Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point
ABSTRACT Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth’s oceans. Here the gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The 11 amphipod individu...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-06-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00009-18 |
| _version_ | 1818691847690649600 |
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| author | Weipeng Zhang Ren-Mao Tian Jin Sun Salim Bougouffa Wei Ding Lin Cai Yi Lan Haoya Tong Yongxin Li Alan J. Jamieson Vladimir B. Bajic Jeffrey C. Drazen Douglas Bartlett Pei-Yuan Qian |
| author_facet | Weipeng Zhang Ren-Mao Tian Jin Sun Salim Bougouffa Wei Ding Lin Cai Yi Lan Haoya Tong Yongxin Li Alan J. Jamieson Vladimir B. Bajic Jeffrey C. Drazen Douglas Bartlett Pei-Yuan Qian |
| author_sort | Weipeng Zhang |
| collection | DOAJ |
| description | ABSTRACT Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth’s oceans. Here the gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The 11 amphipod individuals included for analyses were dominated by Psychromonas, of which a nearly complete genome was successfully recovered (designated CDP1). Compared with previously reported free-living Psychromonas strains, CDP1 has a highly reduced genome. Genome alignment showed deletion of the trimethylamine N-oxide (TMAO) reducing gene cluster in CDP1, suggesting that the “piezolyte” function of TMAO is more important than its function in respiration, which may lead to TMAO accumulation. In terms of nutrient utilization, the bacterium retains its central carbohydrate metabolism but lacks most of the extended carbohydrate utilization pathways, suggesting the confinement of Psychromonas to the host gut and sequestration from more variable environmental conditions. Moreover, CDP1 contains a complete formate hydrogenlyase complex, which might be involved in energy production. The genomic analyses imply that CDP1 may have developed adaptive strategies for a lifestyle within the gut of the hadal amphipod H. gigas. IMPORTANCE As a unique but poorly investigated habitat within marine ecosystems, hadal trenches have received interest in recent years. This study explores the gut microbial composition and function in hadal amphipods, which are among the dominant carrion feeders in hadal habitats. Further analyses of a dominant strain revealed genomic features that may contribute to its adaptation to the amphipod gut environment. Our findings provide new insights into animal-associated bacteria in the hadal biosphere. |
| first_indexed | 2024-12-17T12:48:24Z |
| format | Article |
| id | doaj.art-aba88eb7d6524d87883450e8b2a7c7c9 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-17T12:48:24Z |
| publishDate | 2018-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-aba88eb7d6524d87883450e8b2a7c7c92022-12-21T21:47:40ZengAmerican Society for MicrobiologymSystems2379-50772018-06-013310.1128/mSystems.00009-18Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest PointWeipeng Zhang0Ren-Mao Tian1Jin Sun2Salim Bougouffa3Wei Ding4Lin Cai5Yi Lan6Haoya Tong7Yongxin Li8Alan J. Jamieson9Vladimir B. Bajic10Jeffrey C. Drazen11Douglas Bartlett12Pei-Yuan Qian13Division of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaComputational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaDivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaSchool of Marine Science and Technology, Newcastle University, Newcastle Upon Tyne, Tyne and Wear, United KingdomComputational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDepartment of Oceanography, University of Hawaii at Manoa, Honolulu, Hawaii, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USADivision of Life Science, Hong Kong University of Science and Technology, Kowloon, Hong Kong, ChinaABSTRACT Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth’s oceans. Here the gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The 11 amphipod individuals included for analyses were dominated by Psychromonas, of which a nearly complete genome was successfully recovered (designated CDP1). Compared with previously reported free-living Psychromonas strains, CDP1 has a highly reduced genome. Genome alignment showed deletion of the trimethylamine N-oxide (TMAO) reducing gene cluster in CDP1, suggesting that the “piezolyte” function of TMAO is more important than its function in respiration, which may lead to TMAO accumulation. In terms of nutrient utilization, the bacterium retains its central carbohydrate metabolism but lacks most of the extended carbohydrate utilization pathways, suggesting the confinement of Psychromonas to the host gut and sequestration from more variable environmental conditions. Moreover, CDP1 contains a complete formate hydrogenlyase complex, which might be involved in energy production. The genomic analyses imply that CDP1 may have developed adaptive strategies for a lifestyle within the gut of the hadal amphipod H. gigas. IMPORTANCE As a unique but poorly investigated habitat within marine ecosystems, hadal trenches have received interest in recent years. This study explores the gut microbial composition and function in hadal amphipods, which are among the dominant carrion feeders in hadal habitats. Further analyses of a dominant strain revealed genomic features that may contribute to its adaptation to the amphipod gut environment. Our findings provide new insights into animal-associated bacteria in the hadal biosphere.https://journals.asm.org/doi/10.1128/mSystems.00009-18amphipodgut microbiotaMariana TrenchPsychromonas |
| spellingShingle | Weipeng Zhang Ren-Mao Tian Jin Sun Salim Bougouffa Wei Ding Lin Cai Yi Lan Haoya Tong Yongxin Li Alan J. Jamieson Vladimir B. Bajic Jeffrey C. Drazen Douglas Bartlett Pei-Yuan Qian Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point mSystems amphipod gut microbiota Mariana Trench Psychromonas |
| title | Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point |
| title_full | Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point |
| title_fullStr | Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point |
| title_full_unstemmed | Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point |
| title_short | Genome Reduction in <italic toggle="yes">Psychromonas</italic> Species within the Gut of an Amphipod from the Ocean’s Deepest Point |
| title_sort | genome reduction in italic toggle yes psychromonas italic species within the gut of an amphipod from the ocean s deepest point |
| topic | amphipod gut microbiota Mariana Trench Psychromonas |
| url | https://journals.asm.org/doi/10.1128/mSystems.00009-18 |
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