New deep-branching environmental plastid genomes on the algal tree of life

Marine algae support the entire ocean ecosystem and greatly impact planetary biology. The availability of algae in culture poorly represents their large environmental diversity, and we still have a limited understanding of their convoluted evolution by endosymbiosis. Here, we performed a phylogeny-guided plastid genome-resolved metagenomic survey of Tara Oceans expeditions. We present a manually curated resource of nearly 700 new non-redundant plastid genomes of environmental pelagic algae. This catalogue vastly expands the plastid genome diversity within major algal groups, often corresponding to algae without closely related reference genomes. We also recovered four genomes, including one near complete, forming a deep-branching plastid lineage of nano-size algae (<5 μm) that we informally named leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance notably in the Arctic. Leptophytes encompass the enigmatic marine plastid group DPL2, one of the very few known plastid groups not clearly belonging to any major algal groups and for which only 16S amplicon data is available. Extensive phylogenetic analyses based on 93 plastid genes and gene content comparison firmly place leptophytes together with haptophytes and cryptophytes, although the exact relationships remain ambiguous. Collectively, our study demonstrates that metagenomics can reveal currently hidden diversity of organellar genomes, and shows the importance of including this diversity to improve models for plastid evolution.