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

Cell Reports (Feb 2024)

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

Journal volume & issue: Vol. 43, no. 2
p. 113740

Abstract

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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.

CP: Cell biology

Published in Cell Reports

ISSN: 2211-1247 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Science: Biology (General)
Website: http://www.cell.com/cell-reports/home

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