Molecular Phylogeny of the SELMA Translocation Machinery Recounts the Evolution of Complex Photosynthetic Eukaryotes

Abstract

Photosynthetic eukaryotes and their relatives are the result of an intricate evolutionary history involving a series of plastid acquisitions through endosymbiosis, multiple reversions to heterotrophy, and sometimes total plastid losses. Among these events, one of the most debated is the emergence and diversification of the CASH lineages (Cryptophyta, Alveolata, Stramenopiles, and Haptophyta). Although they all include species bearing a complex plastid that derived from the endosymbiosis of a red alga, their phylogenetic relationships remain controversial, and the timing and number of plastid acquisitions are still undetermined. The inner metabolism of all plastids is mostly supported by nuclear-encoded proteins, and consequently, mechanisms allowing the relocation of those proteins have evolved or were recycled at each endosymbiotic event. Thus, the study of the composition and origins of those translocation machineries provides important clues for understanding how photosynthetic lineages have emerged and might be related. In CASH species, the SELMA complex, composed of about 20 proteins, is dedicated to the transport of preproteins across the periplastidial membrane, the second outermost membrane of complex red plastids. In this work, we present a comprehensive genomic survey and phylogenetic analysis of the proteins composing the SELMA complex. We confirm the presence, homology, and monophyletic origin of SELMA in the four CASH lineages and use these observations to infer a scenario for the serial transmission of secondary red plastids that differs from previous hypotheses and sheds new light on the evolution of photosynthetic eukaryotes.