TY - JOUR
T1 - Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk
AU - O'Connor, Roberta M.
AU - Fung, Jennifer M.
AU - Sharp, Koty H.
AU - Benner, Jack S.
AU - Mcclung, Colleen
AU - Cushing, Shelley
AU - Lamkin, Elizabeth R.
AU - Fomenkov, Alexey I.
AU - Henrissat, Bernard
AU - Londer, Yuri Y.
AU - Scholz, Matthew B.
AU - Posfai, Janos
AU - Malfatti, Stephanie
AU - Tringe, Susannah G.
AU - Woyke, Tanja
AU - Malmstrom, Rex R.
AU - Coleman-Derr, Devin
AU - Altamia, Marvin A.
AU - Dedrick, Sandra
AU - Kaluziak, Stefan T.
AU - Haygood, Margo G.
AU - Distel, Daniel L.
AU - McFall-Ngai, Margaret J.
PY - 2014/11/25
Y1 - 2014/11/25
N2 - 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.
AB - 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.
KW - Carbohydrate-active enzymes
KW - Endosymbionts
KW - Symbiosis
KW - Teredinidae
KW - Xylotrophy
UR - http://www.scopus.com/inward/record.url?scp=84912035375&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84912035375&partnerID=8YFLogxK
U2 - 10.1073/pnas.1413110111
DO - 10.1073/pnas.1413110111
M3 - Article
C2 - 25385629
AN - SCOPUS:84912035375
SN - 0027-8424
VL - 111
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 47
ER -