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Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures

BACKGROUND: The interspecies interactions in a biomethanation community play a vital role in substrate degradation and methane (CH(4)) formation. However, the physiological and molecular mechanisms of interaction among the microbial members of this community remain poorly understood due to the lack...

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Autores principales: Lu, Hongyuan, Ng, Siu-Kin, Jia, Yangyang, Cai, Mingwei, Lee, Patrick K. H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5297212/
https://www.ncbi.nlm.nih.gov/pubmed/28191038
http://dx.doi.org/10.1186/s13068-017-0719-y
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author Lu, Hongyuan
Ng, Siu-Kin
Jia, Yangyang
Cai, Mingwei
Lee, Patrick K. H.
author_facet Lu, Hongyuan
Ng, Siu-Kin
Jia, Yangyang
Cai, Mingwei
Lee, Patrick K. H.
author_sort Lu, Hongyuan
collection PubMed
description BACKGROUND: The interspecies interactions in a biomethanation community play a vital role in substrate degradation and methane (CH(4)) formation. However, the physiological and molecular mechanisms of interaction among the microbial members of this community remain poorly understood due to the lack of an experimentally tractable model system. In this study, we successfully established two coculture models combining the cellulose-degrading bacterium Clostridium cellulovorans 743B with Methanosarcina barkeri Fusaro or Methanosarcina mazei Gö1 for the direct conversion of cellulose to CH(4). RESULTS: Physiological characterizations of these models revealed that the methanogens in both cocultures were able to efficiently utilize the products produced by C. cellulovorans during cellulose degradation. In particular, the simultaneous utilization of hydrogen, formate, and acetate for methanogenesis was observed in the C. cellulovorans–M. barkeri cocultures, whereas monocultures of M. barkeri were unable to grow with formate alone. Enhanced cellulose degradation was observed in both cocultures, and the CH(4) yield of the C. cellulovorans–M. barkeri cocultures (0.87 ± 0.02 mol CH(4)/mol glucose equivalent) was among the highest compared to other coculture studies. A metabolic shift in the fermentation pattern of C. cellulovorans was observed in both cocultures. The expression levels of genes in key pathways that are important to the regulation and metabolism of the interactions in cocultures were examined by reverse transcription-quantitative PCR, and the expression profiles largely matched the physiological observations. CONCLUSIONS: The physiological and molecular characteristics of the interactions of two CH(4)-producing cocultures are reported. Coculturing C. cellulovorans with M. barkeri or M. mazei not only enabled direct conversion of cellulose to CH(4), but also stabilized pH for C. cellulovorans, resulting in a metabolic shift and enhanced cellulose degradation. This study deepens our understanding of interspecies interactions for CH(4) production from cellulose, providing useful insights for assembling consortia as inocula for industrial biomethanation processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-017-0719-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-52972122017-02-10 Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures Lu, Hongyuan Ng, Siu-Kin Jia, Yangyang Cai, Mingwei Lee, Patrick K. H. Biotechnol Biofuels Research BACKGROUND: The interspecies interactions in a biomethanation community play a vital role in substrate degradation and methane (CH(4)) formation. However, the physiological and molecular mechanisms of interaction among the microbial members of this community remain poorly understood due to the lack of an experimentally tractable model system. In this study, we successfully established two coculture models combining the cellulose-degrading bacterium Clostridium cellulovorans 743B with Methanosarcina barkeri Fusaro or Methanosarcina mazei Gö1 for the direct conversion of cellulose to CH(4). RESULTS: Physiological characterizations of these models revealed that the methanogens in both cocultures were able to efficiently utilize the products produced by C. cellulovorans during cellulose degradation. In particular, the simultaneous utilization of hydrogen, formate, and acetate for methanogenesis was observed in the C. cellulovorans–M. barkeri cocultures, whereas monocultures of M. barkeri were unable to grow with formate alone. Enhanced cellulose degradation was observed in both cocultures, and the CH(4) yield of the C. cellulovorans–M. barkeri cocultures (0.87 ± 0.02 mol CH(4)/mol glucose equivalent) was among the highest compared to other coculture studies. A metabolic shift in the fermentation pattern of C. cellulovorans was observed in both cocultures. The expression levels of genes in key pathways that are important to the regulation and metabolism of the interactions in cocultures were examined by reverse transcription-quantitative PCR, and the expression profiles largely matched the physiological observations. CONCLUSIONS: The physiological and molecular characteristics of the interactions of two CH(4)-producing cocultures are reported. Coculturing C. cellulovorans with M. barkeri or M. mazei not only enabled direct conversion of cellulose to CH(4), but also stabilized pH for C. cellulovorans, resulting in a metabolic shift and enhanced cellulose degradation. This study deepens our understanding of interspecies interactions for CH(4) production from cellulose, providing useful insights for assembling consortia as inocula for industrial biomethanation processes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-017-0719-y) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-07 /pmc/articles/PMC5297212/ /pubmed/28191038 http://dx.doi.org/10.1186/s13068-017-0719-y Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Lu, Hongyuan
Ng, Siu-Kin
Jia, Yangyang
Cai, Mingwei
Lee, Patrick K. H.
Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title_full Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title_fullStr Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title_full_unstemmed Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title_short Physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
title_sort physiological and molecular characterizations of the interactions in two cellulose-to-methane cocultures
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5297212/
https://www.ncbi.nlm.nih.gov/pubmed/28191038
http://dx.doi.org/10.1186/s13068-017-0719-y
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