Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier
IntroductionThe protozoan parasite Trichomonas vaginalis is the most common cellular sexually transmitted disease in humans, and the closely related species Trichomonas gallinae is an avian parasite of ecological and economic importance. Phylogenetic evidence suggests T. vaginalis arose during bird...
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| Format: | Article |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1242275/full |
| _version_ | 1797676769557348352 |
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| author | Nicholas P. Bailey Yuxin Shao Shaodua Du Peter G. Foster Jennifer Fettweis Neil Hall Neil Hall Zheng Wang Robert P. Hirt |
| author_facet | Nicholas P. Bailey Yuxin Shao Shaodua Du Peter G. Foster Jennifer Fettweis Neil Hall Neil Hall Zheng Wang Robert P. Hirt |
| author_sort | Nicholas P. Bailey |
| collection | DOAJ |
| description | IntroductionThe protozoan parasite Trichomonas vaginalis is the most common cellular sexually transmitted disease in humans, and the closely related species Trichomonas gallinae is an avian parasite of ecological and economic importance. Phylogenetic evidence suggests T. vaginalis arose during bird to human transmission of a T. gallinae-like ancestor. Trichomonas vaginalis shares a strong clinical association with the independent sexually transmitted pathogen Metamycoplasma (formerly Mycoplasma) hominis, and the uncultured bacterium “Candidatus Malacoplasma (formerly Mycoplasma) girerdii,” with the latter association being an order of magnitude stronger. Both bacterial species have been shown to profoundly influence T. vaginalis growth, energy production and virulence-associated mechanisms.MethodsEvidence for a novel Malacoplasma sp. was discovered by in vivo Illumina metatranscriptomics sequencing of the T. gallinae-infected pigeon mouth. We leveraged published 16S rDNA profiling data from digestive tract of 12 healthy and 24 T. gallinae-infected pigeons to investigate association between the novel Malacoplasma sp. and T. gallinae. We utilised Illumina metagenomics sequencing targeted to pigeon oral and crop samples infected with the novel Malacoplasma sp. to generate its full-length genome sequence. Sequence similarity network analysis was used to compare annotated proteins from the novel Malacoplasma sp. with a range of other related species.ResultsHere we present evidence for a novel Malacoplasma species, related to “Ca. M. girerdii,” that is strongly associated with T. gallinae in the upper digestive tract of domestic pigeons. Analysis of the genome sequence revealed gene features apparently specific to a Trichomonas-symbiotic Malacoplasma lineage.DiscussionThese data support a model of long-term association between Trichomonas and Malacoplasma spp. that has been conserved across diversification of the Trichomonas lineage and the host species barrier from birds to human. |
| first_indexed | 2024-03-11T22:35:06Z |
| format | Article |
| id | doaj.art-a8a5a02ed2984c838b0543a0fb1e9fa2 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-11T22:35:06Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-a8a5a02ed2984c838b0543a0fb1e9fa22023-09-22T19:01:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12422751242275Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrierNicholas P. Bailey0Yuxin Shao1Shaodua Du2Peter G. Foster3Jennifer Fettweis4Neil Hall5Neil Hall6Zheng Wang7Robert P. Hirt8Biosciences Institute, Newcastle University, Newcastle-upon-Tyne, United KingdomInstitute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaInstitute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaNatural History Museum, London, United KingdomVirginia Commonwealth University, Richmond, VA, United StatesEarlham Institute, Norwich, United KingdomSchool of Biological Sciences, University of East Anglia, Norwich, Norfolk, United KingdomInstitute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBiosciences Institute, Newcastle University, Newcastle-upon-Tyne, United KingdomIntroductionThe protozoan parasite Trichomonas vaginalis is the most common cellular sexually transmitted disease in humans, and the closely related species Trichomonas gallinae is an avian parasite of ecological and economic importance. Phylogenetic evidence suggests T. vaginalis arose during bird to human transmission of a T. gallinae-like ancestor. Trichomonas vaginalis shares a strong clinical association with the independent sexually transmitted pathogen Metamycoplasma (formerly Mycoplasma) hominis, and the uncultured bacterium “Candidatus Malacoplasma (formerly Mycoplasma) girerdii,” with the latter association being an order of magnitude stronger. Both bacterial species have been shown to profoundly influence T. vaginalis growth, energy production and virulence-associated mechanisms.MethodsEvidence for a novel Malacoplasma sp. was discovered by in vivo Illumina metatranscriptomics sequencing of the T. gallinae-infected pigeon mouth. We leveraged published 16S rDNA profiling data from digestive tract of 12 healthy and 24 T. gallinae-infected pigeons to investigate association between the novel Malacoplasma sp. and T. gallinae. We utilised Illumina metagenomics sequencing targeted to pigeon oral and crop samples infected with the novel Malacoplasma sp. to generate its full-length genome sequence. Sequence similarity network analysis was used to compare annotated proteins from the novel Malacoplasma sp. with a range of other related species.ResultsHere we present evidence for a novel Malacoplasma species, related to “Ca. M. girerdii,” that is strongly associated with T. gallinae in the upper digestive tract of domestic pigeons. Analysis of the genome sequence revealed gene features apparently specific to a Trichomonas-symbiotic Malacoplasma lineage.DiscussionThese data support a model of long-term association between Trichomonas and Malacoplasma spp. that has been conserved across diversification of the Trichomonas lineage and the host species barrier from birds to human.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1242275/fullTrichomonas gallinaeTrichomonas vaginalisCandidatus Malacoplasma/Mycoplasma girerdiinew bacteria speciesCandidatus Malacoplasma/Mycoplasma trichamicametagenomics |
| spellingShingle | Nicholas P. Bailey Yuxin Shao Shaodua Du Peter G. Foster Jennifer Fettweis Neil Hall Neil Hall Zheng Wang Robert P. Hirt Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier Frontiers in Microbiology Trichomonas gallinae Trichomonas vaginalis Candidatus Malacoplasma/Mycoplasma girerdii new bacteria species Candidatus Malacoplasma/Mycoplasma trichamica metagenomics |
| title | Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier |
| title_full | Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier |
| title_fullStr | Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier |
| title_full_unstemmed | Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier |
| title_short | Evolutionary conservation of Trichomonas-mycoplasma symbiosis across the host species barrier |
| title_sort | evolutionary conservation of trichomonas mycoplasma symbiosis across the host species barrier |
| topic | Trichomonas gallinae Trichomonas vaginalis Candidatus Malacoplasma/Mycoplasma girerdii new bacteria species Candidatus Malacoplasma/Mycoplasma trichamica metagenomics |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1242275/full |
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