Adaptive evolution of stress response genes in parasites aligns with host niche diversity

Abstract Background Stress responses are key the survival of parasites and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the evolution of molecular pathways dealing with environmental stressors in parasitic animals remains limited. Her...

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Main Authors: Armando J. Cruz-Laufer, Maarten P. M. Vanhove, Lutz Bachmann, Maxwell Barson, Hassan Bassirou, Arnold R. Bitja Nyom, Mare Geraerts, Christoph Hahn, Tine Huyse, Gyrhaiss Kapepula Kasembele, Samuel Njom, Philipp Resl, Karen Smeets, Nikol Kmentová
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Language:English
Published: BMC 2025-01-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-024-02091-w
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author Armando J. Cruz-Laufer
Maarten P. M. Vanhove
Lutz Bachmann
Maxwell Barson
Hassan Bassirou
Arnold R. Bitja Nyom
Mare Geraerts
Christoph Hahn
Tine Huyse
Gyrhaiss Kapepula Kasembele
Samuel Njom
Philipp Resl
Karen Smeets
Nikol Kmentová
author_facet Armando J. Cruz-Laufer
Maarten P. M. Vanhove
Lutz Bachmann
Maxwell Barson
Hassan Bassirou
Arnold R. Bitja Nyom
Mare Geraerts
Christoph Hahn
Tine Huyse
Gyrhaiss Kapepula Kasembele
Samuel Njom
Philipp Resl
Karen Smeets
Nikol Kmentová
author_sort Armando J. Cruz-Laufer
collection DOAJ
description Abstract Background Stress responses are key the survival of parasites and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the evolution of molecular pathways dealing with environmental stressors in parasitic animals remains limited. Here, we tested the link between adaptive evolution of parasite stress response genes and their ecological diversity and species richness. We comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two model parasitic flatworm lineages with contrasting ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monopisthocotyla), through whole-genome sequencing of 11 species followed by in silico exon bait capture as well as phylogenetic and codon analyses. Results We assembled the sequences of 48 stress-related genes and report the first foraging (For) gene orthologs in flatworms. We found duplications of heat shock (Hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (H sp) and behaviour (For) in species of Cichlidogyrus infecting East African cichlids—a host lineage under adaptive radiation. These patterns are consistent with a potential adaptation linked to a co-radiation of these parasites and their hosts. Additionally, the absence of cytochrome P450 and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes considered essential for metazoan life. Conclusions This study potentially identifies the first molecular function linked to a flatworm radiation. Furthermore, the observed gene duplications and positive selection indicate the potentially important role of stress responses for the ecological adaptation of parasite species.
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spelling doaj-art-4cf544def0ad42fb98468015e6a39f202025-01-19T12:38:47ZengBMCBMC Biology1741-70072025-01-0123111610.1186/s12915-024-02091-wAdaptive evolution of stress response genes in parasites aligns with host niche diversityArmando J. Cruz-Laufer0Maarten P. M. Vanhove1Lutz Bachmann2Maxwell Barson3Hassan Bassirou4Arnold R. Bitja Nyom5Mare Geraerts6Christoph Hahn7Tine Huyse8Gyrhaiss Kapepula Kasembele9Samuel Njom10Philipp Resl11Karen Smeets12Nikol Kmentová13Faculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityFaculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityNatural History Museum, University of OsloDepartment of Biological Sciences, University of BotswanaDepartment of Biological Sciences, University of NgaoundéréDepartment of Biological Sciences, University of NgaoundéréFaculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityInstitute of Biology, University of GrazDepartment of Biology, Royal Museum for Central AfricaFaculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityDepartment of Biological Sciences, University of NgaoundéréInstitute of Biology, University of GrazFaculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityFaculty of Sciences, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, UHasselt – Hasselt UniversityAbstract Background Stress responses are key the survival of parasites and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the evolution of molecular pathways dealing with environmental stressors in parasitic animals remains limited. Here, we tested the link between adaptive evolution of parasite stress response genes and their ecological diversity and species richness. We comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two model parasitic flatworm lineages with contrasting ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monopisthocotyla), through whole-genome sequencing of 11 species followed by in silico exon bait capture as well as phylogenetic and codon analyses. Results We assembled the sequences of 48 stress-related genes and report the first foraging (For) gene orthologs in flatworms. We found duplications of heat shock (Hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (H sp) and behaviour (For) in species of Cichlidogyrus infecting East African cichlids—a host lineage under adaptive radiation. These patterns are consistent with a potential adaptation linked to a co-radiation of these parasites and their hosts. Additionally, the absence of cytochrome P450 and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes considered essential for metazoan life. Conclusions This study potentially identifies the first molecular function linked to a flatworm radiation. Furthermore, the observed gene duplications and positive selection indicate the potentially important role of stress responses for the ecological adaptation of parasite species.https://doi.org/10.1186/s12915-024-02091-wComparative genomicsPositive selectionMonopisthocotylaHeat shock proteinsOxidative stress
spellingShingle Armando J. Cruz-Laufer
Maarten P. M. Vanhove
Lutz Bachmann
Maxwell Barson
Hassan Bassirou
Arnold R. Bitja Nyom
Mare Geraerts
Christoph Hahn
Tine Huyse
Gyrhaiss Kapepula Kasembele
Samuel Njom
Philipp Resl
Karen Smeets
Nikol Kmentová
Adaptive evolution of stress response genes in parasites aligns with host niche diversity
BMC Biology
Comparative genomics
Positive selection
Monopisthocotyla
Heat shock proteins
Oxidative stress
title Adaptive evolution of stress response genes in parasites aligns with host niche diversity
title_full Adaptive evolution of stress response genes in parasites aligns with host niche diversity
title_fullStr Adaptive evolution of stress response genes in parasites aligns with host niche diversity
title_full_unstemmed Adaptive evolution of stress response genes in parasites aligns with host niche diversity
title_short Adaptive evolution of stress response genes in parasites aligns with host niche diversity
title_sort adaptive evolution of stress response genes in parasites aligns with host niche diversity
topic Comparative genomics
Positive selection
Monopisthocotyla
Heat shock proteins
Oxidative stress
url https://doi.org/10.1186/s12915-024-02091-w
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