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Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1

BACKGROUND: Lignocellulolytic bacteria have revealed to be a promising source for biofuel production, yet the underlying mechanisms are still worth exploring. Our previous study inferred that the highly efficient lignocellulose degradation by bacterium Pantoea ananatis Sd-1 might involve Fenton chem...

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Autores principales: Ma, Jiangshan, Zhang, Keke, Huang, Mei, Hector, Stanton B., Liu, Bin, Tong, Chunyi, Liu, Qian, Zeng, Jiarui, Gao, Yan, Xu, Ting, Liu, Ying, Liu, Xuanming, Zhu, Yonghua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5054592/
https://www.ncbi.nlm.nih.gov/pubmed/27761153
http://dx.doi.org/10.1186/s13068-016-0623-x
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author Ma, Jiangshan
Zhang, Keke
Huang, Mei
Hector, Stanton B.
Liu, Bin
Tong, Chunyi
Liu, Qian
Zeng, Jiarui
Gao, Yan
Xu, Ting
Liu, Ying
Liu, Xuanming
Zhu, Yonghua
author_facet Ma, Jiangshan
Zhang, Keke
Huang, Mei
Hector, Stanton B.
Liu, Bin
Tong, Chunyi
Liu, Qian
Zeng, Jiarui
Gao, Yan
Xu, Ting
Liu, Ying
Liu, Xuanming
Zhu, Yonghua
author_sort Ma, Jiangshan
collection PubMed
description BACKGROUND: Lignocellulolytic bacteria have revealed to be a promising source for biofuel production, yet the underlying mechanisms are still worth exploring. Our previous study inferred that the highly efficient lignocellulose degradation by bacterium Pantoea ananatis Sd-1 might involve Fenton chemistry (Fe(2+) + H(2)O(2) + H(+) → Fe(3+) + OH· + H(2)O), similar to that of white-rot and brown-rot fungi. The aim of this work is to investigate the existence of this Fenton-based oxidation mechanism in the rice straw degradation process of P. ananatis Sd-1. RESULTS: After 3 days incubation of unpretreated rice straw with P. ananatis Sd-1, the percentage in weight reduction of rice straw as well as its cellulose, hemicellulose, and lignin components reached 46.7, 43.1, 42.9, and 37.9 %, respectively. The addition of different hydroxyl radical scavengers resulted in a significant decline (P < 0.001) in rice straw degradation. Pyrolysis gas chromatography–mass spectrometry and Fourier transform infrared spectroscopy analysis revealed the consistency of chemical changes of rice straw components that exists between P. ananatis Sd-1 and Fenton reagent treatment. In addition to the increased total iron ion concentration throughout the rice straw decomposition process, the Fe(3+)-reducing capacity of P. ananatis Sd-1 was induced by rice straw and predominantly contributed by aromatic compounds metabolites. The transcript levels of the glucose-methanol-choline oxidoreductase gene related to hydrogen peroxide production were significantly up-regulated (at least P < 0.01) in rice straw cultures. Higher activities of GMC oxidoreductase and less hydrogen peroxide concentration in rice straw cultures relative to glucose cultures may be responsible for increasing rice straw degradation, which includes Fenton-like reactions. CONCLUSIONS: Our results confirmed the Fenton chemistry-assisted degradation model in P. ananatis Sd-1. We are among the first to show that a Fenton-based oxidation mechanism exists in a bacteria degradation system, which provides a new perspective for how natural plant biomass is decomposed by bacteria. This degradative system may offer an alternative approach to the fungi system for lignocellulosic biofuels production. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0623-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-50545922016-10-19 Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1 Ma, Jiangshan Zhang, Keke Huang, Mei Hector, Stanton B. Liu, Bin Tong, Chunyi Liu, Qian Zeng, Jiarui Gao, Yan Xu, Ting Liu, Ying Liu, Xuanming Zhu, Yonghua Biotechnol Biofuels Research BACKGROUND: Lignocellulolytic bacteria have revealed to be a promising source for biofuel production, yet the underlying mechanisms are still worth exploring. Our previous study inferred that the highly efficient lignocellulose degradation by bacterium Pantoea ananatis Sd-1 might involve Fenton chemistry (Fe(2+) + H(2)O(2) + H(+) → Fe(3+) + OH· + H(2)O), similar to that of white-rot and brown-rot fungi. The aim of this work is to investigate the existence of this Fenton-based oxidation mechanism in the rice straw degradation process of P. ananatis Sd-1. RESULTS: After 3 days incubation of unpretreated rice straw with P. ananatis Sd-1, the percentage in weight reduction of rice straw as well as its cellulose, hemicellulose, and lignin components reached 46.7, 43.1, 42.9, and 37.9 %, respectively. The addition of different hydroxyl radical scavengers resulted in a significant decline (P < 0.001) in rice straw degradation. Pyrolysis gas chromatography–mass spectrometry and Fourier transform infrared spectroscopy analysis revealed the consistency of chemical changes of rice straw components that exists between P. ananatis Sd-1 and Fenton reagent treatment. In addition to the increased total iron ion concentration throughout the rice straw decomposition process, the Fe(3+)-reducing capacity of P. ananatis Sd-1 was induced by rice straw and predominantly contributed by aromatic compounds metabolites. The transcript levels of the glucose-methanol-choline oxidoreductase gene related to hydrogen peroxide production were significantly up-regulated (at least P < 0.01) in rice straw cultures. Higher activities of GMC oxidoreductase and less hydrogen peroxide concentration in rice straw cultures relative to glucose cultures may be responsible for increasing rice straw degradation, which includes Fenton-like reactions. CONCLUSIONS: Our results confirmed the Fenton chemistry-assisted degradation model in P. ananatis Sd-1. We are among the first to show that a Fenton-based oxidation mechanism exists in a bacteria degradation system, which provides a new perspective for how natural plant biomass is decomposed by bacteria. This degradative system may offer an alternative approach to the fungi system for lignocellulosic biofuels production. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0623-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-10-06 /pmc/articles/PMC5054592/ /pubmed/27761153 http://dx.doi.org/10.1186/s13068-016-0623-x Text en © The Author(s) 2016 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
Ma, Jiangshan
Zhang, Keke
Huang, Mei
Hector, Stanton B.
Liu, Bin
Tong, Chunyi
Liu, Qian
Zeng, Jiarui
Gao, Yan
Xu, Ting
Liu, Ying
Liu, Xuanming
Zhu, Yonghua
Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title_full Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title_fullStr Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title_full_unstemmed Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title_short Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1
title_sort involvement of fenton chemistry in rice straw degradation by the lignocellulolytic bacterium pantoea ananatis sd-1
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5054592/
https://www.ncbi.nlm.nih.gov/pubmed/27761153
http://dx.doi.org/10.1186/s13068-016-0623-x
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