A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids

Jürgen F H Strassert,Iker Irisarri,Fabien Burki,Tom A Williams

doi:10.1038/s41467-021-22044-z

Abstract

In modern oceans, eukaryotic phytoplankton is dominated by lineages with red algal-derived plastids such as diatoms, dinoflagellates, and coccolithophores. Despite the ecological importance of these groups and many others representing a huge diversity of forms and lifestyles, we still lack a comprehensive understanding of their evolution and how they obtained their plastids. New hypotheses have emerged to explain the acquisition of red algal-derived plastids by serial endosymbiosis, but the chronology of these putative independent plastid acquisitions remains untested. Here, we establish a timeframe for the origin of red algal-derived plastids under scenarios of serial endosymbiosis, using Bayesian molecular clock analyses applied on a phylogenomic dataset with broad sampling of eukaryote diversity. We find that the hypotheses of serial endosymbiosis are chronologically possible, as the stem lineages of all red plastid-containing groups overlap in time. This period in the Meso- and Neoproterozoic Eras set the stage for the later expansion to dominance of red algal-derived primary production in the contemporary oceans, which profoundly altered the global geochemical and ecological conditions of the Earth.

Highlights

In modern oceans, eukaryotic phytoplankton is dominated by lineages with red algal-derived plastids such as diatoms, dinoflagellates, and coccolithophores
Several models compatible with the rhodoplex hypothesis have been proposed, differing in the specifics of the plastid donor and recipient lineages[16,17,18,19] (Fig. 1). These models of serial endosymbiosis remain highly speculative, in particular, because we do not know if they are chronologically possible—did the plastid donor and recipient lineages co-exist? Addressing this important issue requires a reliable timeframe for eukaryote evolution, which has been challenging to obtain owing to a combination of complicating factors, notably: (1) uncertain phylogenetic relationships among the major eukaryote lineages, (2) the lack of genome-scale data for the few microbial groups with a robust fossil record, and (3) a generally poor understanding of methodological choices on the dates estimated for early eukaryote evolution
Our analyses show that the hypotheses of serial endosymbiosis are chronologically possible, as most red algal plastid acquisitions likely occurred in an overlapping timeframe during the Mesoproterozoic and Neoproterozoic Eras, setting the stage for the subsequent evolution of the most successful algae on Earth

Summary

Introduction

Eukaryotic phytoplankton is dominated by lineages with red algal-derived plastids such as diatoms, dinoflagellates, and coccolithophores. To the primary endosymbiosis, plastids spread to other eukaryote groups from green and red algae by eukaryote-to-eukaryote endosymbioses, i.e. the uptake of primary plastid-containing algae by eukaryotic hosts These higher-order endosymbioses resulted in complex plastids surrounded by additional membranes, some even retaining the endosymbiont nucleus (the nucleomorph) and led to the diversification of many photosynthetic lineages of global ecological importance, especially those with red algal-derived plastids (e.g. diatoms, dinoflagellates and apicomplexan parasites)[5]. The current phylogeny of eukaryotes has given rise to a new framework for explaining the distribution of complex red plastids This framework, unified under the rhodoplex hypothesis, invokes the process of serial endosymbiosis, a single secondary endosymbiosis between a red alga and a eukaryotic host, followed by successive higher-order—tertiary, quaternary—endosymbioses spreading plastids to unrelated groups[15]. These models of serial endosymbiosis remain highly speculative, in particular, because we do not know if they are chronologically possible—did the plastid donor and recipient lineages co-exist? Addressing this important issue requires a reliable timeframe for eukaryote evolution, which has been challenging to obtain owing to a combination of complicating factors, notably: (1) uncertain phylogenetic relationships among the major eukaryote lineages, (2) the lack of genome-scale data for the few microbial groups with a robust fossil record, and (3) a generally poor understanding of methodological choices on the dates estimated for early eukaryote evolution

Methods

Results

Conclusion