Genômica comparativa revela diversificação acelerada do plastoma de Ochrophyta a partir da endossimbiose secundária com um grupo basal de algas vermelhas

Abstract

Photosynthesizing eukaryotes arose from the primary endosymbiosis of a single-celled heterotrophic eukaryote with an ancestral cyanobacteria, giving rise to the plastids present in Archaeplastida, the supergroup of eukaryotes that includes Viridiplantae (green algae and land plants), Rhodophyta (red algae) and Glaucophytes (freshwater algae). Several eukaryotic organisms have acquired plastids through green or red algae in a process known as secondary endosymbiosis. Among them are the diverse phylum of Ochrophyta (brown algae), which have plastids of red origin, and contains the clade of diatoms, which are the main primary source of atmospheric oxygen today. All plastids have their own genome, denominated as plastome, containing several genes ranging from basal gene expression to the formation of photosystem I and II protein complexes, which are responsible for the light stage of photosynthesis. During the process of adaptation of the plastid, several of these genes were transferred to the nuclear genome of these organisms in a process denominated as Endosymbiotic Gene Transfer (EGT). Considering the evolutionary history of plastids and their ecological importance, the aim of our study is to identify the evolutionary patterns within the plastomes of plastids of red lineages, performing a general comparison between Viridiplantae, Rhodophyta and Ochrophyta. We obtained the public data of all plastomes and performed an in silico approach of comparative genomics. From our analyses, we identified that the organism that originated the ancestral secondary plastid of Ochrophyta was an ancestor of a basal lineage of Rhodophyta (Cyanidiophyceae). We identified a higher rate of dN/dS in genes of Ochrophyta photosystems compared to Rhodophyta genes, and divergences in the tertiary structure of photosystem II proteins; these genes lost in the plastome were partly transferred by EGT to the nuclear genome or were lost entirely depending on their function. We identified that the genomic structure of the plastome of Ochrophyta is divergent from what is typically found in Rhodophyta, more closely resembling what is found in the plastome of the green lineage; within this structure, there is the maintenance of Inverted Repeats regions where typically unduplicated genes (such as that of the photosystem) are inside and are duplicated. From these results, we hypothesized that there is an evolutionary approximation between Viridiplantae and Ochrophyta, and the Rhodophyta plastid is an outlier within the evolutionary history of plastids.