Photosynthetic Paulinella: Recapitulation of Primary Plastid Establishment

Abstract

The origin of photosynthesis in eukaryotes stems from a single primary endosymbiosis between a heterotrophic protist cell and a cyanobacterium that occurred more than 1.5 billion years ago. This proto-algal population gave rise to three lineages of the Plantae (Rhodophyta, Viridiplantae, and Glaucophyta). Rhodoplasts and chloroplasts were later spread horizontally into other eukaryotic lineages through secondary endosymbiosis. Primary endosymbiosis is therefore a critical feature of eukaryotic evolution; however, it is difficult to study because of the long evolutionary time span that has passed since primary plastid origin. The filose amoeba Paulinella chromatophora is an exceptional species that contains two plastids, referred to as “chromatophores,” that originated from a Synechococcus-like cyanobacterium. Photosynthetic Paulinella provides an ideal model to gain insights into the origin of photoautotrophy because its sister species are all heterotrophs that prey on cyanobacteria. Here, we review the evolutionary process that led to this second instance of primary endosymbiosis based on recent studies that include biodiversity surveys and plastid and nuclear genome data. Draft genome data from heterotrophic Paulinella using the single-cell genomics approach demonstrate two cases of horizontal gene transfer (HGT) from cyanobacteria, demonstrating that prey items are potential sources of foreign DNA in these taxa. Genome data from photosynthetic Paulinella provide evidence of massive gene loss from the chromatophore genome, endosymbiotic gene transfer (EGT) to the host nucleus, and the potential establishment of a plastid protein import system that relies on the secretory pathway in the amoeba. We also present recent data regarding postendosymbiotic speciation in photosynthetic Paulinella and lineage specific differential gene loss and EGT.