Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

Abstract Background Shipworms are marine xylophagus bivalve molluscs, which can live on a diet solely of wood due to their ability to produce plant cell wall-degrading enzymes. Bacterial carbohydrate-active enzymes (CAZymes), synthesised by endosymbionts living in specialised shipworm cells called b...

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Autores principales:	Giovanna Pesante, Federico Sabbadin, Luisa Elias, Clare Steele-King, J. Reuben Shipway, Adam A. Dowle, Yi Li, Marta Busse-Wicher, Paul Dupree, Katrin Besser, Simon M. Cragg, Neil C. Bruce, Simon J. McQueen-Mason
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Shipworm Lyrodus pedicellatus Wood-borers CAZymes Crystalline style Food groove Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/8881d93befe64ac688da489f9383e1e5
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spelling	oai:doaj.org-article:8881d93befe64ac688da489f9383e1e52021-11-08T11:17:39ZCharacterisation of the enzyme transport path between shipworms and their bacterial symbionts10.1186/s12915-021-01162-61741-7007https://doaj.org/article/8881d93befe64ac688da489f9383e1e52021-11-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01162-6https://doaj.org/toc/1741-7007Abstract Background Shipworms are marine xylophagus bivalve molluscs, which can live on a diet solely of wood due to their ability to produce plant cell wall-degrading enzymes. Bacterial carbohydrate-active enzymes (CAZymes), synthesised by endosymbionts living in specialised shipworm cells called bacteriocytes and located in the animal’s gills, play an important role in wood digestion in shipworms. However, the main site of lignocellulose digestion within these wood-boring molluscs, which contains both endogenous lignocellulolytic enzymes and prokaryotic enzymes, is the caecum, and the mechanism by which bacterial enzymes reach the distant caecum lumen has remained so far mysterious. Here, we provide a characterisation of the path through which bacterial CAZymes produced in the gills of the shipworm Lyrodus pedicellatus reach the distant caecum to contribute to the digestion of wood. Results Through a combination of transcriptomics, proteomics, X-ray microtomography, electron microscopy studies and in vitro biochemical characterisation, we show that wood-digesting enzymes produced by symbiotic bacteria are localised not only in the gills, but also in the lumen of the food groove, a stream of mucus secreted by gill cells that carries food particles trapped by filter feeding to the mouth. Bacterial CAZymes are also present in the crystalline style and in the caecum of their shipworm host, suggesting a unique pathway by which enzymes involved in a symbiotic interaction are transported to their site of action. Finally, we characterise in vitro four new bacterial glycosyl hydrolases and a lytic polysaccharide monooxygenase identified in our transcriptomic and proteomic analyses as some of the major bacterial enzymes involved in this unusual biological system. Conclusion Based on our data, we propose that bacteria and their enzymes are transported from the gills along the food groove to the shipworm’s mouth and digestive tract, where they aid in wood digestion.Giovanna PesanteFederico SabbadinLuisa EliasClare Steele-KingJ. Reuben ShipwayAdam A. DowleYi LiMarta Busse-WicherPaul DupreeKatrin BesserSimon M. CraggNeil C. BruceSimon J. McQueen-MasonBMCarticleShipwormLyrodus pedicellatusWood-borersCAZymesCrystalline styleFood grooveBiology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-18 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Shipworm Lyrodus pedicellatus Wood-borers CAZymes Crystalline style Food groove Biology (General) QH301-705.5
spellingShingle	Shipworm Lyrodus pedicellatus Wood-borers CAZymes Crystalline style Food groove Biology (General) QH301-705.5 Giovanna Pesante Federico Sabbadin Luisa Elias Clare Steele-King J. Reuben Shipway Adam A. Dowle Yi Li Marta Busse-Wicher Paul Dupree Katrin Besser Simon M. Cragg Neil C. Bruce Simon J. McQueen-Mason Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
description	Abstract Background Shipworms are marine xylophagus bivalve molluscs, which can live on a diet solely of wood due to their ability to produce plant cell wall-degrading enzymes. Bacterial carbohydrate-active enzymes (CAZymes), synthesised by endosymbionts living in specialised shipworm cells called bacteriocytes and located in the animal’s gills, play an important role in wood digestion in shipworms. However, the main site of lignocellulose digestion within these wood-boring molluscs, which contains both endogenous lignocellulolytic enzymes and prokaryotic enzymes, is the caecum, and the mechanism by which bacterial enzymes reach the distant caecum lumen has remained so far mysterious. Here, we provide a characterisation of the path through which bacterial CAZymes produced in the gills of the shipworm Lyrodus pedicellatus reach the distant caecum to contribute to the digestion of wood. Results Through a combination of transcriptomics, proteomics, X-ray microtomography, electron microscopy studies and in vitro biochemical characterisation, we show that wood-digesting enzymes produced by symbiotic bacteria are localised not only in the gills, but also in the lumen of the food groove, a stream of mucus secreted by gill cells that carries food particles trapped by filter feeding to the mouth. Bacterial CAZymes are also present in the crystalline style and in the caecum of their shipworm host, suggesting a unique pathway by which enzymes involved in a symbiotic interaction are transported to their site of action. Finally, we characterise in vitro four new bacterial glycosyl hydrolases and a lytic polysaccharide monooxygenase identified in our transcriptomic and proteomic analyses as some of the major bacterial enzymes involved in this unusual biological system. Conclusion Based on our data, we propose that bacteria and their enzymes are transported from the gills along the food groove to the shipworm’s mouth and digestive tract, where they aid in wood digestion.
format	article
author	Giovanna Pesante Federico Sabbadin Luisa Elias Clare Steele-King J. Reuben Shipway Adam A. Dowle Yi Li Marta Busse-Wicher Paul Dupree Katrin Besser Simon M. Cragg Neil C. Bruce Simon J. McQueen-Mason
author_facet	Giovanna Pesante Federico Sabbadin Luisa Elias Clare Steele-King J. Reuben Shipway Adam A. Dowle Yi Li Marta Busse-Wicher Paul Dupree Katrin Besser Simon M. Cragg Neil C. Bruce Simon J. McQueen-Mason
author_sort	Giovanna Pesante
title	Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
title_short	Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
title_full	Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
title_fullStr	Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
title_full_unstemmed	Characterisation of the enzyme transport path between shipworms and their bacterial symbionts
title_sort	characterisation of the enzyme transport path between shipworms and their bacterial symbionts
publisher	BMC
publishDate	2021
url	https://doaj.org/article/8881d93befe64ac688da489f9383e1e5
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Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

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