Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions

Abstract

The extent and role of horizontal gene transfer (HGT) in phytoplankton and, more broadly, eukaryotic evolution remain controversial topics. Recent studies substantiate the importance of HGT in modifying or expanding functions such as metal or reactive species detoxification and buttressing halotolerance. Yet, the potential of HGT to significantly alter the fate of species in a major eukaryotic assemblage remains to be established. We provide such an example for the ecologically important lineages encompassed by cryptophytes, rhizarians, alveolates, stramenopiles, and haptophytes (“CRASH” taxa). We describe robust evidence of prokaryotic HGTs in these taxa affecting functions such as polysaccharide biosynthesis. Numbers of HGTs range from 0.16 to 1.44% of CRASH species gene inventories, comparable to the ca. 1% prokaryote-derived HGTs found in the genomes of extremophilic red algae. Our results substantially expand the impact of HGT in eukaryotes and define a set of general principles for prokaryotic gene fixation in phytoplankton genomes.

The complete chloroplast genome of Saccharina latissima

“…The plastid monophyly of cryptophyta, haptophyta and rhodophyta was significantly clustered with a support value of 90, forming a red-algal clade. Stramenopiles clade and red-algal clade have a closer phylogenetic relationship than the viridiplantae clade, which was widely supported by the secondary endosymbiosis hypothesis (Fan et al 2020).…”

“…Stramenopiles clade and red-algal clade have a closer phylogenetic relationship than the viridiplantae clade, which was widely supported by the secondary endosymbiosis hypothesis (Fan et al. 2020 ).…”

PhycoCosm, a comparative algal genomics resource

“…These plastid genes in nuclear genomes are the result of horizontal gene transfer (HGT) after primary or secondary endosymbiosis ( 43 ). HGT may be even more wide-spread, beyond plastid genes, in Chlorarachniophyta ( 44 ), Cryptophyta, Rhizaria, Alveolata, Heterokonta and Haptophyta ( 45 ), and is to be distinguished from bacterial contamination. To identify genes that result from HGT, we developed a method based on incongruences between gene and species trees ( 46 ).…”

Lipid Droplets in Unicellular Photosynthetic Stramenopiles

“…and P. tricornutum both stem from two endosymbiosis events, where the last endosymbiosis involved the engulfment of a microalga from the red lineage. However, the second endosymbiosis may imply different red algae and/or different heterotrophic cells ( Keeling, 2013 ), as well as distinct patterns of horizontal gene transfers ( Fan et al, 2020 ; Vancaester et al, 2020 ). Thus, although phylogenetically close, their metabolisms might differ.…”