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

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.
Authors:
 [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)
Publication Date:
Grant/Contract Number:
AC02-05CH11231; 1U01TW008163; IOS-0920540; IOS-1442676; IOS-1258090; OCE-0963010; IOS- 1442759
Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 111; Journal Issue: 47; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; teredinidae; endosymbionts; symbiosis; xylotrophy; carbohydrate-active enzymes
OSTI Identifier:
1347687

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 G., and Distel, Daniel L.. Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. United States: N. p., Web. doi: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 G., & Distel, Daniel L.. Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk. United States. doi: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 G., and Distel, Daniel L.. 2014. "Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk". United States. doi:10.1073/pnas.1413110111. https://www.osti.gov/servlets/purl/1347687.
@article{osti_1347687,
title = {Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk},
author = {O’Connor, Roberta M. and Fung, Jennifer M. and Sharp, Koty H. and Benner, Jack S. and McClung, Colleen and Cushing, Shelley and Lamkin, Elizabeth R. and Fomenkov, Alexey I. and Henrissat, Bernard and Londer, Yuri Y. and Scholz, Matthew B. and Posfai, Janos and Malfatti, Stephanie and Tringe, Susannah G. and Woyke, Tanja and Malmstrom, Rex R. and Coleman-Derr, Devin and Altamia, Marvin A. and Dedrick, Sandra and Kaluziak, Stefan T. and Haygood, Margo G. and Distel, Daniel L.},
abstractNote = {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.},
doi = {10.1073/pnas.1413110111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 47,
volume = 111,
place = {United States},
year = {2014},
month = {11}
}