Diatom heterotrophy on brown algal polysaccharides emerged through horizontal gene transfer, gene duplication, and neofunctionalization

A major goal of evolutionary biology is to identify the genetic basis for the emergence of complex adaptive traits. Diatoms are ancestrally photosynthetic microalgae. However, in the genus Nitzschia, loss of photosynthesis led to a group of free-living secondary heterotrophs whose manner of acquiring chemical energy is unclear. Here, we sequence the genome of the non-photosynthetic diatom Nitzschia sing1 and identify the genetic basis for its catabolism of the brown algal cell wall polysaccharide alginate. N. sing1 obtained an endolytic alginate lyase enzyme by horizontal gene transfer (HGT) from a marine bacterium. Subsequent gene duplication through unequal crossing over and transposition led to 91 genes in three distinct gene families. One family retains the ancestral endolytic enzyme function. By contrast, the two others underwent domain duplication, gain, loss, rearrangement, and mutation to encode novel functions that can account for oligosaccharide import through the endomembrane system and the exolytic production of alginate monosaccharides. Together, our results show how a single HGT event followed by substantial gene duplication and neofunctionalization led to alginate catabolism and access to a new ecological niche.