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

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 chlamydiacontrolled assimilation pathway.

The Glaucophyta: the blue-green plants in a nutshell

“…A controversial bacterial signature identified in Archaeplastida genomes, recently corroborated by the inclusion of the Cyanophora genome data, is the dozens (between 50 and 70) of genes putatively acquired from Chlamydiaelike bacteria via gene transfer early in the evolution of this eukaryote supergroup [8,22,[93][94][95]. Interestingly, some of these Chlamydiae-derived proteins are plastid-localized, or contain predicted plastid-targeting signals [93,94].…”

“…Some authors have proposed that the latter two enzymes, now essential components of the Archaeplastida starch biosynthesis pathway, played key roles in the successful establishment of the eukaryote-cyanobacterium endosymbiosis that led to the origin of the Archaeplastida ancestor. Briefly, this hypothesis postulates that the metabolic interaction of three symbiotic partners (i.e., eukaryote, Chlamydiae-like, and cyanobacterium) established a steady flux of carbon compounds, which resulted in a key event to consolidate a stable eukaryote-cyanobacterium endosymbiosis [22,96]. A recent review published in Acta Societatis Botanicorum Poloniae thoroughly discusses diverse aspects of this tripartite hypothesis [95].…”

“…They include the ATP/ADP translocator (NTT), which regulates the critical exchange of organellar ADP for ATP from cytoplasmic pools, and UhpC-type hexose-phosphate transporters [8,34]. Other prominent cases of proteins of Chlamydiae origin encoded in the Archaeplastida genomes are the cytosolic glycogen debranching enzyme (isoamylase; GlgX) and the ADP-glucose dependent starch synthase (GlgA) [8,22]. Some authors have proposed that the latter two enzymes, now essential components of the Archaeplastida starch biosynthesis pathway, played key roles in the successful establishment of the eukaryote-cyanobacterium endosymbiosis that led to the origin of the Archaeplastida ancestor.…”

“…involved in starch biosynthesis [22] and the presence of PRONE (plant-specific Rop nucleotide exchanger) guanine nucleotide exchange factors (proteins that activate GTPases) only in archaeplastidians [23].…”

A contemplation on the secondary origin of green algal and plant plastids

“…In other words, if the plastids and their associated traits are stripped from the cells, we are left with few to no clues as to the affinity of the three archaeplastidan groups in comparison to other eukaryotic groups. This does not exclude those shared traits that originated via lateral gene transfer from non-cyanobactierial sources, such as the presumed chlamydial symbiont ( [17,46], but see discussion in [47]). Most of such shared traits (or genes) are nevertheless related to plastid function, such as starch synthesis, and have been shown to be capable of being serially transferred via secondary/tertiary plastid-generating endosymbiosis [48].…”