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Title: A bacterial pioneer produces cellulase complexes that persist through community succession

Abstract

Cultivation of microbial consortia provides low-complexity communities that can serve as tractable models to understand community dynamics. Time-resolved metagenomics demonstrated that an aerobic cellulolytic consortium cultivated from compost exhibited community dynamics consistent with the definition of an endogenous heterotrophic succession. The genome of the proposed pioneer population, 'Candidatus Reconcilibacillus cellulovorans', possessed a gene cluster containing multidomain glycoside hydrolases (GHs). Purification of the soluble cellulase activity from a 300litre cultivation of this consortium revealed that ~70% of the activity arose from the 'Ca. Reconcilibacillus cellulovorans' multidomain GHs assembled into cellulase complexes through glycosylation. These remarkably stable complexes have supramolecular structures for enzymatic cellulose hydrolysis that are distinct from cellulosomes. The persistence of these complexes during cultivation indicates that they may be active through multiple cultivations of this consortium and act as public goods that sustain the community. Thus, the provision of extracellular GHs as public goods may influence microbial community dynamics in native biomass-deconstructing communities relevant to agriculture, human health and biotechnology.

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [6];  [4];  [7];  [8]; ORCiD logo [9];  [10];  [10];  [11];  [3];  [3]; ORCiD logo [7];  [12];  [7]; ORCiD logo [7]
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of Basel (Switzerland). Dept. of Chemistry
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Taipei Medical Univ. (Taiwan). Graduate Inst. of Biomedical Informatics and College of Medical Science and Technology
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division and Advanced Biofuels Process Development Unit
  4. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Mannheim Univ. of Applied Sciences (Germany). Faculty of Biotechnology
  5. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of Vienna (Austria). Division of Microbial Ecology, Dept. of Microbiology and Ecosystem Science and Research network “Chemistry meets Microbiology”
  6. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Braunschweig Univ. of Technology (Germany). Inst. of Genetics
  7. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
  8. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Corning Inc., Corning, NY (United States)
  9. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Mannheim Univ. of Applied Sciences (Germany). Faculty of Biotechnology
  10. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  11. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  12. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States). Biological and Materials Science Center
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (EE-3B); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; German Research Foundation (DFG); National Institutes of Health (NIH)
OSTI Identifier:
1436168
Grant/Contract Number:  
AC02-05CH11231; KO 5295/1-1; SC0015662; 1S10OD018530; P41GM10349010
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; 09 BIOMASS FUELS; Bacterial genomics; Environmental microbiology; Metagenomics

Citation Formats

Kolinko, Sebastian, Wu, Yu-Wei, Tachea, Firehiwot, Denzel, Evelyn, Hiras, Jennifer, Gabriel, Raphael, Backer, Nora, Chan, Leanne Jade G., Eichorst, Stephanie A., Frey, Dario, Chen, Qiushi, Azadi, Parastoo, Adams, Paul D., Pray, Todd R., Tanjore, Deepti, Petzold, Christopher J., Gladden, John M., Simmons, Blake A., and Singer, Steven W. A bacterial pioneer produces cellulase complexes that persist through community succession. United States: N. p., 2017. Web. doi:10.1038/s41564-017-0052-z.
Kolinko, Sebastian, Wu, Yu-Wei, Tachea, Firehiwot, Denzel, Evelyn, Hiras, Jennifer, Gabriel, Raphael, Backer, Nora, Chan, Leanne Jade G., Eichorst, Stephanie A., Frey, Dario, Chen, Qiushi, Azadi, Parastoo, Adams, Paul D., Pray, Todd R., Tanjore, Deepti, Petzold, Christopher J., Gladden, John M., Simmons, Blake A., & Singer, Steven W. A bacterial pioneer produces cellulase complexes that persist through community succession. United States. doi:10.1038/s41564-017-0052-z.
Kolinko, Sebastian, Wu, Yu-Wei, Tachea, Firehiwot, Denzel, Evelyn, Hiras, Jennifer, Gabriel, Raphael, Backer, Nora, Chan, Leanne Jade G., Eichorst, Stephanie A., Frey, Dario, Chen, Qiushi, Azadi, Parastoo, Adams, Paul D., Pray, Todd R., Tanjore, Deepti, Petzold, Christopher J., Gladden, John M., Simmons, Blake A., and Singer, Steven W. Mon . "A bacterial pioneer produces cellulase complexes that persist through community succession". United States. doi:10.1038/s41564-017-0052-z. https://www.osti.gov/servlets/purl/1436168.
@article{osti_1436168,
title = {A bacterial pioneer produces cellulase complexes that persist through community succession},
author = {Kolinko, Sebastian and Wu, Yu-Wei and Tachea, Firehiwot and Denzel, Evelyn and Hiras, Jennifer and Gabriel, Raphael and Backer, Nora and Chan, Leanne Jade G. and Eichorst, Stephanie A. and Frey, Dario and Chen, Qiushi and Azadi, Parastoo and Adams, Paul D. and Pray, Todd R. and Tanjore, Deepti and Petzold, Christopher J. and Gladden, John M. and Simmons, Blake A. and Singer, Steven W.},
abstractNote = {Cultivation of microbial consortia provides low-complexity communities that can serve as tractable models to understand community dynamics. Time-resolved metagenomics demonstrated that an aerobic cellulolytic consortium cultivated from compost exhibited community dynamics consistent with the definition of an endogenous heterotrophic succession. The genome of the proposed pioneer population, 'Candidatus Reconcilibacillus cellulovorans', possessed a gene cluster containing multidomain glycoside hydrolases (GHs). Purification of the soluble cellulase activity from a 300litre cultivation of this consortium revealed that ~70% of the activity arose from the 'Ca. Reconcilibacillus cellulovorans' multidomain GHs assembled into cellulase complexes through glycosylation. These remarkably stable complexes have supramolecular structures for enzymatic cellulose hydrolysis that are distinct from cellulosomes. The persistence of these complexes during cultivation indicates that they may be active through multiple cultivations of this consortium and act as public goods that sustain the community. Thus, the provision of extracellular GHs as public goods may influence microbial community dynamics in native biomass-deconstructing communities relevant to agriculture, human health and biotechnology.},
doi = {10.1038/s41564-017-0052-z},
journal = {Nature Microbiology},
number = 1,
volume = 3,
place = {United States},
year = {2017},
month = {11}
}

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    Works referencing / citing this record:

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