Metabolic Effectors Secreted by Bacterial Pathogens: Essential Facilitators of Plastid Endosymbiosis?

Steven G Ball,Maria-Cecilia Arias,Ugo Cenci,Agathe Subtil,Andreas P.M Weber,David Dauvillée,Lena Gehre,Christophe Colleoni,Debashish Bhattacharya,Ahmed Moustafa

doi:10.1105/tpc.112.101329

Abstract

Under the endosymbiont hypothesis, over a billion years ago a heterotrophic eukaryote entered into a symbiotic relationship with a cyanobacterium (the cyanobiont). This partnership culminated in the plastid that has spread to forms as diverse as plants and diatoms. However, why primary plastid acquisition has not been repeated multiple times remains unclear. Here, we report a possible answer to this question by showing that primary plastid endosymbiosis was likely to have been primed by the secretion in the host cytosol of effector proteins from intracellular Chlamydiales pathogens. We provide evidence suggesting that the cyanobiont might have rescued its afflicted host by feeding photosynthetic carbon into a chlamydia-controlled assimilation pathway.

Highlights

Members of the photoautotrophic lineage, the Archaeplastida consisting of the Chloroplastida, Rhodophyceae, and Glaucophyta are the founding lineage of photosynthetic eukaryotes (Rodríguez-Ezpeleta et al, 2005, Reyes-Prieto et al, 2007; Chan et al, 2011)
Despite the advantages offered by photosynthesis and the innumerable opportunities that presumably have existed for phagotrophic protists to recapitulate plastid acquisition, only one other case is known of primary plastid endosymbiosis, in the photosynthetic amoeba Paulinella (Nowack et al, 2008)
We reanalyzed the contribution of Chlamydiales to the genomes of Archaeplastida using the additional data (e.g., >60k proteins from the red algae Calliarthron tuberculosum and Porphyridium cruentum; Chan et al, 2011) that have become available since previous analyses (Huang and Gogarten, 2007; Becker et al, 2008; Moustafa et al, 2008)

Summary

Introduction

Members of the photoautotrophic lineage, the Archaeplastida ( called Kingdom Plantae) consisting of the Chloroplastida (green algae and plants), Rhodophyceae (red algae), and Glaucophyta (glaucophytes) are the founding lineage of photosynthetic eukaryotes (Rodríguez-Ezpeleta et al, 2005, Reyes-Prieto et al, 2007; Chan et al, 2011). We show that the sole extant enzyme that could have been devoted to the assimilation of photosynthate in the host cytosol is an enzyme of chlamydial origin Because such assimilation is necessary for the selection of plastid endosymbiosis, this enzyme had to be present at the onset of endosymbiosis in the host cytosol. This specific function defines a previously unsuspected class of effectors secreted by Chlamydiales bacteria. This finding suggests strongly that an intracellular bacterium ancestor to the extant order Chlamydiales, a cyanobacterium, and a eukaryotic host were linked together in a stable tripartite symbiotic relationship that led to the establishment of the plant lineages

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Conclusion