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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [4];  [4];  [5];  [4];  [6];  [4];  [7];  [4];  [8];  [8];  [8];  [8];  [8];  [9];  [10];  [2] more »;  [11];  [2] « less
  1. Tufts Medical Center, Boston, MA (United States)
  2. Northeastern Univ., Nahant, MA (United States)
  3. Eckerd College, St. Petersburg, FL (United States)
  4. New England Biolabs, Ipswich, MA (United States)
  5. Harvard Univ., Boston, MA (United States)
  6. Architecture et Fonction des Macromolecules Biologiques, Marseille Cedex (France)
  7. Michigan State Univ., East Lansing, MI (United States)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. Univ. of the Philippines, Quezon City (Philippines)
  10. Boston College, Chestnut Hill, MA (United States)
  11. Oregon Health & Sciences Univ., Portland, OR (United States)

In animals, gut microbes are essential for digestion. Here in this paper, we show that bacteria outside the gut can also play a critical role in digestion. In shipworms, wood-eating marine bivalves, endosymbiotic bacteria are found within specialized cells in the gills. We show that these endosymbionts produce wood-degrading enzymes that are selectively transported to the shipworm’s bacteria-free gut, where wood digestion occurs. Because only selected wood-degrading enzymes are transported, the shipworm system naturally identifies those endosymbiont enzymes most relevant to lignocellulose deconstruction without interference from other microbial proteins. Furthermore, this work expands the known biological repertoire of bacterial endosymbionts to include digestion of food and identifies previously undescribed enzymes and enzyme combinations of potential value to biomass-based industries, such as cellulosic biofuel production.

Research Organization:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
Grant/Contract Number:
AC02-05CH11231; 1U01TW008163; IOS-0920540; IOS-1442676; IOS-1258090; OCE-0963010; IOS- 1442759
OSTI ID:
1347687
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, Issue 47; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 70 works
Citation information provided by
Web of Science

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Cited By (21)

Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles journal May 2019
Uncovering the molecular mechanisms of lignocellulose digestion in shipworms journal March 2018
Symbiotic Bacteria in Gills and Guts of Chinese Mitten Crab (Eriocheir sinensis) Differ from the Free-Living Bacteria in Water journal January 2016
Discovery, activity and characterisation of an AA10 lytic polysaccharide oxygenase from the shipworm symbiont Teredinibacter turnerae journal September 2019
Simplified and representative bacterial community of maize roots journal March 2017
The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei journal November 2018
It’s what’s inside that counts: computer-aided tomography for evaluating the rate and extent of wood consumption by shipworms journal April 2018
Endoglucanase activity in Neoteredo reynei (Bivalvia, Teredinidae) digestive organs and its content
  • de Moraes Akamine, Daniela Toma; de Almeida Cozendey da Silva, Daniel; de Lima Câmara, Gabriela
  • World Journal of Microbiology and Biotechnology, Vol. 34, Issue 6 https://doi.org/10.1007/s11274-018-2468-x
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Altered Stool Microbiota of Infants with Cystic Fibrosis Shows a Reduction in Genera Associated with Immune Programming from Birth journal August 2019
Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite journal August 2018
Physiological and Molecular Understanding of Bacterial Polysaccharide Monooxygenases journal June 2017
Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications journal October 2019
Structure and function of a glycoside hydrolase family 8 endoxylanase from Teredinibacter turnerae journal October 2018
Plasticity in reproduction and nutrition in wood-boring bivalves (Xylophaga atlantica) from the Mid-Atlantic Ridge journal September 2016
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome journal July 2018
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