Cargando…

Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis

The relationship between cytoplasmic incompatibility and the obligate intracellular alphaproteobacteria Wolbachia has for a long time been reported. Although the molecular mechanisms responsible for this reproductive alteration are beginning to be understood, the effects of Wolbachia on germ cell st...

Descripción completa

Detalles Bibliográficos
Autores principales: Riparbelli, Maria Giovanna, Pratelli, Ambra, Callaini, Giuliano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10571642/
https://www.ncbi.nlm.nih.gov/pubmed/37830551
http://dx.doi.org/10.3390/cells12192337
_version_ 1785120048771235840
author Riparbelli, Maria Giovanna
Pratelli, Ambra
Callaini, Giuliano
author_facet Riparbelli, Maria Giovanna
Pratelli, Ambra
Callaini, Giuliano
author_sort Riparbelli, Maria Giovanna
collection PubMed
description The relationship between cytoplasmic incompatibility and the obligate intracellular alphaproteobacteria Wolbachia has for a long time been reported. Although the molecular mechanisms responsible for this reproductive alteration are beginning to be understood, the effects of Wolbachia on germ cell structure and dynamics have not yet been fully investigated. We report here that the presence of Wolbachia in infected cysts of elongating spermatids is associated with major structural defects that become more evident in mature sperm. We find mitochondrial defects, an improper axoneme structure, reduced sperm numbers, and individualization failures. The large heterogeneous variety of the ultrastructural defects found in elongating spermatids and mature sperm provide the first cytological evidence for the reduced fertility associated with Wolbachia infection in Drosophila simulans males. The observed abnormalities could be the result of the mechanical stress induced by the high bacteria numbers during the process of spermatid elongation, rather than the result of the released factors affecting the proper morphogenesis of the germ cells. Moreover, high Wolbachia densities in male germ cells may not be appropriate for causing cytoplasmic incompatibility as the bacteria are harmful for spermatid differentiation, leading to abnormal sperm that is unlikely to be functional.
format Online
Article
Text
id pubmed-10571642
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-105716422023-10-14 Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis Riparbelli, Maria Giovanna Pratelli, Ambra Callaini, Giuliano Cells Article The relationship between cytoplasmic incompatibility and the obligate intracellular alphaproteobacteria Wolbachia has for a long time been reported. Although the molecular mechanisms responsible for this reproductive alteration are beginning to be understood, the effects of Wolbachia on germ cell structure and dynamics have not yet been fully investigated. We report here that the presence of Wolbachia in infected cysts of elongating spermatids is associated with major structural defects that become more evident in mature sperm. We find mitochondrial defects, an improper axoneme structure, reduced sperm numbers, and individualization failures. The large heterogeneous variety of the ultrastructural defects found in elongating spermatids and mature sperm provide the first cytological evidence for the reduced fertility associated with Wolbachia infection in Drosophila simulans males. The observed abnormalities could be the result of the mechanical stress induced by the high bacteria numbers during the process of spermatid elongation, rather than the result of the released factors affecting the proper morphogenesis of the germ cells. Moreover, high Wolbachia densities in male germ cells may not be appropriate for causing cytoplasmic incompatibility as the bacteria are harmful for spermatid differentiation, leading to abnormal sperm that is unlikely to be functional. MDPI 2023-09-22 /pmc/articles/PMC10571642/ /pubmed/37830551 http://dx.doi.org/10.3390/cells12192337 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Riparbelli, Maria Giovanna
Pratelli, Ambra
Callaini, Giuliano
Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title_full Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title_fullStr Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title_full_unstemmed Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title_short Wolbachia Induces Structural Defects Harmful to Drosophila simulans Riverside Spermiogenesis
title_sort wolbachia induces structural defects harmful to drosophila simulans riverside spermiogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10571642/
https://www.ncbi.nlm.nih.gov/pubmed/37830551
http://dx.doi.org/10.3390/cells12192337
work_keys_str_mv AT riparbellimariagiovanna wolbachiainducesstructuraldefectsharmfultodrosophilasimulansriversidespermiogenesis
AT pratelliambra wolbachiainducesstructuraldefectsharmfultodrosophilasimulansriversidespermiogenesis
AT callainigiuliano wolbachiainducesstructuraldefectsharmfultodrosophilasimulansriversidespermiogenesis