Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

Roberta M. O'Connor, Jennifer M. Fung, Koty H. Sharp, Jack S. Benner, Colleen Mcclung, Shelley Cushing, Elizabeth R. Lamkin, Alexey I. Fomenkov, Bernard Henrissat, Yuri Y. Londer, Matthew B. Scholz, Janos Posfai, Stephanie Malfatti, Susannah G. Tringe, Tanja Woyke, Rex R. Malmstrom, Devin Coleman-Derr, Marvin A. Altamia, Sandra Dedrick, Stefan T. Kaluziak & 3 others Margo Haygood, Daniel L. Distel, Margaret J. McFall-Ngai

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Bacteria play many important roles in animal digestive systems, including the provision of enzymes critical to digestion. Typically, complex communities of bacteria reside in the gut lumen in direct contact with the ingested materials they help to digest. Here, we demonstrate a previously undescribed digestive strategy in the wood-eating marine bivalve Bankia setacea, wherein digestive bacteria are housed in a location remote from the gut. These bivalves, commonly known as shipworms, lack a resident microbiota in the gut compartment where wood is digested but harbor endosymbiotic bacteria within specialized cells in their gills. We show that this comparatively simple bacterial community produces wood-degrading enzymes that are selectively translocated from gill to gut. These enzymes, which include just a small subset of the predicted wood-degrading enzymes encoded in the endosymbiont genomes, accumulate in the gut to the near exclusion of other endosymbiont-made proteins. This strategy of remote enzyme production provides the shipworm with a mechanism to capture liberated sugars from wood without competition from an endogenous gut microbiota. Because only those proteins required forwood digestion are translocated to the gut, this newly described system reveals which of many possible enzymes and enzyme combinations are minimally required for wood degradation. Thus, although it has historically had negative impacts on human welfare, the shipworm digestive process now has the potential to have a positive impact on industries that convert wood and other plant biomass to renewable fuels, fine chemicals, food, feeds, textiles, and paper products.

Original languageEnglish (US)
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number47
DOIs
StatePublished - Nov 25 2014

Fingerprint

Mollusca
Bacteria
Enzymes
Bivalvia
Digestion
Digestive System
Textiles
Biomass
Industry
Proteins
Eating
Genome
Food

Keywords

  • Carbohydrate-active enzymes
  • Endosymbionts
  • Symbiosis
  • Teredinidae
  • Xylotrophy

ASJC Scopus subject areas

  • General

Cite this

O'Connor, R. M., Fung, J. M., Sharp, K. H., Benner, J. S., Mcclung, C., Cushing, S., ... McFall-Ngai, M. J. (2014). Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. Proceedings of the National Academy of Sciences of the United States of America, 111(47). https://doi.org/10.1073/pnas.1413110111

Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. / O'Connor, Roberta M.; Fung, Jennifer M.; Sharp, Koty H.; Benner, Jack S.; Mcclung, Colleen; Cushing, Shelley; Lamkin, Elizabeth R.; Fomenkov, Alexey I.; Henrissat, Bernard; Londer, Yuri Y.; Scholz, Matthew B.; Posfai, Janos; Malfatti, Stephanie; Tringe, Susannah G.; Woyke, Tanja; Malmstrom, Rex R.; Coleman-Derr, Devin; Altamia, Marvin A.; Dedrick, Sandra; Kaluziak, Stefan T.; Haygood, Margo; Distel, Daniel L.; McFall-Ngai, Margaret J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 47, 25.11.2014.

Research output: Contribution to journalArticle

O'Connor, RM, Fung, JM, Sharp, KH, Benner, JS, Mcclung, C, Cushing, S, Lamkin, ER, Fomenkov, AI, Henrissat, B, Londer, YY, Scholz, MB, Posfai, J, Malfatti, S, Tringe, SG, Woyke, T, Malmstrom, RR, Coleman-Derr, D, Altamia, MA, Dedrick, S, Kaluziak, ST, Haygood, M, Distel, DL & McFall-Ngai, MJ 2014, 'Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 47. https://doi.org/10.1073/pnas.1413110111
O'Connor, Roberta M. ; Fung, Jennifer M. ; Sharp, Koty H. ; Benner, Jack S. ; Mcclung, Colleen ; Cushing, Shelley ; Lamkin, Elizabeth R. ; Fomenkov, Alexey I. ; Henrissat, Bernard ; Londer, Yuri Y. ; Scholz, Matthew B. ; Posfai, Janos ; Malfatti, Stephanie ; Tringe, Susannah G. ; Woyke, Tanja ; Malmstrom, Rex R. ; Coleman-Derr, Devin ; Altamia, Marvin A. ; Dedrick, Sandra ; Kaluziak, Stefan T. ; Haygood, Margo ; Distel, Daniel L. ; McFall-Ngai, Margaret J. / Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 47.
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