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

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cam.issuedOnline2021-11
dc.contributor.authorPesante, Giovanna
dc.contributor.authorSabbadin, Federico
dc.contributor.authorElias, Luisa
dc.contributor.authorSteele-King, Clare
dc.contributor.authorShipway, J Reuben
dc.contributor.authorDowle, Adam A
dc.contributor.authorLi, Yi
dc.contributor.authorBusse-Wicher, Marta
dc.contributor.authorDupree, Paul
dc.contributor.authorBesser, Katrin
dc.contributor.authorCragg, Simon M
dc.contributor.authorBruce, Neil C
dc.contributor.authorMcQueen-Mason, Simon J
dc.contributor.orcidMcQueen-Mason, Simon J [0000-0002-6781-4768]
dc.date.accessioned2022-01-06T12:56:46Z
dc.date.available2022-01-06T12:56:46Z
dc.date.issued2021-11-01
dc.date.updated2022-01-06T12:56:45Z
dc.description.abstractBACKGROUND: 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.
dc.identifier.doi10.17863/CAM.79672
dc.identifier.eissn1741-7007
dc.identifier.issn1741-7007
dc.identifier.otherPMC8561940
dc.identifier.other34724941
dc.identifier.urihttps://www.repository.cam.ac.uk/handle/1810/332226
dc.languageeng
dc.language.isoeng
dc.publisherSpringer Science and Business Media LLC
dc.publisher.urlhttp://dx.doi.org/10.1186/s12915-021-01162-6
dc.rightsAttribution 4.0 International
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.sourceessn: 1741-7007
dc.sourcenlmid: 101190720
dc.subjectBacteria
dc.subjectCAZymes
dc.subjectCrystalline style
dc.subjectFood groove
dc.subjectLignocellulose
dc.subjectLyrodus pedicellatus
dc.subjectShipworm
dc.subjectSymbiosis
dc.subjectWood-borers
dc.subjectAnimals
dc.subjectBacteria
dc.subjectBivalvia
dc.subjectPhylogeny
dc.subjectProteomics
dc.subjectSymbiosis
dc.titleCharacterisation of the enzyme transport path between shipworms and their bacterial symbionts.
dc.typeArticle
dcterms.dateAccepted2021-10-04
prism.issueIdentifier1
prism.publicationNameBMC Biol
prism.volume19
pubs.funder-project-idBiotechnology and Biological Sciences Research Council (BB/L001926/1)
pubs.funder-project-idBBSRC (via University of York) (R15011 BB/L001926/1)
rioxxterms.licenseref.urihttps://creativecommons.org/licenses/by/4.0/
rioxxterms.versionVoR
rioxxterms.versionofrecord10.1186/s12915-021-01162-6

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