Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles
ABSTRACT Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describ...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-04-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00032-22 |
| _version_ | 1818141638153732096 |
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| author | Jessica M. Blanton Logan M. Peoples Mackenzie E. Gerringer Caroline M. Iacuaniello Natalya D. Gallo Thomas D. Linley Alan J. Jamieson Jeffrey C. Drazen Douglas H. Bartlett Eric E. Allen |
| author_facet | Jessica M. Blanton Logan M. Peoples Mackenzie E. Gerringer Caroline M. Iacuaniello Natalya D. Gallo Thomas D. Linley Alan J. Jamieson Jeffrey C. Drazen Douglas H. Bartlett Eric E. Allen |
| author_sort | Jessica M. Blanton |
| collection | DOAJ |
| description | ABSTRACT Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describe the gut microbiomes of two hadal snailfishes, Pseudoliparis swirei (Mariana Trench) and Notoliparis kermadecensis (Kermadec Trench), using 16S rRNA gene amplicon sequencing. We contextualize these microbiomes with comparisons to the abyssal macrourid Coryphaenoides yaquinae and the continental shelf-dwelling snailfish Careproctus melanurus. The microbial communities of the hadal snailfishes were distinct from their shallower counterparts and were dominated by the same sequences related to the Mycoplasmataceae and Desulfovibrionaceae. These shared taxa indicate that symbiont lineages have remained similar to the ancestral symbiont since their geographic separation or that they are dispersed between geographically distant trenches and subsequently colonize specific hosts. The abyssal and hadal fishes contained sequences related to known, cultured piezophiles, microbes that grow optimally under high hydrostatic pressure, including Psychromonas, Moritella, and Shewanella. These taxa are adept at colonizing nutrient-rich environments present in the deep ocean, such as on particles and in the guts of hosts, and we hypothesize they could make a dietary contribution to deep-sea fishes by degrading chitin and producing fatty acids. We characterize the gut microbiota within some of the deepest fishes to provide new insight into the diversity and distribution of host-associated microbial taxa and the potential of these animals, and the microbes they harbor, for understanding adaptation to deep-sea habitats. IMPORTANCE Hadal trenches, characterized by high hydrostatic pressures and low temperatures, are one of the most extreme environments on our planet. By examining the microbiome of abyssal and hadal fishes, we provide insight into the diversity and distribution of host-associated life at great depth. Our findings show that there are similar microbial populations in fishes geographically separated by thousands of miles, reflecting strong selection for specific microbial lineages. Only a few psychropiezophilic taxa, which do not reflect the diversity of microbial life at great depth, have been successfully isolated in the laboratory. Our examination of deep-sea fish microbiomes shows that typical high-pressure culturing methodologies, which have largely remained unchanged since the pioneering work of Claude ZoBell in the 1950s, may simulate the chemical environment found in animal guts and helps explain why the same deep-sea genera are consistently isolated. |
| first_indexed | 2024-12-11T11:03:03Z |
| format | Article |
| id | doaj.art-954801faa63d4ebcad6f59e89658491f |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-11T11:03:03Z |
| publishDate | 2022-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-954801faa63d4ebcad6f59e89658491f2022-12-22T01:09:48ZengAmerican Society for MicrobiologymSphere2379-50422022-04-017210.1128/msphere.00032-22Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known PiezophilesJessica M. Blanton0Logan M. Peoples1Mackenzie E. Gerringer2Caroline M. Iacuaniello3Natalya D. Gallo4Thomas D. Linley5Alan J. Jamieson6Jeffrey C. Drazen7Douglas H. Bartlett8Eric E. Allen9Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USADepartment of Biology, State University of New York at Geneseo, Geneseo, New York, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USADepartment of Biological Sciences, University of Bergen, Bergen, NorwayOceanlab, University of Aberdeen, Institute of Biological and Environmental Sciences, Newburgh, Aberdeenshire, United KingdomMinderoo-UWA Deep-Sea Centre, School of Biological Sciences and Oceans Institute, The University of Western Australia, Perth, AustraliaDepartment of Oceanography, University of Hawaiʻi at Mānoa, Honolulu, Hawaii, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USAABSTRACT Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describe the gut microbiomes of two hadal snailfishes, Pseudoliparis swirei (Mariana Trench) and Notoliparis kermadecensis (Kermadec Trench), using 16S rRNA gene amplicon sequencing. We contextualize these microbiomes with comparisons to the abyssal macrourid Coryphaenoides yaquinae and the continental shelf-dwelling snailfish Careproctus melanurus. The microbial communities of the hadal snailfishes were distinct from their shallower counterparts and were dominated by the same sequences related to the Mycoplasmataceae and Desulfovibrionaceae. These shared taxa indicate that symbiont lineages have remained similar to the ancestral symbiont since their geographic separation or that they are dispersed between geographically distant trenches and subsequently colonize specific hosts. The abyssal and hadal fishes contained sequences related to known, cultured piezophiles, microbes that grow optimally under high hydrostatic pressure, including Psychromonas, Moritella, and Shewanella. These taxa are adept at colonizing nutrient-rich environments present in the deep ocean, such as on particles and in the guts of hosts, and we hypothesize they could make a dietary contribution to deep-sea fishes by degrading chitin and producing fatty acids. We characterize the gut microbiota within some of the deepest fishes to provide new insight into the diversity and distribution of host-associated microbial taxa and the potential of these animals, and the microbes they harbor, for understanding adaptation to deep-sea habitats. IMPORTANCE Hadal trenches, characterized by high hydrostatic pressures and low temperatures, are one of the most extreme environments on our planet. By examining the microbiome of abyssal and hadal fishes, we provide insight into the diversity and distribution of host-associated life at great depth. Our findings show that there are similar microbial populations in fishes geographically separated by thousands of miles, reflecting strong selection for specific microbial lineages. Only a few psychropiezophilic taxa, which do not reflect the diversity of microbial life at great depth, have been successfully isolated in the laboratory. Our examination of deep-sea fish microbiomes shows that typical high-pressure culturing methodologies, which have largely remained unchanged since the pioneering work of Claude ZoBell in the 1950s, may simulate the chemical environment found in animal guts and helps explain why the same deep-sea genera are consistently isolated.https://journals.asm.org/doi/10.1128/msphere.00032-22hadalpiezophilesnailfishtrench |
| spellingShingle | Jessica M. Blanton Logan M. Peoples Mackenzie E. Gerringer Caroline M. Iacuaniello Natalya D. Gallo Thomas D. Linley Alan J. Jamieson Jeffrey C. Drazen Douglas H. Bartlett Eric E. Allen Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles mSphere hadal piezophile snailfish trench |
| title | Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles |
| title_full | Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles |
| title_fullStr | Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles |
| title_full_unstemmed | Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles |
| title_short | Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles |
| title_sort | microbiomes of hadal fishes across trench habitats contain similar taxa and known piezophiles |
| topic | hadal piezophile snailfish trench |
| url | https://journals.asm.org/doi/10.1128/msphere.00032-22 |
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