Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species

BACKGROUND: Many species of filarial nematodes depend on Wolbachia endobacteria to carry out their life cycle. Other species are naturally Wolbachia-free. The biological mechanisms underpinning Wolbachia-dependence and independence in filarial nematodes are not known. Previous studies have indicated...

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Autores principales: McNulty, Samantha N, Mullin, Andrew S, Vaughan, Jefferson A, Tkach, Vasyl V, Weil, Gary J, Fischer, Peter U
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3409033/
https://www.ncbi.nlm.nih.gov/pubmed/22530989
http://dx.doi.org/10.1186/1471-2164-13-145
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author McNulty, Samantha N
Mullin, Andrew S
Vaughan, Jefferson A
Tkach, Vasyl V
Weil, Gary J
Fischer, Peter U
author_facet McNulty, Samantha N
Mullin, Andrew S
Vaughan, Jefferson A
Tkach, Vasyl V
Weil, Gary J
Fischer, Peter U
author_sort McNulty, Samantha N
collection PubMed
description BACKGROUND: Many species of filarial nematodes depend on Wolbachia endobacteria to carry out their life cycle. Other species are naturally Wolbachia-free. The biological mechanisms underpinning Wolbachia-dependence and independence in filarial nematodes are not known. Previous studies have indicated that Wolbachia have an impact on mitochondrial gene expression, which may suggest a role in energy metabolism. If Wolbachia can supplement host energy metabolism, reduced mitochondrial function in infected filarial species may account for Wolbachia-dependence. Wolbachia also have a strong influence on mitochondrial evolution due to vertical co-transmission. This could drive alterations in mitochondrial genome sequence in infected species. Comparisons between the mitochondrial genome sequences of Wolbachia-dependent and independent filarial worms may reveal differences indicative of altered mitochondrial function. RESULTS: The mitochondrial genomes of 5 species of filarial nematodes, Acanthocheilonema viteae, Chandlerella quiscali, Loa loa, Onchocerca flexuosa, and Wuchereria bancrofti, were sequenced, annotated and compared with available mitochondrial genome sequences from Brugia malayi, Dirofilaria immitis, Onchocerca volvulus and Setaria digitata. B. malayi, D. immitis, O. volvulus and W. bancrofti are Wolbachia-dependent while A. viteae, C. quiscali, L. loa, O. flexuosa and S. digitata are Wolbachia-free. The 9 mitochondrial genomes were similar in size and AT content and encoded the same 12 protein-coding genes, 22 tRNAs and 2 rRNAs. Synteny was perfectly preserved in all species except C. quiscali, which had a different order for 5 tRNA genes. Protein-coding genes were expressed at the RNA level in all examined species. In phylogenetic trees based on mitochondrial protein-coding sequences, species did not cluster according to Wolbachia dependence. CONCLUSIONS: Thus far, no discernable differences were detected between the mitochondrial genome sequences of Wolbachia-dependent and independent species. Additional research will be needed to determine whether mitochondria from Wolbachia-dependent filarial species show reduced function in comparison to the mitochondria of Wolbachia-independent species despite their sequence-level similarities.
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spelling pubmed-34090332012-08-01 Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species McNulty, Samantha N Mullin, Andrew S Vaughan, Jefferson A Tkach, Vasyl V Weil, Gary J Fischer, Peter U BMC Genomics Research Article BACKGROUND: Many species of filarial nematodes depend on Wolbachia endobacteria to carry out their life cycle. Other species are naturally Wolbachia-free. The biological mechanisms underpinning Wolbachia-dependence and independence in filarial nematodes are not known. Previous studies have indicated that Wolbachia have an impact on mitochondrial gene expression, which may suggest a role in energy metabolism. If Wolbachia can supplement host energy metabolism, reduced mitochondrial function in infected filarial species may account for Wolbachia-dependence. Wolbachia also have a strong influence on mitochondrial evolution due to vertical co-transmission. This could drive alterations in mitochondrial genome sequence in infected species. Comparisons between the mitochondrial genome sequences of Wolbachia-dependent and independent filarial worms may reveal differences indicative of altered mitochondrial function. RESULTS: The mitochondrial genomes of 5 species of filarial nematodes, Acanthocheilonema viteae, Chandlerella quiscali, Loa loa, Onchocerca flexuosa, and Wuchereria bancrofti, were sequenced, annotated and compared with available mitochondrial genome sequences from Brugia malayi, Dirofilaria immitis, Onchocerca volvulus and Setaria digitata. B. malayi, D. immitis, O. volvulus and W. bancrofti are Wolbachia-dependent while A. viteae, C. quiscali, L. loa, O. flexuosa and S. digitata are Wolbachia-free. The 9 mitochondrial genomes were similar in size and AT content and encoded the same 12 protein-coding genes, 22 tRNAs and 2 rRNAs. Synteny was perfectly preserved in all species except C. quiscali, which had a different order for 5 tRNA genes. Protein-coding genes were expressed at the RNA level in all examined species. In phylogenetic trees based on mitochondrial protein-coding sequences, species did not cluster according to Wolbachia dependence. CONCLUSIONS: Thus far, no discernable differences were detected between the mitochondrial genome sequences of Wolbachia-dependent and independent species. Additional research will be needed to determine whether mitochondria from Wolbachia-dependent filarial species show reduced function in comparison to the mitochondria of Wolbachia-independent species despite their sequence-level similarities. BioMed Central 2012-04-24 /pmc/articles/PMC3409033/ /pubmed/22530989 http://dx.doi.org/10.1186/1471-2164-13-145 Text en Copyright ©2012 McNulty et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
McNulty, Samantha N
Mullin, Andrew S
Vaughan, Jefferson A
Tkach, Vasyl V
Weil, Gary J
Fischer, Peter U
Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title_full Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title_fullStr Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title_full_unstemmed Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title_short Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species
title_sort comparing the mitochondrial genomes of wolbachia-dependent and independent filarial nematode species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3409033/
https://www.ncbi.nlm.nih.gov/pubmed/22530989
http://dx.doi.org/10.1186/1471-2164-13-145
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