Evolutionary analysis identifies a Golgi pathway and correlates lineage-specific factors with endomembrane organelle emergence in apicomplexans
Christen M. Klinger,
Elena Jimenez-Ruiz,
Tobias Mourier,
Andreas Klingl,
Leandro Lemgruber,
Arnab Pain,
Joel B. Dacks,
Markus Meissner
Affiliations
Christen M. Klinger
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
Elena Jimenez-Ruiz
Experimental Parasitology, Department of Veterinary Sciences, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität, LMU, Munich, Germany
Tobias Mourier
Pathogen Genomics Laboratory, Bioscience Programme, Biological, and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Kingdom of Saudi Arabia
Andreas Klingl
Pflanzliche Entwicklungsbiologie, Biozentrum der Ludwig-Maximilians-Universität, Munich, Germany
Leandro Lemgruber
Cellular Analysis Facility, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK
Arnab Pain
Pathogen Genomics Laboratory, Bioscience Programme, Biological, and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Kingdom of Saudi Arabia; International Institute for Zoonosis Control, GI-CoRE, Hokkaido University, Sapporo, Japan
Joel B. Dacks
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 (Budweis), Czech Republic; Centre for Life’s Origin and Evolution, Department of Genetics, Evolution & Environment, University College London, London, UK; Corresponding author
Markus Meissner
Experimental Parasitology, Department of Veterinary Sciences, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität, LMU, Munich, Germany; Corresponding author
Summary: 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.
