Evolutionary analysis identifies a Golg ipathway and correlates lineage-specific factors with endomembrane organelle emergence in apicomplexans

Authors:

Christen M. Klinger, Elena Jimenez-Ruiz, Tobias Mourier, Andreas Klingl, Leandro Lemgruber, Arnab Pain, Joel B. Dacks, Markus Meissner

Keywords:

evolutionary cell biology Golgi Arl Toxoplasma gondii molecular evolution Apicomplexa Toxoplasma evolution membrane trafficking phylogenetic screen

Abstract:

The organelle paralogy hypothesis (OPH) aims to explain the evolution of non-endosymbiotically derived organelles. It predicts that lineage-specific pathways or organelles should result when identity-encoding membrane-trafficking components duplicate and co-evolve. Here, we investigate the presence of such lineage-specific membrane-trafficking machinery paralogs in Apicomplexa, a globally important parasitic lineage. We are able to identify 18 paralogs of known membrane-trafficking machinery, in several cases co-incident with the presence of new endomembrane organelles in apicomplexans or their parent lineage, the Alveolata. Moreover, focused analysis of the apicomplexan Arf-like small GTPases (i.e., ArlX3) revealed a specific post-Golgi trafficking pathway. This pathway appears involved in delivery of proteins to micronemes and rhoptries, with knockdown demonstrating reduced invasion capacity. Overall, our data have identified an unforeseen post-Golgi trafficking pathway in apicomplexans and are consistent with the OPH mechanism acting to produce endomembrane pathways or organelles at various evolutionary stages across the alveolate lineage.

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