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.
Highlights
In particular we show that half of the genes encoding enzymes of tryptophan synthesis in Archaeplastida are of chlamydial origin
Plastid endosymbiosis consists of a process by which a eukaryote phagotroph internalized a cyanobacterial ancestor and established a symbiotic link consisting of photosynthetic carbon export from the cyanobiont to the host cytosol (McFadden, 2014)
We propose that a Trp operon from a Chlamydiales was donated to the cyanobacterial ancestor of plastids through conjugation within a common chlamydial inclusion
Summary
Archaeplastida in LGTs from Chlamydiales (Brinkman et al, 2002; Huang and Gogarten, 2007; Becker et al, 2008; Moustafa et al, 2008; Collingro et al, 2011; Ball et al, 2013). Both of these are here confirmed as chlamydial LGTs. We have reproduced the phylogenies of TrpA, TrpB, and TrpG coding, respectively, the two tryptophan synthase α and β subunits and the anthranilate synthase β subunit and conclude that they all display very clear-cut cyanobacterial ancestry, as previously demonstrated (Reyes-Prieto and Moustafa, 2012). This LGT possibly escaped previous detection because of the proximity of a subset of candidate donor cyanobacterial sequences (Figure 2B). We favor a non-cyanobacterial origin for TyrP among the deeply rooted γ-proteobacteria as the latter predate by far Nostocales diversification (Battistuzzi et al, 2004)
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