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

Klinger, C. M., Jimenez-Ruiz, E., Mourier, T., Klingl, A., Lemgruber, L. , Pain, A., Dacks, J. B. and Meissner, M. (2024) Evolutionary analysis identifies a Golgi pathway and correlates lineage-specific factors with endomembrane organelle emergence in apicomplexans. Cell Reports, 43(2), 113740. (doi: 10.1016/j.celrep.2024.113740) (PMID:38363682)

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.

• Item Type: Articles
• Additional Information: C.M.K. was funded by an Alberta Innovates Health Solutions Fulltime Studentship and a Canada Vanier Graduate Scholarship. His research has been funded in part by the generosity of the Stollery Children’s Hospital Foundation and supporters of the Lois Hole Hospital for Women through the Women and Children’s Health Research Institute. A.P. and T.M. were funded by a KAUST faculty baseline fund (BAS/1/1020-01-01). Research in the Dacks lab is funded by NSERC Discovery Grants (RES0043758 and RES0046091). Research in the Meissner lab is funded by a DFG Programme Grant (ME 2675/6-2) and by the DFG Equipment grant (INST 86/1831-1).
• Keywords: phylogenetic screen, Arl, Apicomplexa, evolutionary cell biology, Golgi, evolution, membrane trafficking, Toxoplasma, molecular evolution, CP: Cell biology, Toxoplasma gondii
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Lemgruber Soares, Dr Leandro
• Authors: Klinger, C. M., Jimenez-Ruiz, E., Mourier, T., Klingl, A., Lemgruber, L., Pain, A., Dacks, J. B., and Meissner, M.
• College/School: College of Medical Veterinary and Life Sciences > School of Infection & Immunity
• Journal Name: Cell Reports
• Publisher: Elsevier (Cell Press)
• ISSN: 2639-1856
• ISSN (Online): 2211-1247
• Copyright Holders: Copyright: © 2024 The Authors
• First Published: First published in Cell Reports
• Publisher Policy: Reproduced under a Creative Commons licence