Comparative Genomics of Chloropicon primus and Chloropicon roscoffensis Provide Insights into the Evolutionary Dynamics and Ecological Success of These Tiny Green Algae in Marine Environments

Abstract

The tiny green algae belonging to the class Chloropicophyceae play a key role in marine phytoplankton communities, especially in moderately oligotrophic water; yet, little is known about their biology, lifestyles, and what allows them to thrive in various oceanic environments. A single representative of this class (Chloropicon primus), comprising eight recognized species, has been previously subjected to genome analysis. To gain insight into the evolutionary changes that occurred during speciation in the Chloropicon genus and better understand the genes that distinguish Chloropicon species from other green algae traditionally designated as prasinophytes, we sequenced the genome of a second strain of C. primus and those of three strains of the closely related Chloropicon roscoffensis, the latter species representing the most dominant Chloropicon lineage in oceans. Our analyses highlighted substantial interspecific variations, including differences in chromosome number, gene content, gene arrangement, and ploidy state. Both C. primus genomes were predominantly diploid, while the C. roscoffensis genomes were either haploid or diploid. Specific proteins were identified for each species. Chloropicon roscoffensis possesses a biochemical C4-like inorganic carbon concentrating mechanism that potentially enables recycling of mitochondrial CO2 derived from photorespiration and respiration for carbon fixation in the chloroplast. In addition, it features specific proteins linked to the central carbon metabolism that suggest better coping mechanisms for abiotic stresses compared to C. primus. We also uncovered a previously undescribed eukaryotic recycling pathway for the micronutrient queuosine, a hypermodified nucleoside that is essential for post-transcriptional modification of several tRNAs at their anticodon wobble position.