Identification of a deep-branching lineage of algae using environmental plastid genomes

Marine algae underpin entire ocean ecosystems. Yet algae in culture poorly represent their large environmental diversity, and we have a limited understanding of their convoluted evolution by endosymbiosis. Here, we perform a phylogeny-guided plastid genome-resolved metagenomic survey of Tara Oceans expeditions. We present a curated resource of 660 new non-redundant plastid genomes of environmental marine algae, vastly expanding plastid genome diversity within major algal groups, including many without closely related reference genomes. Notably, we recover four plastid genomes, including one near-complete, forming a deep-branching plastid lineage of nano-size algae that we informally name leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance in the Arctic. A near-complete mitochondrial genome showing strong co-occurrence with leptophyte plastids is also recovered and assigned to this group. Leptophytes encompass the enigmatic plastid group DPL2, one of the very few known plastid groups not clearly belonging to major algal groups and previously known only from 16S rDNA sequences. Comparative organellar genomics and phylogenomics indicate that leptophytes are sister to haptophytes, and raise the intriguing possibility that cryptophytes acquired their plastids from haptophytes. Collectively, our study demonstrates that metagenomics can reveal hidden organellar diversity, and improve models of plastid evolution.