Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk
Abstract
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:
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- Tufts Medical Center, Boston, MA (United States)
- Northeastern Univ., Nahant, MA (United States)
- Eckerd College, St. Petersburg, FL (United States)
- New England Biolabs, Ipswich, MA (United States)
- Harvard Univ., Boston, MA (United States)
- Architecture et Fonction des Macromolecules Biologiques, Marseille Cedex (France)
- Michigan State Univ., East Lansing, MI (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Univ. of the Philippines, Quezon City (Philippines)
- Boston College, Chestnut Hill, MA (United States)
- Oregon Health & Sciences Univ., Portland, OR (United States)
- Publication Date:
- 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)
- OSTI Identifier:
- 1347687
- Grant/Contract Number:
- AC02-05CH11231; 1U01TW008163; IOS-0920540; IOS-1442676; IOS-1258090; OCE-0963010; IOS- 1442759
- Resource 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)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; teredinidae; endosymbionts; symbiosis; xylotrophy; carbohydrate-active enzymes
Citation Formats
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., 2014.
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. 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 G., and Distel, Daniel L. Mon .
"Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk". United States. https://doi.org/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 = {Mon Nov 10 00:00:00 EST 2014},
month = {Mon Nov 10 00:00:00 EST 2014}
}
Web of Science
Works referenced in this record:
mathFISH, a Web Tool That Uses Thermodynamics-Based Mathematical Models for In Silico Evaluation of Oligonucleotide Probes for Fluorescence In Situ Hybridization
journal, December 2010
- Yilmaz, L. Safak; Parnerkar, Shreyas; Noguera, Daniel R.
- Applied and Environmental Microbiology, Vol. 77, Issue 3
Comparative Genomic Analysis of the Endosymbionts of Herbivorous Insects Reveals Eco-Environmental Adaptations: Biotechnology Applications
journal, January 2013
- Shi, Weibing; Xie, Shangxian; Chen, Xueyan
- PLoS Genetics, Vol. 9, Issue 1
UCHIME improves sensitivity and speed of chimera detection
journal, June 2011
- Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C.
- Bioinformatics, Vol. 27, Issue 16
The DOE-JGI Standard Operating Procedure for the Annotations of Microbial Genomes
journal, July 2009
- Mavromatis, Konstantinos; Ivanova, Natalia N.; Chen, I-Min A.
- Standards in Genomic Sciences, Vol. 1, Issue 1
Addressing Shewanella oneidensis “cytochromome”: The first step towards high-throughput expression of cytochromes c
journal, November 2008
- Londer, Yuri Y.; Giuliani, Sarah E.; Peppler, Terese
- Protein Expression and Purification, Vol. 62, Issue 1
Novel enzymes for the degradation of cellulose
journal, January 2012
- Horn, Svein; Vaaje-Kolstad, Gustav; Westereng, Bjørge
- Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 45
Clustal W and Clustal X version 2.0
journal, September 2007
- Larkin, M. A.; Blackshields, G.; Brown, N. P.
- Bioinformatics, Vol. 23, Issue 21, p. 2947-2948
GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense
journal, June 2014
- Chaudhary, R.; Atamian, H. S.; Shen, Z.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 24
Proteomic Investigation of Aphid Honeydew Reveals an Unexpected Diversity of Proteins
journal, September 2013
- Sabri, Ahmed; Vandermoten, Sophie; Leroy, Pascal D.
- PLoS ONE, Vol. 8, Issue 9
Real-Time DNA Sequencing from Single Polymerase Molecules
journal, January 2009
- Eid, John; Fehr, Adrian; Gray, Jeremy
- Science, Vol. 323, Issue 5910, p. 133-138
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013
- Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
- Nature Methods, Vol. 10, Issue 6
Physiological aspects of wood consumption, growth, and reproduction in the shipworm Lyrodus pedicellatus Quatrefages (Bivalvia:Teredinidae)
journal, May 1981
- Gallager, Scott M.; Turner, Ruth D.; Berg, Carl J.
- Journal of Experimental Marine Biology and Ecology, Vol. 52, Issue 1
Bacterial associations in the teredo Bankia australis (Lamellibranchia: Mollusca)
journal, April 1973
- Popham, J. D.; Dickson, M. R.
- Marine Biology, Vol. 19, Issue 4
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Coexistence of Multiple Proteobacterial Endosymbionts in the Gills of the Wood-Boring Bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae)
journal, December 2002
- Distel, D. L.; Beaudoin, D. J.; Morrill, W.
- Applied and Environmental Microbiology, Vol. 68, Issue 12
Microbial Distribution and Abundance in the Digestive System of Five Shipworm Species (Bivalvia: Teredinidae)
journal, September 2012
- Betcher, Meghan A.; Fung, Jennifer M.; Han, Andrew W.
- PLoS ONE, Vol. 7, Issue 9
Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane—Distinct translocases and mechanisms
journal, September 2008
- Natale, Paolo; Brüser, Thomas; Driessen, Arnold J. M.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Species identification, phylogenetic analysis and detection of herbicide-resistant biotypes of Amaranthus based on ALS and ITS
journal, July 2020
- Xu, Han; Pan, Xubin; Wang, Cong
- Scientific Reports, Vol. 10, Issue 1
Synergy between 13C-metabolic flux analysis and flux balance analysis for understanding metabolic adaption to anaerobiosis in E. coli
journal, January 2011
- Chen, Xuewen; Alonso, Ana P.; Allen, Doug K.
- Metabolic Engineering, Vol. 13, Issue 1
Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake
journal, March 2020
- Liu, Yang; Ren, Ze; Qu, Xiaodong
- Scientific Reports, Vol. 10, Issue 1
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Extensive Variation in Intracellular Symbiont Community Composition among Members of a Single Population of the Wood-Boring Bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae)
journal, January 2006
- Luyten, Y. A.; Thompson, J. R.; Morrill, W.
- Applied and Environmental Microbiology, Vol. 72, Issue 1
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates
journal, January 2010
- Kunin, Victor; Engelbrektson, Anna; Ochman, Howard
- Environmental Microbiology, Vol. 12, Issue 1
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5)
text, January 2012
- Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang
- BioMed Central
Phylogenetic Analysis of Microbial Communities in Different Regions of the Gastrointestinal Tract in Panaque nigrolineatus, a Wood-Eating Fish
journal, October 2012
- McDonald, Ryan; Schreier, Harold J.; Watts, Joy E. M.
- PLoS ONE, Vol. 7, Issue 10
New enzyme insights drive advances in commercial ethanol production
journal, April 2014
- Harris, Paul V.; Xu, Feng; Kreel, Nathaniel E.
- Current Opinion in Chemical Biology, Vol. 19
Metagenomic Profiling Reveals Lignocellulose Degrading System in a Microbial Community Associated with a Wood-Feeding Beetle
journal, September 2013
- Scully, Erin D.; Geib, Scott M.; Hoover, Kelli
- PLoS ONE, Vol. 8, Issue 9
A flexible and efficient template format for circular consensus sequencing and SNP detection
journal, June 2010
- Travers, K. J.; Chin, C. -S.; Rank, D. R.
- Nucleic Acids Research, Vol. 38, Issue 15
A Cellulolytic Nitrogen-Fixing Bacterium Cultured from the Gland of Deshayes in Shipworms (Bivalvia: Teredinidae)
journal, September 1983
- Waterbury, J. B.; Calloway, C. B.; Turner, R. D.
- Science, Vol. 221, Issue 4618
MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001
- Huelsenbeck, J. P.; Ronquist, F.
- Bioinformatics, Vol. 17, Issue 8
Symbiotic digestion of lignocellulose in termite guts
journal, February 2014
- Brune, Andreas
- Nature Reviews Microbiology, Vol. 12, Issue 3
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Physical and computational analysis of the yeast Kluyveromyces lactis secreted proteome
journal, July 2008
- Swaim, Catherine L.; Anton, Brian P.; Sharma, Shamik S.
- PROTEOMICS, Vol. 8, Issue 13
Insights into Plant Cell Wall Degradation from the Genome Sequence of the Soil Bacterium Cellvibrio japonicus
journal, June 2008
- DeBoy, R. T.; Mongodin, E. F.; Fouts, D. E.
- Journal of Bacteriology, Vol. 190, Issue 15, p. 5455-5463
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Metagenomic Analysis of the Microbiota from the Crop of an Invasive Snail Reveals a Rich Reservoir of Novel Genes
journal, November 2012
- Cardoso, Alexander M.; Cavalcante, Janaína J. V.; Cantão, Maurício E.
- PLoS ONE, Vol. 7, Issue 11
Complete Genome Sequence of the Complex Carbohydrate-Degrading Marine Bacterium, Saccharophagus degradans Strain 2-40T
journal, May 2008
- Weiner, Ronald M.; Taylor, Larry E.; Henrissat, Bernard
- PLoS Genetics, Vol. 4, Issue 5
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia)
book, January 1966
- Turner, Ruth Dixon
- Cambridge, Museum of Comparative Zoology,
The Complete Genome of Teredinibacter turnerae T7901: An Intracellular Endosymbiont of Marine Wood-Boring Bivalves (Shipworms)
journal, July 2009
- Yang, Joyce C.; Madupu, Ramana; Durkin, A. Scott
- PLoS ONE, Vol. 4, Issue 7
The COG database: new developments in phylogenetic classification of proteins from complete genomes
journal, January 2001
- Tatusov, R. L.
- Nucleic Acids Research, Vol. 29, Issue 1
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5)
journal, January 2012
- Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang
- BMC Evolutionary Biology, Vol. 12, Issue 1
Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing
journal, December 2011
- Clark, Tyson A.; Murray, Iain A.; Morgan, Richard D.
- Nucleic Acids Research, Vol. 40, Issue 4
Quantitative Imaging of Nitrogen Fixation by Individual Bacteria Within Animal Cells
journal, September 2007
- Lechene, C. P.; Luyten, Y.; McMahon, G.
- Science, Vol. 317, Issue 5844
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011
- Hess, M.; Sczyrba, A.; Egan, R.
- Science, Vol. 331, Issue 6016
Genetic differentiation among isolates of Teredinibacter turnerae, a widely occurring intracellular endosymbiont of shipworms
journal, March 2014
- Altamia, Marvin A.; Wood, Nicole; Fung, Jennifer M.
- Molecular Ecology, Vol. 23, Issue 6
Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys
journal, June 2011
- Werner, Jeffrey J.; Koren, Omry; Hugenholtz, Philip
- The ISME Journal, Vol. 6, Issue 1
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons
journal, January 2011
- Haas, B. J.; Gevers, D.; Earl, A. M.
- Genome Research, Vol. 21, Issue 3
Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae)
journal, November 2002
- Distel, D. L.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 52, Issue 6
jModelTest 2: more models, new heuristics and parallel computing
journal, July 2012
- Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón
- Nature Methods, Vol. 9, Issue 8
Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by using 16S rRNA sequence analysis and oligodeoxynucleotide probe hybridization.
journal, January 1991
- Distel, D. L.; DeLong, E. F.; Waterbury, J. B.
- Applied and Environmental Microbiology, Vol. 57, Issue 8
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations.
journal, January 1990
- Amann, R. I.; Binder, B. J.; Olson, R. J.
- Applied and Environmental Microbiology, Vol. 56, Issue 6
A Photometric Adaptation of the Somogyi Method for the Determination of Glucose
journal, May 1944
- Nelson, Norton
- Journal of Biological Chemistry, Vol. 153, Issue 2
Works referencing / citing this record:
Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles
journal, May 2019
- Busch, André; Danchin, Etienne G. J.; Pauchet, Yannick
- BMC Evolutionary Biology, Vol. 19, Issue 1
Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
journal, March 2018
- Sabbadin, Federico; Pesante, Giovanna; Elias, Luisa
- Biotechnology for Biofuels, Vol. 11, Issue 1
Symbiotic Bacteria in Gills and Guts of Chinese Mitten Crab (Eriocheir sinensis) Differ from the Free-Living Bacteria in Water
journal, January 2016
- Zhang, Meiling; Sun, Yuhong; Chen, Liqiao
- PLOS ONE, Vol. 11, Issue 1
Discovery, activity and characterisation of an AA10 lytic polysaccharide oxygenase from the shipworm symbiont Teredinibacter turnerae
journal, September 2019
- Fowler, Claire. A.; Sabbadin, Federico; Ciano, Luisa
- Biotechnology for Biofuels, Vol. 12, Issue 1
Simplified and representative bacterial community of maize roots
journal, March 2017
- Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
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
- Brito, Thais L.; Campos, Amanda B.; Bastiaan von Meijenfeldt, F. A.
- PLOS ONE, Vol. 13, Issue 11
It’s what’s inside that counts: computer-aided tomography for evaluating the rate and extent of wood consumption by shipworms
journal, April 2018
- Charles, François; Coston-Guarini, Jennifer; Guarini, Jean-Marc
- Journal of Wood Science, Vol. 64, Issue 4
Endoglucanase activity in Neoteredo reynei (Bivalvia, Teredinidae) digestive organs and its content
journal, June 2018
- 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
Altered Stool Microbiota of Infants with Cystic Fibrosis Shows a Reduction in Genera Associated with Immune Programming from Birth
journal, August 2019
- Antosca, Katherine M.; Chernikova, Diana A.; Price, Courtney E.
- Journal of Bacteriology, Vol. 201, Issue 16
Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite
journal, August 2018
- Liu, Ning; Li, Hongjie; Chevrette, Marc G.
- The ISME Journal, Vol. 13, Issue 1
Physiological and Molecular Understanding of Bacterial Polysaccharide Monooxygenases
journal, June 2017
- Agostoni, Marco; Hangasky, John A.; Marletta, Michael A.
- Microbiology and Molecular Biology Reviews, Vol. 81, Issue 3
Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications
journal, October 2019
- Shipway, J. Reuben; Rosenberg, Gary; Concepcion, Gisela P.
- PLOS ONE, Vol. 14, Issue 10
Structure and function of a glycoside hydrolase family 8 endoxylanase from Teredinibacter turnerae
journal, October 2018
- Fowler, Claire A.; Hemsworth, Glyn R.; Cuskin, Fiona
- Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10
Plasticity in reproduction and nutrition in wood-boring bivalves (Xylophaga atlantica) from the Mid-Atlantic Ridge
journal, September 2016
- Gaudron, Sylvie Marylène; Haga, T.; Wang, H.
- Marine Biology, Vol. 163, Issue 10
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome
journal, July 2018
- Armstrong, Zachary; Mewis, Keith; Liu, Feng
- The ISME Journal, Vol. 12, Issue 11
Ralstonia solanacearum lipopeptide induces chlamydospore development in fungi and facilitates bacterial entry into fungal tissues
journal, March 2016
- Spraker, Joseph E.; Sanchez, Laura M.; Lowe, Tiffany M.
- The ISME Journal, Vol. 10, Issue 9
Lignocellulosic bioma ss : Biosynthesis, degradation, and industrial utilization
journal, October 2015
- Guerriero, Gea; Hausman, Jean-Francois; Strauss, Joseph
- Engineering in Life Sciences, Vol. 16, Issue 1
Parallel lives of symbionts and hosts: chemical mutualism in marine animals
journal, January 2018
- Morita, Maho; Schmidt, Eric W.
- Natural Product Reports, Vol. 35, Issue 4
Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius
journal, March 2019
- Altamia, Marvin A.; Shipway, J. Reuben; Concepcion, Gisela P.
- International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 3
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome
journal, July 2018
- Armstrong, Zachary; Mewis, Keith; Liu, Feng
- The ISME Journal, Vol. 12, Issue 11
Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite
journal, August 2018
- Liu, Ning; Li, Hongjie; Chevrette, Marc G.
- The ISME Journal, Vol. 13, Issue 1
Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles
journal, May 2019
- Busch, André; Danchin, Etienne G. J.; Pauchet, Yannick
- BMC Evolutionary Biology, Vol. 19, Issue 1
Symbiotic Bacteria in Gills and Guts of Chinese Mitten Crab (Eriocheir sinensis) Differ from the Free-Living Bacteria in Water
journal, January 2016
- Zhang, Meiling; Sun, Yuhong; Chen, Liqiao
- PLOS ONE, Vol. 11, Issue 1
Bacteriome-localized intracellular symbionts in pollen-feeding beetles of the genus dasytes (Coleoptera, Dasytidae)
text, January 2016
- Weiss, Benjamin; Kaltenpoth, Martin
- Frontiers Media
Comparative Metagenomics of Cellulose- and Poplar Hydrolysate-Degrading Microcosms from Gut Microflora of the Canadian Beaver (Castor canadensis) and North American Moose (Alces americanus) after Long-Term Enrichment
journal, December 2017
- Wong, Mabel T.; Wang, Weijun; Couturier, Marie
- Frontiers in Microbiology, Vol. 8