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Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia

The intracellular endosymbiotic proteobacteria Wolbachia have evolved across the phyla nematoda and arthropoda. In Wolbachia phylogeny, supergroup F is the only clade known so far with members from both arthropod and filarial nematode hosts and therefore can provide unique insights into their evolut...

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Autores principales: Sinha, Amit, Li, Zhiru, Poole, Catherine B, Ettwiller, Laurence, Lima, Nathália F, Ferreira, Marcelo U, Fombad, Fanny F, Wanji, Samuel, Carlow, Clotilde K S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10195089/
https://www.ncbi.nlm.nih.gov/pubmed/37154102
http://dx.doi.org/10.1093/gbe/evad073
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author Sinha, Amit
Li, Zhiru
Poole, Catherine B
Ettwiller, Laurence
Lima, Nathália F
Ferreira, Marcelo U
Fombad, Fanny F
Wanji, Samuel
Carlow, Clotilde K S
author_facet Sinha, Amit
Li, Zhiru
Poole, Catherine B
Ettwiller, Laurence
Lima, Nathália F
Ferreira, Marcelo U
Fombad, Fanny F
Wanji, Samuel
Carlow, Clotilde K S
author_sort Sinha, Amit
collection PubMed
description The intracellular endosymbiotic proteobacteria Wolbachia have evolved across the phyla nematoda and arthropoda. In Wolbachia phylogeny, supergroup F is the only clade known so far with members from both arthropod and filarial nematode hosts and therefore can provide unique insights into their evolution and biology. In this study, four new supergroup F Wolbachia genomes have been assembled using a metagenomic assembly and binning approach, wMoz and wMpe from the human filarial parasites Mansonella ozzardi and M. perstans, and wOcae and wMoviF from the blue mason bee Osmia caerulescens and the sheep ked Melophagus ovinus, respectively. A comprehensive phylogenomic analysis revealed two distinct lineages of filarial Wolbachia in supergroup F, indicating multiple horizontal transfer events between arthropod and nematode hosts. The analysis also reveals that the evolution of Wolbachia-filaria symbioses is accompanied by a convergent pseudogenization and loss of the bacterioferritin gene, a phenomenon found to be shared by all filarial Wolbachia, even those outside supergroup F. These observations indicate that differences in heme metabolism might be a key feature distinguishing filarial and arthropod Wolbachia. The new genomes provide a valuable resource for further studies on symbiosis, evolution, and the discovery of new antibiotics to treat mansonellosis.
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spelling pubmed-101950892023-05-19 Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia Sinha, Amit Li, Zhiru Poole, Catherine B Ettwiller, Laurence Lima, Nathália F Ferreira, Marcelo U Fombad, Fanny F Wanji, Samuel Carlow, Clotilde K S Genome Biol Evol Article The intracellular endosymbiotic proteobacteria Wolbachia have evolved across the phyla nematoda and arthropoda. In Wolbachia phylogeny, supergroup F is the only clade known so far with members from both arthropod and filarial nematode hosts and therefore can provide unique insights into their evolution and biology. In this study, four new supergroup F Wolbachia genomes have been assembled using a metagenomic assembly and binning approach, wMoz and wMpe from the human filarial parasites Mansonella ozzardi and M. perstans, and wOcae and wMoviF from the blue mason bee Osmia caerulescens and the sheep ked Melophagus ovinus, respectively. A comprehensive phylogenomic analysis revealed two distinct lineages of filarial Wolbachia in supergroup F, indicating multiple horizontal transfer events between arthropod and nematode hosts. The analysis also reveals that the evolution of Wolbachia-filaria symbioses is accompanied by a convergent pseudogenization and loss of the bacterioferritin gene, a phenomenon found to be shared by all filarial Wolbachia, even those outside supergroup F. These observations indicate that differences in heme metabolism might be a key feature distinguishing filarial and arthropod Wolbachia. The new genomes provide a valuable resource for further studies on symbiosis, evolution, and the discovery of new antibiotics to treat mansonellosis. Oxford University Press 2023-05-08 /pmc/articles/PMC10195089/ /pubmed/37154102 http://dx.doi.org/10.1093/gbe/evad073 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Article
Sinha, Amit
Li, Zhiru
Poole, Catherine B
Ettwiller, Laurence
Lima, Nathália F
Ferreira, Marcelo U
Fombad, Fanny F
Wanji, Samuel
Carlow, Clotilde K S
Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title_full Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title_fullStr Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title_full_unstemmed Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title_short Multiple Lineages of Nematode-Wolbachia Symbiosis in Supergroup F and Convergent Loss of Bacterioferritin in Filarial Wolbachia
title_sort multiple lineages of nematode-wolbachia symbiosis in supergroup f and convergent loss of bacterioferritin in filarial wolbachia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10195089/
https://www.ncbi.nlm.nih.gov/pubmed/37154102
http://dx.doi.org/10.1093/gbe/evad073
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