Phylogenomic insights into the first multicellular streptophyte

Abstract

SUMMARYStreptophytes are best known as the clade containing the teeming diversity of embryophytes (land plants)1–4. Next to embryophytes are however a range of freshwater and terrestrial algae that bear important information on the emergence of key traits of land plants. Among these, the Klebsormidiophyceae stand out. Thriving in diverse environments—from mundane (ubiquitous occurrence on tree barks and rocks) to extreme (from the Atacama Desert to the Antarctic); Klebsormidiophyceae can exhibit filamentous body plans and display remarkable resilience as colonizers of terrestrial habitats5,6. Currently, the lack of a robust phylogenetic framework for the Klebsormidiophyceae hampers our understanding of the evolutionary history of these key traits. Here, we conducted a phylogenomic analysis utilizing advanced models that can counteract systematic biases. We sequenced 24 new transcriptomes of Klebsormidiophyceae and combined them with 14 previously published genomic and transcriptomic datasets. Using phylogenomic analysis built on 420 loci and sophisticated models, we establish a novel phylogenetic structure, dividing the six distinct genera of Klebsormidiophyceae in a novel four-order-system, with deep divergences more than 898, 765, and 734 million years ago. The reconstruction of ancestral states for habitat suggests an evolutionary history of multiple transitions between terrestrial-aquatic habitats, with Klebsormidiales having conquered land earlier than embryophytes. Focusing on the body plan of the last common ancestor of Klebsormidiophyceae, we postulate it was likely filamentous whereas the sarcinoids and unicells in Klebsormidiophyceae are likely derived states. Our data reveal that the first multicellular streptophytes likely lived more than 900 million years ago.