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.
Highlights
Genome evolution in intracellular microbial symbionts is characterized by gene loss, generating some of the smallest and most gene-poor genomes known
Buchnera with fully sequenced genomes fall into two groups: (1) those from species such as Baizongia pistaciae, C. cedri and Uroleucon ambrosiae that have lost the whole pantothenate biosynthesis pathway [4,28,29]; and (2) those from species such as A. pisum, Myzus persicae and Schizaphis graminum that retain identically fragmented pathways characterized by loss of panD, panE and ilvE [12,30,31] (Figure 1)
Evolutionary retention by multiple Buchnera lineages of identically fragmented pantothenate biosynthesis pathways that include two genes that only function in pantothenate biosynthesis, led us to hypothesize that the pantothenate biosynthesis pathway in these species is functional
Summary
Genome evolution in intracellular microbial symbionts is characterized by gene loss, generating some of the smallest and most gene-poor genomes known. The evolutionary retention of fragmented metabolic pathways in the gene-poor genomes of endosymbionts suggests that they are functional. It is not always clear how they maintain functionality. The smallest known bacterial genomes, containing fewer than 200 protein-coding genes, belong to insect associated obligate endosymbionts [6,7,9,10]. Eliminated genes include those that are either functionally redundant, or not essential for maintenance of the symbiosis [1,2,3]. Even endosymbiont essential nutrient biosynthesis pathways experience gene loss such that it is common to find fragmented, but evolutionary retained, pathways that appear incomplete and non-functional [11,12]
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