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Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster
Wolbachia is a group of intracellular symbiotic bacteria that widely infect arthropods and nematodes. Wolbachia infection can regulate host reproduction with the most common phenotype in insects being cytoplasmic incompatibility (CI), which results in embryonic lethality when uninfected eggs fertili...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8384202/ https://www.ncbi.nlm.nih.gov/pubmed/34383852 http://dx.doi.org/10.1371/journal.ppat.1009859 |
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author | Zhang, Hua-Bao Cao, Zheng Qiao, Jun-Xue Zhong, Zi-Qian Pan, Chen-Chen Liu, Chen Zhang, Li-Min Wang, Yu-Feng |
author_facet | Zhang, Hua-Bao Cao, Zheng Qiao, Jun-Xue Zhong, Zi-Qian Pan, Chen-Chen Liu, Chen Zhang, Li-Min Wang, Yu-Feng |
author_sort | Zhang, Hua-Bao |
collection | PubMed |
description | Wolbachia is a group of intracellular symbiotic bacteria that widely infect arthropods and nematodes. Wolbachia infection can regulate host reproduction with the most common phenotype in insects being cytoplasmic incompatibility (CI), which results in embryonic lethality when uninfected eggs fertilized with sperms from infected males. This suggests that CI-induced defects are mainly in paternal side. However, whether Wolbachia-induced metabolic changes play a role in the mechanism of paternal-linked defects in embryonic development is not known. In the current study, we first use untargeted metabolomics method with LC-MS to explore how Wolbachia infection influences the metabolite profiling of the insect hosts. The untargeted metabolomics revealed 414 potential differential metabolites between Wolbachia-infected and uninfected 1-day-old (1d) male flies. Most of the differential metabolites were significantly up-regulated due to Wolbachia infection. Thirty-four metabolic pathways such as carbohydrate, lipid and amino acid, and vitamin and cofactor metabolism were affected by Wolbachia infection. Then, we applied targeted metabolomics analysis with GC-MS and showed that Wolbachia infection resulted in an increased energy expenditure of the host by regulating glycometabolism and fatty acid catabolism, which was compensated by increased food uptake. Furthermore, overexpressing two acyl-CoA catabolism related genes, Dbi (coding for diazepam-binding inhibitor) or Mcad (coding for medium-chain acyl-CoA dehydrogenase), ubiquitously or specially in testes caused significantly decreased paternal-effect egg hatch rate. Oxidative stress and abnormal mitochondria induced by Wolbachia infection disrupted the formation of sperm nebenkern. These findings provide new insights into mechanisms of Wolbachia-induced paternal defects from metabolic phenotypes. |
format | Online Article Text |
id | pubmed-8384202 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-83842022021-08-25 Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster Zhang, Hua-Bao Cao, Zheng Qiao, Jun-Xue Zhong, Zi-Qian Pan, Chen-Chen Liu, Chen Zhang, Li-Min Wang, Yu-Feng PLoS Pathog Research Article Wolbachia is a group of intracellular symbiotic bacteria that widely infect arthropods and nematodes. Wolbachia infection can regulate host reproduction with the most common phenotype in insects being cytoplasmic incompatibility (CI), which results in embryonic lethality when uninfected eggs fertilized with sperms from infected males. This suggests that CI-induced defects are mainly in paternal side. However, whether Wolbachia-induced metabolic changes play a role in the mechanism of paternal-linked defects in embryonic development is not known. In the current study, we first use untargeted metabolomics method with LC-MS to explore how Wolbachia infection influences the metabolite profiling of the insect hosts. The untargeted metabolomics revealed 414 potential differential metabolites between Wolbachia-infected and uninfected 1-day-old (1d) male flies. Most of the differential metabolites were significantly up-regulated due to Wolbachia infection. Thirty-four metabolic pathways such as carbohydrate, lipid and amino acid, and vitamin and cofactor metabolism were affected by Wolbachia infection. Then, we applied targeted metabolomics analysis with GC-MS and showed that Wolbachia infection resulted in an increased energy expenditure of the host by regulating glycometabolism and fatty acid catabolism, which was compensated by increased food uptake. Furthermore, overexpressing two acyl-CoA catabolism related genes, Dbi (coding for diazepam-binding inhibitor) or Mcad (coding for medium-chain acyl-CoA dehydrogenase), ubiquitously or specially in testes caused significantly decreased paternal-effect egg hatch rate. Oxidative stress and abnormal mitochondria induced by Wolbachia infection disrupted the formation of sperm nebenkern. These findings provide new insights into mechanisms of Wolbachia-induced paternal defects from metabolic phenotypes. Public Library of Science 2021-08-12 /pmc/articles/PMC8384202/ /pubmed/34383852 http://dx.doi.org/10.1371/journal.ppat.1009859 Text en © 2021 Zhang et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Zhang, Hua-Bao Cao, Zheng Qiao, Jun-Xue Zhong, Zi-Qian Pan, Chen-Chen Liu, Chen Zhang, Li-Min Wang, Yu-Feng Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title | Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title_full | Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title_fullStr | Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title_full_unstemmed | Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title_short | Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster |
title_sort | metabolomics provide new insights into mechanisms of wolbachia-induced paternal defects in drosophila melanogaster |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8384202/ https://www.ncbi.nlm.nih.gov/pubmed/34383852 http://dx.doi.org/10.1371/journal.ppat.1009859 |
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