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

Abstract : Chlamydiales were recently proposed to have sheltered the future cyanobacterialancestor of plastids in a common inclusion. The intracellular pathogens are thoughtto have donated those critical transporters that triggered the efflux of photosyntheticcarbon and the consequent onset of symbiosis. Chlamydiales are also suspected tohave encoded glycogen metabolism TTS (Type Three Secretion) effectors responsible forphotosynthetic carbon assimilation in the eukaryotic cytosol. We now review the reasonsunderlying other chlamydial lateral gene transfers evidenced in the descendants of plastidendosymbiosis. In particular we show that half of the genes encoding enzymes oftryptophan synthesis in Archaeplastida are of chlamydial origin. Tryptophan concentrationis an essential cue triggering two alternative modes of replication in Chlamydiales.In addition, sophisticated tryptophan starvation mechanisms are known to act asantibacterial defenses in animal hosts. We propose that Chlamydiales have donated theirtryptophan operon to the emerging plastid to ensure increased synthesis of tryptophanby the plastid ancestor. This would have allowed massive expression of the tryptophanrich chlamydial transporters responsible for symbiosis. It would also have allowedpossible export of this valuable amino-acid in the inclusion of the tryptophan hungrypathogens. Free-living single cell cyanobacteria are devoid of proteins able to transportthis amino-acid. We therefore investigated the phylogeny of the Tyr/Trp transportershomologous toE. coliTyrP/Mre and found yet another LGT from Chlamydiales toArchaeplastida thereby considerably strengthening our proposal.