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

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

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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.
Original languageEnglish
Article number233
Number of pages18
JournalBMC Biology
Volume19
Issue number1
DOIs
Publication statusPublished - 1 Nov 2021

Keywords

  • Shipworm
  • Lyrodus pedicellatus
  • Wood-borers
  • CAZymes
  • Crystalline style
  • Food groove
  • Lignocellulose
  • Bacteria
  • Symbiosis
  • UKRI
  • BBSRC
  • BB/L001926/1
  • EPSRC
  • EP/K039660/1
  • EP/M028127/1

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