Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk.
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 for wood 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.
Tufts Medical Center, Boston, MA 02111;
Roberta M
RM
O'Connor
Ocean Genome Legacy Center of New England Biolabs, Marine Sciences Center, Northeastern University, Nahant, MA 01908;
Jennifer M
JM
Fung
James Center for Molecular and Life Sciences, Eckerd College, St. Petersburg, FL 33711;
Koty H
KH
Sharp
New England Biolabs, Ipswich, MA 01938;
Jack S
JS
Benner
New England Biolabs, Ipswich, MA 01938;
Colleen
C
McClung
New England Biolabs, Ipswich, MA 01938;
Shelley
S
Cushing
Harvard University, Boston, MA 02115;
Elizabeth R
ER
Lamkin
New England Biolabs, Ipswich, MA 01938;
Alexey I
AI
Fomenkov
Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique, Unité Mixte de Recherches 7257, Case 932, Campus de Luminy, 13288 Marseille Cedex 09, France;
Bernard
B
Henrissat
New England Biolabs, Ipswich, MA 01938;
Yuri Y
YY
Londer
Institute for Cyber Enabled Research, Michigan State University, East Lansing, MI 48824-1226;
Matthew B
MB
Scholz
New England Biolabs, Ipswich, MA 01938;
Janos
J
Posfai
Joint Genome Institute, Department of Energy, Walnut Creek, CA 94598;
Stephanie
S
Malfatti
Joint Genome Institute, Department of Energy, Walnut Creek, CA 94598;
Susannah G
SG
Tringe
Joint Genome Institute, Department of Energy, Walnut Creek, CA 94598;
Tanja
T
Woyke
Joint Genome Institute, Department of Energy, Walnut Creek, CA 94598;
Rex R
RR
Malmstrom
Joint Genome Institute, Department of Energy, Walnut Creek, CA 94598;
Devin
D
Coleman-Derr
Marine Sciences Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines;
Marvin A
MA
Altamia
Boston College, Chestnut Hill, MA 02467; and.
Sandra
S
Dedrick
Ocean Genome Legacy Center of New England Biolabs, Marine Sciences Center, Northeastern University, Nahant, MA 01908;
Stefan T
ST
Kaluziak
Institute of Environmental Health, Oregon Health & Sciences University, Portland, OR 97239-3098.
Margo G
MG
Haygood
Ocean Genome Legacy Center of New England Biolabs, Marine Sciences Center, Northeastern University, Nahant, MA 01908; d.distel@neu.edu.
Daniel L
DL
Distel
D000818:Animals; D001419:Bacteria / Q000145:classification*; D004063:Digestion; D005247:Feeding Behavior; D005880:Gills / Q000382:microbiology*; D054892:Metagenome; D008969:Molecular Sequence Data; D008974:Mollusca / Q000378:metabolism*; D010802:Phylogeny; D014934:Wood
Teredinidae; carbohydrate-active enzymes; endosymbionts; symbiosis; xylotrophy