A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor

Acid crisis characterized by acid accumulation and/or low pH is a common reason for the failure of anaerobic digestion (AD), which is usually applied for wastewater and waste treatment. Acid-tolerant methanogens are rarely reported to be active in the artificial anaerobic digester. In this study, we...

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Main Authors: Wenhao Han, Pinjing He, Yucheng Lin, Liming Shao, Fan Lü
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02757/full
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author Wenhao Han
Wenhao Han
Pinjing He
Pinjing He
Yucheng Lin
Yucheng Lin
Liming Shao
Liming Shao
Fan Lü
Fan Lü
author_facet Wenhao Han
Wenhao Han
Pinjing He
Pinjing He
Yucheng Lin
Yucheng Lin
Liming Shao
Liming Shao
Fan Lü
Fan Lü
author_sort Wenhao Han
collection DOAJ
description Acid crisis characterized by acid accumulation and/or low pH is a common reason for the failure of anaerobic digestion (AD), which is usually applied for wastewater and waste treatment. Acid-tolerant methanogens are rarely reported to be active in the artificial anaerobic digester. In this study, we observed that the thermophilic methanogenesis by a consortium in the form of flocs and not granules could still be recovered during long-term operation at acetate concentration of up to 104 mM and pH 5.5 by adjusting the pH gradually or directly to pH 5.5 or 5.0. The acclimation process involving the gradual decrease in pH could enhance the resistance of the consortium against extreme acidification. The stable isotopic signature analysis of biogas revealed that Methanosarcina, which produced methane through acetoclastic methanogenesis (AM) pathway, was the predominant methane producer when the pH was decreased gradually to 5.0. Meanwhile, the abundance of Coprothermobacter increased with a decrease in pH. Contrastingly, when directly subjected to an environment of pH 5.5 and 104 mM acetate (15.84-mM free acetic acid) after a 42-day lag phase, Methanothermobacter was the predominant methanogen. Methanothermobacter initiated methane production through the hydrogenotrophic pathway and formed syntrophic relationship/consortium with the potential acetate-oxidizing bacteria, Thermacetogenium and Coprothermobacter. Comparative metagenomic and metatranscriptomic analysis on this self-adapted and acid-tolerant consortium revealed that the genes, such as GroEL, DnaK, CheY, and flagellum-related genes (FlaA, FlgE, and FliC) from Anaerobaculum, Thermacetogenium, and Coprothermobacter were highly overexpressed in response to system acidification. Microbial self-adaptation patterns (community structure adjustment, methanogenesis pathway shift, and transcriptional regulation) of thermophilic methanogenic consortium to gradual and sudden acidification were evaluated by integrated stable isotopic signature and comparative meta-omic approaches. The study elucidated the acid-resistant mechanism of thermophilic methanogenic consortium and deepened our knowledge of the function, interaction, and microbial characteristics of Methanosarcina, Methanothermobacter, and Coprothermobacter under extreme acidic environment.
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spelling doaj.art-64eeee46860544c49b374819d6f50fa82022-12-21T18:19:30ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02757480705A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic BioreactorWenhao Han0Wenhao Han1Pinjing He2Pinjing He3Yucheng Lin4Yucheng Lin5Liming Shao6Liming Shao7Fan Lü8Fan Lü9State Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai, ChinaShanghai Institute of Pollution Control and Ecological Security, Shanghai, ChinaShanghai Institute of Pollution Control and Ecological Security, Shanghai, ChinaInstitute of Waste Treatment and Reclamation, Tongji University, Shanghai, ChinaState Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai, ChinaShanghai Institute of Pollution Control and Ecological Security, Shanghai, ChinaShanghai Institute of Pollution Control and Ecological Security, Shanghai, ChinaInstitute of Waste Treatment and Reclamation, Tongji University, Shanghai, ChinaState Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai, ChinaInstitute of Waste Treatment and Reclamation, Tongji University, Shanghai, ChinaAcid crisis characterized by acid accumulation and/or low pH is a common reason for the failure of anaerobic digestion (AD), which is usually applied for wastewater and waste treatment. Acid-tolerant methanogens are rarely reported to be active in the artificial anaerobic digester. In this study, we observed that the thermophilic methanogenesis by a consortium in the form of flocs and not granules could still be recovered during long-term operation at acetate concentration of up to 104 mM and pH 5.5 by adjusting the pH gradually or directly to pH 5.5 or 5.0. The acclimation process involving the gradual decrease in pH could enhance the resistance of the consortium against extreme acidification. The stable isotopic signature analysis of biogas revealed that Methanosarcina, which produced methane through acetoclastic methanogenesis (AM) pathway, was the predominant methane producer when the pH was decreased gradually to 5.0. Meanwhile, the abundance of Coprothermobacter increased with a decrease in pH. Contrastingly, when directly subjected to an environment of pH 5.5 and 104 mM acetate (15.84-mM free acetic acid) after a 42-day lag phase, Methanothermobacter was the predominant methanogen. Methanothermobacter initiated methane production through the hydrogenotrophic pathway and formed syntrophic relationship/consortium with the potential acetate-oxidizing bacteria, Thermacetogenium and Coprothermobacter. Comparative metagenomic and metatranscriptomic analysis on this self-adapted and acid-tolerant consortium revealed that the genes, such as GroEL, DnaK, CheY, and flagellum-related genes (FlaA, FlgE, and FliC) from Anaerobaculum, Thermacetogenium, and Coprothermobacter were highly overexpressed in response to system acidification. Microbial self-adaptation patterns (community structure adjustment, methanogenesis pathway shift, and transcriptional regulation) of thermophilic methanogenic consortium to gradual and sudden acidification were evaluated by integrated stable isotopic signature and comparative meta-omic approaches. The study elucidated the acid-resistant mechanism of thermophilic methanogenic consortium and deepened our knowledge of the function, interaction, and microbial characteristics of Methanosarcina, Methanothermobacter, and Coprothermobacter under extreme acidic environment.https://www.frontiersin.org/article/10.3389/fmicb.2019.02757/fullthermophilic anaerobic digestionextreme acidificationmeta-omicslong-term survivaltranscriptional regulationacid tolerance
spellingShingle Wenhao Han
Wenhao Han
Pinjing He
Pinjing He
Yucheng Lin
Yucheng Lin
Liming Shao
Liming Shao
Fan Lü
Fan Lü
A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
Frontiers in Microbiology
thermophilic anaerobic digestion
extreme acidification
meta-omics
long-term survival
transcriptional regulation
acid tolerance
title A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
title_full A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
title_fullStr A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
title_full_unstemmed A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
title_short A Methanogenic Consortium Was Active and Exhibited Long-Term Survival in an Extremely Acidified Thermophilic Bioreactor
title_sort methanogenic consortium was active and exhibited long term survival in an extremely acidified thermophilic bioreactor
topic thermophilic anaerobic digestion
extreme acidification
meta-omics
long-term survival
transcriptional regulation
acid tolerance
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02757/full
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