Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents
Abstract Background Chemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments wor...
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| Format: | Article |
| Language: | English |
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BMC
2017-05-01
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| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12862-017-0966-3 |
| _version_ | 1818729262413250560 |
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| author | Phuong-Thao Ho Eunji Park Soon Gyu Hong Eun-Hye Kim Kangchon Kim Sook-Jin Jang Robert C. Vrijenhoek Yong-Jin Won |
| author_facet | Phuong-Thao Ho Eunji Park Soon Gyu Hong Eun-Hye Kim Kangchon Kim Sook-Jin Jang Robert C. Vrijenhoek Yong-Jin Won |
| author_sort | Phuong-Thao Ho |
| collection | DOAJ |
| description | Abstract Background Chemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge. Results Both of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5–5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77–1.62%/nucleotide/million years. Conclusions Our present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean. |
| first_indexed | 2024-12-17T22:43:06Z |
| format | Article |
| id | doaj.art-7670d181cedc45c4b3f88fefd35a86a2 |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-17T22:43:06Z |
| publishDate | 2017-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-7670d181cedc45c4b3f88fefd35a86a22022-12-21T21:29:53ZengBMCBMC Evolutionary Biology1471-21482017-05-0117111610.1186/s12862-017-0966-3Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal ventsPhuong-Thao Ho0Eunji Park1Soon Gyu Hong2Eun-Hye Kim3Kangchon Kim4Sook-Jin Jang5Robert C. Vrijenhoek6Yong-Jin Won7Interdisciplinary Program of EcoCreative, The Graduate School, Ewha Womans UniversityDivision of EcoScience, Ewha Womans UniversityDivision of Polar Life Sciences, Korea Polar Research InstituteDivision of Polar Life Sciences, Korea Polar Research InstituteInterdisciplinary Program of EcoCreative, The Graduate School, Ewha Womans UniversityInterdisciplinary Program of EcoCreative, The Graduate School, Ewha Womans UniversityMonterey Bay Aquarium Research InstituteInterdisciplinary Program of EcoCreative, The Graduate School, Ewha Womans UniversityAbstract Background Chemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge. Results Both of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5–5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77–1.62%/nucleotide/million years. Conclusions Our present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean.http://link.springer.com/article/10.1186/s12862-017-0966-3Chemosynthetic symbiosisDeep-sea hydrothermal ventBathymodiolus musselsSulfur-oxidizing endosymbiontGammaproteobacteriaGeographical population structure |
| spellingShingle | Phuong-Thao Ho Eunji Park Soon Gyu Hong Eun-Hye Kim Kangchon Kim Sook-Jin Jang Robert C. Vrijenhoek Yong-Jin Won Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents BMC Evolutionary Biology Chemosynthetic symbiosis Deep-sea hydrothermal vent Bathymodiolus mussels Sulfur-oxidizing endosymbiont Gammaproteobacteria Geographical population structure |
| title | Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents |
| title_full | Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents |
| title_fullStr | Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents |
| title_full_unstemmed | Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents |
| title_short | Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents |
| title_sort | geographical structure of endosymbiotic bacteria hosted by bathymodiolus mussels at eastern pacific hydrothermal vents |
| topic | Chemosynthetic symbiosis Deep-sea hydrothermal vent Bathymodiolus mussels Sulfur-oxidizing endosymbiont Gammaproteobacteria Geographical population structure |
| url | http://link.springer.com/article/10.1186/s12862-017-0966-3 |
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