Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation
ABSTRACT The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental, and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains,...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-08-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00284-23 |
| _version_ | 1797730326860005376 |
|---|---|
| author | Corinna Breusing Yao Xiao Shelbi L. Russell Russell B. Corbett-Detig Sixuan Li Jin Sun Chong Chen Yi Lan Pei-Yuan Qian Roxanne A. Beinart |
| author_facet | Corinna Breusing Yao Xiao Shelbi L. Russell Russell B. Corbett-Detig Sixuan Li Jin Sun Chong Chen Yi Lan Pei-Yuan Qian Roxanne A. Beinart |
| author_sort | Corinna Breusing |
| collection | DOAJ |
| description | ABSTRACT The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental, and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains, it is unknown how differences in ecological characteristics among host-symbiont associations influence the genomic structure of symbiont populations. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses. Bathymodiolus septemdierum lives in close symbiotic relationship with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with little exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum show structuring by geographic location, but that the dominant symbiont strain is uncorrelated with vent site. These patterns are in contrast to co-occurring Alviniconcha and Ifremeria gastropod symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. Our results suggest that relative habitat homogeneity combined with sufficient symbiont dispersal and genomic mixing might promote persistence of similar symbiont strains across geographic locations, while mixotrophy might decrease selective pressures on the host to affiliate with locally adapted symbiont strains. Overall, these data contribute to our understanding of the potential mechanisms influencing symbiont population structure across a spectrum of marine microbial symbioses that occupy contrasting ecological niches. IMPORTANCE Beneficial relationships between animals and microbial organisms (symbionts) are ubiquitous in nature. In the ocean, microbial symbionts are typically acquired from the environment and their composition across geographic locations is often shaped by adaptation to local habitat conditions. However, it is currently unknown how generalizable these patterns are across symbiotic systems that have contrasting ecological characteristics. To address this question, we compared symbiont population structure between deep-sea hydrothermal vent mussels and co-occurring but ecologically distinct snail species. Our analyses show that mussel symbiont populations are less partitioned by geography and do not demonstrate evidence for environmental adaptation. We posit that the mussel's mixotrophic feeding mode may lower its need to affiliate with locally adapted symbiont strains, while microhabitat stability and symbiont genomic mixing likely favors persistence of symbiont strains across geographic locations. Altogether, these findings further our understanding of the mechanisms shaping symbiont population structure in marine environmentally transmitted symbioses. |
| first_indexed | 2024-03-12T11:42:41Z |
| format | Article |
| id | doaj.art-8e185b075789404eb8b56b83e62d4ea3 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-12T11:42:41Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-8e185b075789404eb8b56b83e62d4ea32023-08-31T13:00:43ZengAmerican Society for MicrobiologymSystems2379-50772023-08-018410.1128/msystems.00284-23Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiationCorinna Breusing0Yao Xiao1Shelbi L. Russell2Russell B. Corbett-Detig3Sixuan Li4Jin Sun5Chong Chen6Yi Lan7Pei-Yuan Qian8Roxanne A. Beinart9Graduate School of Oceanography, University of Rhode Island , Narragansett, Rhode Island, USADepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology , Hong Kong, ChinaDepartment of Biomolecular Engineering, University of California Santa Cruz , Santa Cruz, California, USADepartment of Biomolecular Engineering, University of California Santa Cruz , Santa Cruz, California, USAGraduate School of Oceanography, University of Rhode Island , Narragansett, Rhode Island, USAInstitute of Evolution & Marine Biodiversity, Ocean University of China , Qingdao, ChinaX-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC) , Yokosuka, JapanDepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology , Hong Kong, ChinaDepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology , Hong Kong, ChinaGraduate School of Oceanography, University of Rhode Island , Narragansett, Rhode Island, USAABSTRACT The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental, and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains, it is unknown how differences in ecological characteristics among host-symbiont associations influence the genomic structure of symbiont populations. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses. Bathymodiolus septemdierum lives in close symbiotic relationship with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with little exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum show structuring by geographic location, but that the dominant symbiont strain is uncorrelated with vent site. These patterns are in contrast to co-occurring Alviniconcha and Ifremeria gastropod symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. Our results suggest that relative habitat homogeneity combined with sufficient symbiont dispersal and genomic mixing might promote persistence of similar symbiont strains across geographic locations, while mixotrophy might decrease selective pressures on the host to affiliate with locally adapted symbiont strains. Overall, these data contribute to our understanding of the potential mechanisms influencing symbiont population structure across a spectrum of marine microbial symbioses that occupy contrasting ecological niches. IMPORTANCE Beneficial relationships between animals and microbial organisms (symbionts) are ubiquitous in nature. In the ocean, microbial symbionts are typically acquired from the environment and their composition across geographic locations is often shaped by adaptation to local habitat conditions. However, it is currently unknown how generalizable these patterns are across symbiotic systems that have contrasting ecological characteristics. To address this question, we compared symbiont population structure between deep-sea hydrothermal vent mussels and co-occurring but ecologically distinct snail species. Our analyses show that mussel symbiont populations are less partitioned by geography and do not demonstrate evidence for environmental adaptation. We posit that the mussel's mixotrophic feeding mode may lower its need to affiliate with locally adapted symbiont strains, while microhabitat stability and symbiont genomic mixing likely favors persistence of symbiont strains across geographic locations. Altogether, these findings further our understanding of the mechanisms shaping symbiont population structure in marine environmentally transmitted symbioses.https://journals.asm.org/doi/10.1128/msystems.00284-23chemosynthetic symbiosishydrothermal ventssymbiont strain compositionniche partitioninghomologous recombinationlocal adaptation |
| spellingShingle | Corinna Breusing Yao Xiao Shelbi L. Russell Russell B. Corbett-Detig Sixuan Li Jin Sun Chong Chen Yi Lan Pei-Yuan Qian Roxanne A. Beinart Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation mSystems chemosynthetic symbiosis hydrothermal vents symbiont strain composition niche partitioning homologous recombination local adaptation |
| title | Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| title_full | Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| title_fullStr | Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| title_full_unstemmed | Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| title_short | Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| title_sort | ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation |
| topic | chemosynthetic symbiosis hydrothermal vents symbiont strain composition niche partitioning homologous recombination local adaptation |
| url | https://journals.asm.org/doi/10.1128/msystems.00284-23 |
| work_keys_str_mv | AT corinnabreusing ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT yaoxiao ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT shelbilrussell ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT russellbcorbettdetig ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT sixuanli ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT jinsun ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT chongchen ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT yilan ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT peiyuanqian ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation AT roxanneabeinart ecologicaldifferencesamonghydrothermalventsymbiosesmaydrivecontrastingpatternsofsymbiontpopulationdifferentiation |