Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis , have microbial origins

Abstract

The shikimic acid pathway is responsible for the biosynthesis of many aromatic compounds by a broad range of organisms, including bacteria, fungi, plants, and some protozoans. Animals are considered to lack this pathway, as evinced by their dietary requirement for shikimate-derived aromatic amino acids. We challenge the universality of this traditional view in this report of genes encoding enzymes for the shikimate pathway in an animal, the starlet sea anemone Nematostella vectensis. Molecular evidence establishes horizontal transfer of ancestral genes of the shikimic acid pathway into the N. vectensis genome from both bacterial and eukaryotic (dinoflagellate) donors. Bioinformatic analysis also reveals four genes that are closely related to those of Tenacibaculum sp. MED152, raising speculation for the existence of a previously unsuspected bacterial symbiont. Indeed, the genome of the holobiont (i.e., the entity consisting of the host and its symbionts) comprises a high content of Tenacibaculum-like gene orthologs, including a 16S rRNA sequence that establishes the phylogenetic position of this associate to be within the family Flavobacteriaceae. These results provide a complementary view for the biogenesis of shikimate-related metabolites in marine Cnidaria as a ''shared metabolic adaptation'' between the partners. symbiosis ͉ Tenacibaculum ͉ Cnidaria

Activation of the cnidarian oxidative stress response by ultraviolet light, polycyclic aromatic hydrocarbons and crude oil

“…The differential sensitivity may be due to thicker or more pigmented tissue in adults, maturation of defense mechanisms, and/or the presence of greater energetic reserves to fuel defensive or cellular repair processes. Nematostella vectensis contains a suite of fluorescent proteins (Ikmi and Gibson, 2010) as well as enzymes needed to synthesize mycosporine-like amino acids (Starcevic et al, 2008). These compounds are photoprotective in other cnidarians (Salih et al, 2000;Shick and Dunlap, 2002), but their physiological role in N. vectensis has not been determined, and it is yet unknown how the photoprotective capacity varies during development.…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…The acquisition by the starlet sea anemone, Nematostella vectensis, of bacterial genes involved in the shikimic acid [14] and glyoxilate pathways [15] has been proposed from bioinformatics studies performed on the Nematostella genome. In addition, an interesting gene encoding a protein with mismatch repair activity has been postulated to be targeted to octocorals mitochondrial DNA [16], however, the gene donor or the relevance of gene function remains unknown.…”

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

“…Examples of HGT between unrelated or nonmating species are abundant among prokaryotes (10,11) but less so between prokaryotes and unicellular (12)(13)(14) or multicellular eukaryotes (15)(16)(17)(18)(19)(20). Most of these latter examples are associated with parasitism or phagotrophy, including the elegant studies of HGT from the ␣-proteobacteria Wolbachia to insects and nematodes (16)(17)(18), and the finding of rhizobial-like genes in plant parasitic nematodes (19,20).…”