Plastid phylogenomics with broad taxon sampling further elucidates the distinct evolutionary origins and timing of secondary green plastids

Christopher Jackson,Andrew H Knoll,Heroen Verbruggen,Cheong Xin Chan

doi:10.1038/s41598-017-18805-w

Christopher Jackson, Andrew H Knoll + Show 2 more

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https://doi.org/10.1038/s41598-017-18805-w

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Abstract

Secondary plastids derived from green algae occur in chlorarachniophytes, photosynthetic euglenophytes, and the dinoflagellate genus Lepidodinium. Recent advances in understanding the origin of these plastids have been made, but analyses suffer from relatively sparse taxon sampling within the green algal groups to which they are related. In this study we aim to derive new insights into the identity of the plastid donors, and when in geological time the independent endosymbiosis events occurred. We use newly sequenced green algal chloroplast genomes from carefully chosen lineages potentially related to chlorarachniophyte and Lepidodinium plastids, combined with recently published chloroplast genomes, to present taxon-rich phylogenetic analyses to further pinpoint plastid origins. We integrate phylogenies with fossil information and relaxed molecular clock analyses. Our results indicate that the chlorarachniophyte plastid may originate from a precusor of siphonous green algae or a closely related lineage, whereas the Lepidodinium plastid originated from a pedinophyte. The euglenophyte plastid putatively originated from a lineage of prasinophytes within the order Pyramimonadales. Our molecular clock analyses narrow in on the likely timing of the secondary endosymbiosis events, suggesting that the event leading to Lepidodinium likely occurred more recently than those leading to the chlorarachniophyte and photosynthetic euglenophyte lineages.

Highlights

The spread of plastids by secondary endosymbiosis – the uptake of an alga containing a primary plastid by a heterotrophic eukaryotic host – has driven the evolution of many photosynthetic lineages of global ecological and economic importance
While there is ongoing controversy about exactly how many secondary endosymbiosis events have led to the numerous lineages containing a secondary red plastid[21], the situation for secondary green plastids is more clear-cut, and it is apparent that euglenophytes, chlorarachniophytes and Lepidodinium acquired their plastids in three independent evolutionary events
Using our dataset of 151 taxa and 64 genes (Dataset A; see methods), we carried out Maximum likelihood (ML) and Bayesian analyses using both nucleotide and amino-acid alignments

Summary

Introduction

The spread of plastids by secondary endosymbiosis – the uptake of an alga containing a primary plastid by a heterotrophic eukaryotic host – has driven the evolution of many photosynthetic lineages of global ecological and economic importance. Haptophytes, diatoms and most photosynthetic dinoflagellates, for example, contain red-algal derived plastids originating from secondary (or subsequent higher) endosymbiotic events[1,2,3], and together these organisms constitute major primary producers in marine environments. Other lineages contain a secondary plastid originating from a green algal ancestor[4,5,6,7]. Three lineages are known to contain secondary plastids derived from green algae: euglenophytes, chlorarachniophytes and the dinoflagellate genus Lepidodinium[10]. Chlorarachniophytes, a small group of exclusively marine unicellular algae, are often amoeboid in form and belong to the supergroup Rhizaria Together with cryptophytes they are unique among lineages with secondary plastids in that they retain a vestigial nucleus from the algal endosymbiont, termed a nucleomorph[13,14]. We aim to pinpoint the closest extant relatives of the ancestral green algae that were involved in the three distinct endosymbiosis events, and to infer the timing of these events using relaxed molecular clock methods

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