Was the Chlamydial Adaptative Strategy to Tryptophan Starvation an Early Determinant of Plastid Endosymbiosis?

Abstract

Chlamydiales were recently proposed to have sheltered the future cyanobacterial ancestor of plastids in a common inclusion. The intracellular pathogens are thought to have donated those critical transporters that triggered the efflux of photosynthetic carbon and the consequent onset of symbiosis. Chlamydiales are also suspected to have encoded glycogen metabolism TTS (Type Three Secretion) effectors responsible for photosynthetic carbon assimilation in the eukaryotic cytosol. We now review the reasons underlying other chlamydial lateral gene transfers evidenced in the descendants of plastid endosymbiosis. In particular we show that half of the genes encoding enzymes of tryptophan synthesis in Archaeplastida are of chlamydial origin. Tryptophan concentration is an essential cue triggering two alternative modes of replication in Chlamydiales. In addition, sophisticated tryptophan starvation mechanisms are known to act as antibacterial defenses in animal hosts. We propose that Chlamydiales have donated their tryptophan operon to the emerging plastid to ensure increased synthesis of tryptophan by the plastid ancestor. This would have allowed massive expression of the tryptophan rich chlamydial transporters responsible for symbiosis. It would also have allowed possible export of this valuable amino-acid in the inclusion of the tryptophan hungry pathogens. Free-living single cell cyanobacteria are devoid of proteins able to transport this amino-acid. We therefore investigated the phylogeny of the Tyr/Trp transporters homologous to E. coli TyrP/Mre and found yet another LGT from Chlamydiales to Archaeplastida thereby considerably strengthening our proposal.

Analysis of an improved Cyanophora paradoxa genome assembly

“…Some of us previously proposed the ‘ménage à trois’ hypothesis (MATH) to explain the presence of the chlamydial HGT signal in Archaeplastida genomes by positing a direct role of Chlamydiales in the metabolic integration of the ancestral plastid 88 , 89 . Under the MATH, Chlamydiales housed the cyanobiont inside the parasitic inclusion, thereby protecting it from host antibacterial defences.…”

Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid

“…A surprisingly high number of chlamydial-like proteins are present in primary plastids of plants and algae (Moustafa et al, 2008;Becker et al, 2008), which led to the 'm enage a trois' hypothesis proposing that a chlamydial endosymbiont was directly implicated in integration of a nascent plastid, and in some manner may have even been essential to the process (Facchinelli et al, 2013;Cenci et al, 2016). Many point at the Chlamydiae as the donor group, the most notable example being a complete second SUF pathway of FeS cluster assembly and hence potentially the result of a single transfer event.…”

“…Many point at the Chlamydiae as the donor group, the most notable example being a complete second SUF pathway of FeS cluster assembly and hence potentially the result of a single transfer event. A surprisingly high number of chlamydial-like proteins are present in primary plastids of plants and algae (Moustafa et al, 2008;Becker et al, 2008), which led to the 'm enage a trois' hypothesis proposing that a chlamydial endosymbiont was directly implicated in integration of a nascent plastid, and in some manner may have even been essential to the process (Facchinelli et al, 2013;Cenci et al, 2016). Whether this could also be the case for secondary plastid establishment remains an intriguing possibility.…”

Biotic interactions as drivers of algal origin and evolution

“…Both glaucophytes and red algae store carbohydrates in their cytosol, suggesting that the glycogen/starch pool may have provided an opportunity to buffer the unsynchronized demand and supply of carbon of the cyanobiont and its host. Several observations support this idea: (1) enzymes involved in the manipulation of host carbohydrate metabolism are pathogen effectors secreted by the type‐III secretion system (Gehre et al ., ); (2) pathogenic Chlamydiae synthesize extracellular storage carbohydrates within parasitophorous vacuoles using analogous nucleotide‐sugars and nucleotide‐sugar transporters (Gehre et al ., ); (3) nucleotide‐sugar transporters of host origin are evolutionary ancestors of plastid carbon exporters in red and green algae, as well as in plastids of secondary or tertiary endosymbiotic origin (Moog et al ., ); and (4) analysis of the tryptophan biosynthesis pathway in Archaeplastida shows that one‐half (4/8) of the genes encoding proteins in this pathway are putatively of chlamydial origin, as are the Escherichia coli tyr/mtr (tyrosine/tryptophan) transporter genes (Cenci et al ., , ).…”

“…Cenci et al . () posit that the chlamydial trp operon transfer occurred via conjugation during the co‐localization of chlamydial and cyanobacterial cells in inclusion vesicles. At a later time, some trp genes were moved to the Archaeplastida nuclear genome by endosymbiotic gene transfer (EGT) (Martin & Herrmann, ) from the cyanobacterial plastid forerunner.…”