Phylogenomics Untangles the Metabolic Potential of Picochlorum tauri, a New Picoalgal Species Causing a Winter Bloom in the Mediterranean Thau Lagoon

Abstract

In the winter of 2018–2019, the Mediterranean Thau lagoon experienced an intense green bloom with severe ecological consequences. Here, we aimed at identifying the blooming species and deciphering its metabolic potential. The blooming alga was identified by a metabarcoding approach and later isolated in an axenic form. High-quality nuclear and organellar genome sequences were generated. Phylogenetic and phylogenomic analyses revealed that the alga is a new member of the genus Picochlorum (Trebouxiophyceae, Chlorophyta) that we named Picochlorum tauri. Comparative genomic analyses were conducted to provide insights into (i) genome reduction in the Picochlorum genus with respect to other trebouxiophycean genera and (ii) the metabolic specificities of P. tauri with respect to other eukaryotic picophytoplankton. Genome mining unveiled in P. tauri an extended gene repertoire for carbon concentrating mechanisms, a reduced number of routes for acetyl-CoA synthesis from pyruvate and citrate, and a vitamin B12-dependent carboxylation pathway for propionyl-CoA breakdown. By contrast to the surveyed photosynthetic picoeukaryotes, P. tauri has specific functional traits linked to carbon metabolism, vitamin and chlorophyll synthesis, which are expected to boost physiology. These traits might have contributed to the fast development and maintenance of P. tauri in cool waters under low solar radiance.