Proposal of a new thraustochytrid genus Hondaea gen. nov. and comparison of its lipid dynamics with the closely related pseudo-cryptic genus Aurantiochytrium

Thraustochytrids are marine protists highly ecologically relevant in mangrove environments. The family Thraustochytriaceae underwent profound taxonomical rearrangements in the last decade, with the description and emendation of several genera. Here, we identified two new thraustochytrid strains (CCAP 4062/1 and CCAP 4062/3) collected from the same mangrove environment in Mayotte Island (Indian Ocean) and representative of two sister clades in the phylogenetic Aurantiochytrium super clade. Phylogenomic (on 2389 genes) and phylogenetic analyses on 18S rDNA sequences led us to propose the description of a new genus, Hondaea gen. nov. (CCAP 4062/3), closely related and pseudo-cryptic to Aurantiochytrium (CCAP 4062/1). Compared to Aurantiochytrium, Hondaea did not produce amoeboid cells and its zoospores were smaller. Chemotaxonomical traits, such as fatty acid, sterol, and carotenoid profiles measured along the growth curves, validated the new genus description. Genome sequencing and manual annotation of lipid metabolism genes revealed similar pathways in both strains. However, such pathways showed different dynamics during the growth phases. Aurantiochytrium accumulated carotenoids (canthaxanthin) and large amounts of triacylglycerols enriched in ω3-docosahexaenoic acid in the stationary phase, while squalene and free cholesterol increased during the early exponential phase. In contrast, Hondaea accumulated low amounts of triacylglycerols enriched in odd and saturated fatty acids during the early exponential phase, whereas free-sterol and carotenoid contents were little affected. These results suggest that these genera evolved independently, although phylogenetically and ecologically closely related. This comparative study also showed that the biotechnological potential of thraustochytrids cannot be deduced solely from phylogenetic and genomic analyses.