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.

Cellular Analysis Facility College of Medical Veterinary and Life Sciences University of Glasgow Glasgow UK

Division of Infectious Diseases Department of Medicine and Department of Biological Sciences University of Alberta Edmonton AB Canada; Women and Children's Health Research Institute University of Alberta Edmonton AB Canada

Division of Infectious Diseases Department of Medicine and Department of Biological Sciences University of Alberta Edmonton AB Canada; Women and Children's Health Research Institute University of Alberta Edmonton AB Canada; Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic; Centre for Life's Origin and Evolution Department of Genetics Evolution and Environment University College London London UK

Experimental Parasitology Department of Veterinary Sciences Faculty of Veterinary Medicine Ludwig Maximilians Universität LMU Munich Germany

Pathogen Genomics Laboratory Bioscience Programme Biological and Environmental Sciences and Engineering Thuwal 23955 6900 Kingdom of Saudi Arabia

Pathogen Genomics Laboratory Bioscience Programme Biological and Environmental Sciences and Engineering Thuwal 23955 6900 Kingdom of Saudi Arabia; International Institute for Zoonosis Control GI CoRE Hokkaido University Sapporo Japan

Pflanzliche Entwicklungsbiologie Biozentrum der Ludwig Maximilians Universität Munich Germany

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