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...

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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	host-microbe interactions symbiosis holobiont chemosynthesis hydrothermal vents metaproteomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f7e0263634cf403d81096c1dc7e70015
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spelling	oai:doaj.org-article:f7e0263634cf403d81096c1dc7e700152021-11-15T15:54:47ZHost-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis10.1128/mBio.02243-192150-7511https://doaj.org/article/f7e0263634cf403d81096c1dc7e700152019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02243-19https://doaj.org/toc/2150-7511ABSTRACT 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.Tjorven HinzkeManuel KleinerCorinna BreusingHorst FelbeckRobert HäslerStefan M. SievertRabea SchlüterPhilip RosenstielThorsten B. H. ReuschThomas SchwederStephanie MarkertAmerican Society for Microbiologyarticlehost-microbe interactionssymbiosisholobiontchemosynthesishydrothermal ventsmetaproteomicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	host-microbe interactions symbiosis holobiont chemosynthesis hydrothermal vents metaproteomics Microbiology QR1-502
spellingShingle	host-microbe interactions symbiosis holobiont chemosynthesis hydrothermal vents metaproteomics Microbiology QR1-502 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
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.
format	article
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
title	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_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_sort	host-microbe interactions in the chemosynthetic <italic toggle="yes">riftia pachyptila</italic> symbiosis
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/f7e0263634cf403d81096c1dc7e70015
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Host-Microbe Interactions in the Chemosynthetic <italic toggle="yes">Riftia pachyptila</italic> Symbiosis

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