Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis
ABSTRACT The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lack...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02243-19 |
| _version_ | 1818932542592516096 |
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| author | Tjorven Hinzke Manuel Kleiner Corinna Breusing Horst Felbeck Robert Häsler Stefan M. Sievert Rabea Schlüter Philip Rosenstiel Thorsten B. H. Reusch Thomas Schweder Stephanie Markert |
| author_facet | Tjorven Hinzke Manuel Kleiner Corinna Breusing Horst Felbeck Robert Häsler Stefan M. Sievert Rabea Schlüter Philip Rosenstiel Thorsten B. H. Reusch Thomas Schweder Stephanie Markert |
| author_sort | Tjorven Hinzke |
| collection | DOAJ |
| description | ABSTRACT The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis. IMPORTANCE All animals are associated with microorganisms; hence, host-microbe interactions are of fundamental importance for life on earth. However, we know little about the molecular basis of these interactions. Therefore, we studied the deep-sea Riftia pachyptila symbiosis, a model association in which the tubeworm host is associated with only one phylotype of endosymbiotic bacteria and completely depends on this sulfur-oxidizing symbiont for nutrition. Using a metaproteomics approach, we identified both metabolic interaction processes, such as substrate transfer between the two partners, and interactions that serve to maintain the symbiotic balance, e.g., host efforts to control the symbiont population or symbiont strategies to modulate these host efforts. We suggest that these interactions are essential principles of mutualistic animal-microbe associations. |
| first_indexed | 2024-12-20T04:34:09Z |
| format | Article |
| id | doaj.art-f7e0263634cf403d81096c1dc7e70015 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-20T04:34:09Z |
| publishDate | 2019-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-f7e0263634cf403d81096c1dc7e700152022-12-21T19:53:18ZengAmerican Society for MicrobiologymBio2150-75112019-12-0110610.1128/mBio.02243-19Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> SymbiosisTjorven Hinzke0Manuel Kleiner1Corinna Breusing2Horst Felbeck3Robert Häsler4Stefan M. Sievert5Rabea Schlüter6Philip Rosenstiel7Thorsten B. H. Reusch8Thomas Schweder9Stephanie Markert10Institute of Marine Biotechnology e.V., Greifswald, GermanyEnergy Bioengineering Group, University of Calgary, Calgary, CanadaMonterey Bay Aquarium Research Institute, Moss Landing, California, USAScripps Institution of Oceanography, University of California San Diego, San Diego, California, USAInstitute of Clinical Molecular Biology (IKMB), Kiel University, Kiel, GermanyBiology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USAImaging Center of the Department of Biology, University of Greifswald, Greifswald, GermanyInstitute of Clinical Molecular Biology (IKMB), Kiel University, Kiel, GermanyMarine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, GermanyInstitute of Marine Biotechnology e.V., Greifswald, GermanyInstitute of Marine Biotechnology e.V., Greifswald, GermanyABSTRACT The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis. IMPORTANCE All animals are associated with microorganisms; hence, host-microbe interactions are of fundamental importance for life on earth. However, we know little about the molecular basis of these interactions. Therefore, we studied the deep-sea Riftia pachyptila symbiosis, a model association in which the tubeworm host is associated with only one phylotype of endosymbiotic bacteria and completely depends on this sulfur-oxidizing symbiont for nutrition. Using a metaproteomics approach, we identified both metabolic interaction processes, such as substrate transfer between the two partners, and interactions that serve to maintain the symbiotic balance, e.g., host efforts to control the symbiont population or symbiont strategies to modulate these host efforts. We suggest that these interactions are essential principles of mutualistic animal-microbe associations.https://journals.asm.org/doi/10.1128/mBio.02243-19host-microbe interactionssymbiosisholobiontchemosynthesishydrothermal ventsmetaproteomics |
| spellingShingle | Tjorven Hinzke Manuel Kleiner Corinna Breusing Horst Felbeck Robert Häsler Stefan M. Sievert Rabea Schlüter Philip Rosenstiel Thorsten B. H. Reusch Thomas Schweder Stephanie Markert Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis mBio host-microbe interactions symbiosis holobiont chemosynthesis hydrothermal vents metaproteomics |
| title | Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis |
| title_full | Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis |
| title_fullStr | Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis |
| title_full_unstemmed | Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis |
| title_short | Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis |
| title_sort | host microbe interactions in the chemosynthetic italic toggle yes riftia pachyptila italic symbiosis |
| topic | host-microbe interactions symbiosis holobiont chemosynthesis hydrothermal vents metaproteomics |
| url | https://journals.asm.org/doi/10.1128/mBio.02243-19 |
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