Abstract

The common ancestor of red algae (Rhodophyta) has undergone massive genome reduction, whereby 25% of the gene inventory has been lost, followed by its split into the species-poor extremophilic Cyanidiophytina and the broadly distributed mesophilic red algae. Success of the mesophile radiation is surprising given their highly reduced gene inventory. To address this latter issue, we combine an improved genome assembly from the unicellular red alga Porphyridium purpureum with a diverse collection of other algal genomes to reconstruct ancient endosymbiotic gene transfers (EGTs) and gene duplications. We find EGTs associated with the core photosynthetic machinery that may have played important roles in plastid establishment. More significant are the extensive duplications and diversification of nuclear gene families encoding phycobilisome linker proteins that stabilize light-harvesting functions. We speculate that the origin of these complex families in mesophilic red algae may have contributed to their adaptation to a diversity of light environments.

Highlights

  • The common ancestor of red algae (Rhodophyta) has undergone massive genome reduction, whereby 25% of the gene inventory has been lost, followed by its split into the species-poor extremophilic Cyanidiophytina and the broadly distributed mesophilic red algae

  • Benchmarking Universal Single-Copy Orthologs (BUSCO) analysis[36] showed that the gene models encompass 90.4% of the 429 conserved eukaryotic BUSCO gene set, which is the highest value among currently available red algal genomes (Supplementary Table 3)

  • These proteins contributed to the establishment of photosynthetic components during the early phases of primary endosymbiosis and to the stability of PBS structures

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Summary

Introduction

The common ancestor of red algae (Rhodophyta) has undergone massive genome reduction, whereby 25% of the gene inventory has been lost, followed by its split into the species-poor extremophilic Cyanidiophytina and the broadly distributed mesophilic red algae. Success of the mesophile radiation is surprising given their highly reduced gene inventory To address this latter issue, we combine an improved genome assembly from the unicellular red alga Porphyridium purpureum with a diverse collection of other algal genomes to reconstruct ancient endosymbiotic gene transfers (EGTs) and gene duplications. The three Archaeplastida taxa share a plastid protein import system whereby nuclear-encoded, plastid-destined proteins contain a presequence that targets them to the organelle via translocons at the inner/outer chloroplast (plastid) membranes (TIC/TOC). This conserved nanomachine was established during the early stages of endosymbiosis (i.e., before diversification into the three algal lineages) by the ancient EGT events[3,4,5]. This protein complex is composed of PE, PC, and allophycocyanin (APC)

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