bacterial symbionts (Takiya et al, 2006;Wu et al, 2006;Dubilier et al, 2008;Zimmermann et al, 2014) has been postulated to involve the use of different energy sources to reduce competition between the bacterial species (Duperron et al, 2006;Kleiner et al, 2012b). It has also been suggested that some symbionts might rely on one another for their metabolism, in a mutual dependency resulting from loss of metabolic redundancies that originally existed within symbiotic partners at the time of their acquisition by the host (Wu et al, 2006;Rao et al, 2015). The extent to which these phenomena occur in sponge symbionts is currently largely unknown.…”

Winding paths to simplicity: genome evolution in facultative insect symbionts

“…2012) and their coresidence with Portiera in the primary bacteriocytes (Rao et al. 2015), all support that these whitefly associated ‘ Ca . Hamiltonella defensa’ have provided yet another example of evolutionary transition from facultative symbionts to obligate mutualists.…”

“…Through genome analysis of two whitefly associated strains, MED (Rao et al. 2012, 2015) and MEAM1 (Rollat-Farnier et al. 2015), it was found that these whitefly associated ‘ Ca .…”