Rapidly accumulating genetic data from environmental sequencing approaches have revealed an extraordinary level of unsuspected diversity within marine phytoplankton, which is responsible for around 50% of global net primary production. However, the phenotypic identity of many of the organisms distinguished by environmental DNA sequences remains unclear. The rappemonads are a plastid-bearing protistan lineage that to date has only been identified by environmental plastid 16S rRNA sequences. The phenotypic identity of this group, which does not confidently cluster in any known algal clades in 16S rRNA phylogenetic reconstructions, has remained unknown since the first report of environmental sequences over two decades ago. We show that rappemonads are closely related to a haptophyte microalga, Pavlomulina ranunculiformis gen. nov. sp. nov., and belong to a new haptophyte class, the Rappephyceae. Organellar phylogenomic analyses provide strong evidence for the inclusion of this lineage within the Haptophyta as a sister group to the Prymnesiophyceae. Members of this new class have a cosmopolitan distribution in coastal and oceanic regions. The relative read abundance of Rappephyceae in a large environmental barcoding dataset was comparable to, or greater than, that of major haptophyte species, such as the bloom-forming Gephyrocapsa huxleyi and Prymnesium parvum, indicating that they likely have a significant impact as primary producers. Detailed characterization of Pavlomulina allowed for reconstruction of the ancient evolutionary history of the Haptophyta, a group that is one of most important components of extant marine phytoplankton communities.

The original alignment data for organellar phylogenomics are kindly provided from Dr. Sergio A. Munoz-Gomez and Dr. Christopher J. Jackson, published in https://doi.org/10.1016/j.cub.2017.04.054 and https://doi.org/10.1093/gbe/evu218, respectively. Plastid 16S and nuclear 18S rRNA genes were retrieved as described in https://doi.org/10.1016/j.cub.2021.03.012. The original dataset of plastid Rpl36 was obtained from https://doi.org/10.1186/1471-2164-15-604. The corresponding gene/protein sequences of Pavlomulina ranunculiformis were added to the datasets.

Alignment was performed by MAFFT L-INS-i.
Ambiguously aligned sites were selected and trimmed by Gblocks (-t=d and -b5=h for nucleotides and -t=p and -b5=h for amino acids).
Single protein datasets were then concatenated for phylogenomics.