Filling the Gap, Evolutionarily Conserved Omp85 in Plastids of Chromalveolates

Abstract

Chromalveolates are a diverse group of protists that include many ecologically and medically relevant organisms such as diatoms and apicomplexan parasites. They possess plastids generally surrounded by four membranes, which evolved by engulfment of a red alga. Today, most plastid proteins must be imported, but many aspects of protein import into complex plastids are still cryptic. In particular, how proteins cross the third outermost membrane has remained unexplained. We identified a protein in the third outermost membrane of the diatom Phaeodactylum tricornutum with properties comparable to those of the Omp85 family. We demonstrate that the targeting route of P. tricornutum Omp85 parallels that of the translocation channel of the outer envelope membrane of chloroplasts, Toc75. In addition, the electrophysiological properties are similar to those of the Omp85 proteins involved in protein translocation. This supports the hypothesis that P. tricornutum Omp85 is involved in precursor protein translocation, which would close a gap in the fundamental understanding of the evolutionary origin and function of protein import in secondary plastids.

Chloroplast Omp85 proteins change orientation during evolution

“…This could indicate either a Toc33-dependent import pathway of Toc75-III or an interaction within the TOC complex, which would then require a reversed topology, contrary to what would be predicted. More recently, data on an Omp85-like protein in the diatom Phaeodactylum tricornutum suggested that at least in complex plastids, both termini might face the outside of the plastid envelope (31,32). Thus, the available data are contradictory concerning the topology of the chloroplast Omp85 proteins.…”

Evidence for glycoprotein transport into complex plastids

“…In P. tricornutum preprotein transport across these membranes is presumably mediated by a Toc/Tic-like machinery similar to primary plastids. A Toc75 homolog, the protein ptOmp85 (P. tricornutum outer membrane protein 85), was recently identified and characterized by Bullmann and colleagues (17,37). However, Toc75 as well as the Tic complex within the inner plastid membrane are generally not believed to be able to transport bulky proteins (26) and it has been shown that plastid preproteins necessarily have to be transported in an unfolded conformation (32).…”

“…Stromal proteins are transported across membranes three and four, presumably mediated by a Toc/Tic (translocon of the outer/inner chloroplast membrane)-like system as it is known from primary plastids. Core components like a Toc75 homolog and several Tic factors were identified by in silico analyses and partially characterized in diatoms and related organisms (17)(18)(19).…”

Tic22 Is an Essential Chaperone Required for Protein Import into the Apicoplast

“…The apicomplexan homologue of Tic20 localizes to the inner apicoplast membrane and is essential for parasite survival and for protein import (18). Apicomplexan genomes also harbor a plastid-targeted Tic22 homologue and an, as yet, uncharacterized homologue of Toc75 (16,17). The presence of these homologues suggest that protein translocation across the inner two membranes of apicoplasts is similar to that in plants.…”