A substrate ambiguous enzyme facilitates genome reduction in an intracellular symbiont

Abstract

BackgroundGenome evolution in intracellular microbial symbionts is characterized by gene loss, generating some of the smallest and most gene-poor genomes known. As a result of gene loss these genomes commonly contain metabolic pathways that are fragmented relative to their free-living relatives. The evolutionary retention of fragmented metabolic pathways in the gene-poor genomes of endosymbionts suggests that they are functional. However, it is not always clear how they maintain functionality. To date, the fragmented metabolic pathways of endosymbionts have been shown to maintain functionality through complementation by host genes, complementation by genes of another endosymbiont and complementation by genes in host genomes that have been horizontally acquired from a microbial source that is not the endosymbiont. Here, we demonstrate a fourth mechanism.ResultsWe investigate the evolutionary retention of a fragmented pathway for the essential nutrient pantothenate (vitamin B5) in the pea aphid, Acyrthosiphon pisum endosymbiosis with Buchnera aphidicola. Using quantitative analysis of gene expression we present evidence for complementation of the Buchnera pantothenate biosynthesis pathway by host genes. Further, using complementation assays in an Escherichia coli mutant we demonstrate functional replacement of a pantothenate biosynthesis enzyme, 2-dehydropantoate 2-reductase (E.C. 1.1.1.169), by an endosymbiont gene, ilvC, encoding a substrate ambiguous enzyme.ConclusionsEarlier studies have speculated that missing enzyme steps in fragmented endosymbiont metabolic pathways are completed by adaptable endosymbiont enzymes from other pathways. Here, we experimentally demonstrate completion of a fragmented endosymbiont vitamin biosynthesis pathway by recruitment of a substrate ambiguous enzyme from another pathway. In addition, this work extends host/symbiont metabolic collaboration in the aphid/Buchnera symbiosis from amino acid metabolism to include vitamin biosynthesis.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0110-4) contains supplementary material, which is available to authorized users.

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

“…Neither B. tabaci nor its primary endosymbiont Portiera apparently possesses the canonical gene, panE , mediating the intermediate step. However, Portiera does have ilvC , which has been shown to mediate the panE reaction in another symbiotic bacterium ( Buchnera in aphids) [51], suggesting that B. tabaci - Portiera association may be capable of pantothenate synthesis by a shared metabolic pathway between the horizontally acquired gene in the insect genome and the symbiont gene (Fig. 4b).…”

Evaluation of the reference genes for expression analysis using quantitative real‐time polymerase chain reaction in the green peach aphid, Myzus persicae

“…Previous studies also found that ribosomal protein S3A and EF‐1α showed significant difference between the bacteriocyte and the whole body in pea aphid (Nakabachi et al ., ). Similarly, GAPDH has been consistently used as an ideal reference gene across a range of experiment treatments (Price & Wilson, ). In the reference analyses in P. xylostella , GAPDH was ranked as the most stable reference gene under mechanical injury.…”

microRNA regulation in an ancient obligate endosymbiosis

“…4.1.1.50), an enzyme involved in the production of spermine and spermidine from the essential amino acid methionine. In the context of the aphid/ Buchnera symbiosis, (i) spermine is a metabolic precursor for the biosynthesis of β‐alanine, a β amino acid that Buchnera has lost the ability to synthesize but requires for pantothenate (B5) biosynthesis (Price & Wilson, ); and (ii) spermidine is a metabolic precursor of putrescine, an aphid‐synthesized metabolite required for the Buchnera ‐mediated biosynthesis of adenine (Macdonald et al., ; Ramsey et al., ).…”