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Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes

INTRODUCTION: The genus Wolbachia provides a typical example of intracellular bacteria that infect the germline of arthropods and filarial nematodes worldwide. Their importance as biological regulators of invertebrates, so it is particularly important to study the evolution, divergence and host adap...

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Autores principales: Liu, Bo, Ren, Ye-Song, Su, Cheng-Yuan, Abe, Yoshihisa, Zhu, Dao-Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9937081/
https://www.ncbi.nlm.nih.gov/pubmed/36819029
http://dx.doi.org/10.3389/fmicb.2023.1084839
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author Liu, Bo
Ren, Ye-Song
Su, Cheng-Yuan
Abe, Yoshihisa
Zhu, Dao-Hong
author_facet Liu, Bo
Ren, Ye-Song
Su, Cheng-Yuan
Abe, Yoshihisa
Zhu, Dao-Hong
author_sort Liu, Bo
collection PubMed
description INTRODUCTION: The genus Wolbachia provides a typical example of intracellular bacteria that infect the germline of arthropods and filarial nematodes worldwide. Their importance as biological regulators of invertebrates, so it is particularly important to study the evolution, divergence and host adaptation of these bacteria at the genome-wide level. METHODS: Here, we used publicly available Wolbachia genomes to reconstruct their evolutionary history and explore their adaptation under host selection. RESULTS: Our findings indicate that segmental and single-gene duplications, such as DNA methylase, bZIP transcription factor, heat shock protein 90, in single monophyletic Wolbachia lineages (including supergroups A and B) may be responsible for improving the ability to adapt to a broad host range in arthropod-infecting strains. In contrast to A strains, high genetic diversity and rapidly evolving gene families occur in B strains, which may promote the ability of supergroup B strains to adapt to new hosts and their large-scale spreading. In addition, we hypothesize that there might have been two independent horizontal transfer events of cif genes in two sublineages of supergroup A strains. Interestingly, during the independent evolution of supergroup A and B strains, the rapid evolution of cif genes in supergroup B strains resulted in the loss of their functional domain, reflected in a possible decrease in the proportion of induced cytoplasmic incompatibility (CI) strains. DISCUSSION: This present study highlights for reconstructing of evolutionary history, addressing host adaptation-related evolution and exploring the origin and divergence of CI genes in each Wolbachia supergroup. Our results thus not only provide a basis for further exploring the evolutionary history of Wolbachia adaptation under host selection but also reveal a new research direction for studying the molecular regulation of Wolbachia- induced cytoplasmic incompatibility.
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spelling pubmed-99370812023-02-18 Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes Liu, Bo Ren, Ye-Song Su, Cheng-Yuan Abe, Yoshihisa Zhu, Dao-Hong Front Microbiol Microbiology INTRODUCTION: The genus Wolbachia provides a typical example of intracellular bacteria that infect the germline of arthropods and filarial nematodes worldwide. Their importance as biological regulators of invertebrates, so it is particularly important to study the evolution, divergence and host adaptation of these bacteria at the genome-wide level. METHODS: Here, we used publicly available Wolbachia genomes to reconstruct their evolutionary history and explore their adaptation under host selection. RESULTS: Our findings indicate that segmental and single-gene duplications, such as DNA methylase, bZIP transcription factor, heat shock protein 90, in single monophyletic Wolbachia lineages (including supergroups A and B) may be responsible for improving the ability to adapt to a broad host range in arthropod-infecting strains. In contrast to A strains, high genetic diversity and rapidly evolving gene families occur in B strains, which may promote the ability of supergroup B strains to adapt to new hosts and their large-scale spreading. In addition, we hypothesize that there might have been two independent horizontal transfer events of cif genes in two sublineages of supergroup A strains. Interestingly, during the independent evolution of supergroup A and B strains, the rapid evolution of cif genes in supergroup B strains resulted in the loss of their functional domain, reflected in a possible decrease in the proportion of induced cytoplasmic incompatibility (CI) strains. DISCUSSION: This present study highlights for reconstructing of evolutionary history, addressing host adaptation-related evolution and exploring the origin and divergence of CI genes in each Wolbachia supergroup. Our results thus not only provide a basis for further exploring the evolutionary history of Wolbachia adaptation under host selection but also reveal a new research direction for studying the molecular regulation of Wolbachia- induced cytoplasmic incompatibility. Frontiers Media S.A. 2023-02-03 /pmc/articles/PMC9937081/ /pubmed/36819029 http://dx.doi.org/10.3389/fmicb.2023.1084839 Text en Copyright © 2023 Liu, Ren, Su, Abe and Zhu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Liu, Bo
Ren, Ye-Song
Su, Cheng-Yuan
Abe, Yoshihisa
Zhu, Dao-Hong
Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title_full Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title_fullStr Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title_full_unstemmed Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title_short Pangenomic analysis of Wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
title_sort pangenomic analysis of wolbachia provides insight into the evolution of host adaptation and cytoplasmic incompatibility factor genes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9937081/
https://www.ncbi.nlm.nih.gov/pubmed/36819029
http://dx.doi.org/10.3389/fmicb.2023.1084839
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