Algal endosymbionts as vectors of horizontal gene transfer in photosynthetic eukaryotes

Debashish Bhattacharya,Huan Qiu,Hwan Su Yoon

doi:10.3389/fpls.2013.00366

Abstract

Photosynthesis in eukaryotes occurs in the plastid, an organelle that is derived from a single cyanobacterial primary endosymbiosis in the common ancestor of the supergroup Plantae (or Archaeplastida) that includes green, red, and glaucophyte algae and plants. However a variety of other phytoplankton such as the chlorophyll c-containing diatoms, dinoflagellates, and haptophytes contain a red alga-derived plastid that traces its origin to secondary or tertiary (eukaryote engulfs eukaryote) endosymbiosis. The hypothesis of Plantae monophyly has only recently been substantiated, however the extent and role of endosymbiotic and horizontal gene transfer (EGT and HGT) in algal genome evolution still remain to be fully understood. What is becoming clear from analysis of complete genome data is that algal gene complements can no longer be considered essentially eukaryotic in provenance; i.e., with the expected addition of several hundred cyanobacterial genes derived from EGT and a similar number derived from the mitochondrial ancestor. For example, we now know that foreign cells such as Chlamydiae and other prokaryotes have made significant contributions to plastid functions in Plantae. Perhaps more surprising is the recent finding of extensive bacterium-derived HGT in the nuclear genome of the unicellular red alga Porphyridium purpureum that does not relate to plastid functions. These non-endosymbiont gene transfers not only shaped the evolutionary history of Plantae but also were propagated via secondary endosymbiosis to a multitude of other phytoplankton. Here we discuss the idea that Plantae (in particular red algae) are one of the major players in eukaryote genome evolution by virtue of their ability to act as “sinks” and “sources” of foreign genes through HGT and endosymbiosis, respectively. This hypothesis recognizes the often under-appreciated Rhodophyta as major sources of genetic novelty among photosynthetic eukaryotes.

Highlights

Photosynthetic eukaryotes are a taxonomically diverse group with a wide variety of cell morphologies and lifestyles that are key primary producers (Field et al, 1998)
All eukaryotic photosynthesis relies on the intracellular organelle, the plastid that was derived over one billion years ago from a cyanobacterial primary endosymbiosis
Whereas eukaryotic photosynthesis commenced with primary endosymbiosis, its greatest impact was achieved through additional rounds of secondary and tertiary endosymbiosis, whereby the cyanobacterium-derived organelle was transferred to a myriad of other protist hosts

Summary

INTRODUCTION

Photosynthetic eukaryotes (i.e., algae and plants) are a taxonomically diverse group with a wide variety of cell morphologies (e.g., diatoms, dinoflagellates, coccolithophores) and lifestyles that are key primary producers (Field et al, 1998). All eukaryotic photosynthesis relies on the intracellular organelle, the plastid (chloroplast in plants and green algae) that was derived over one billion years ago from a cyanobacterial primary endosymbiosis. In this process, a once free-living cyanobacterium capable of oxygenic photosynthesis was engulfed and retained in a heterotrophic protist, and over time evolved into the intracellular organelle (Section I in Figure 1; Cavalier-Smith, 1999; Bhattacharya et al, 2004). Whereas eukaryotic photosynthesis commenced with primary endosymbiosis, its greatest impact was achieved through additional rounds of secondary and tertiary endosymbiosis, whereby the cyanobacterium-derived organelle was transferred to a myriad of other protist hosts (e.g., red algal endosymbiosis; Section III in Figure 1; Keeling, 2010; Dorrell and Smith, 2011).

Algal endosymbionts and HGT

Findings

CONCLUSION