Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion

In anaerobic digestion (AD), butyrate is degraded by syntrophic consortium, but can accumulate in highly loaded AD systems. The effect of butyrate on the AD process attracts much less attention than propionate or acetate. In this work, an enrichment culture of the thermophilic butyrate-oxidizing syn...

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Main Authors: Anna A. Nikitina, Anna Y. Kallistova, Denis S. Grouzdev, Tat’yana V. Kolganova, Andrey A. Kovalev, Dmitriy A. Kovalev, Vladimir Panchenko, Ivar Zekker, Alla N. Nozhevnikova, Yuriy V. Litti
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Applied Sciences
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Online Access:https://www.mdpi.com/2076-3417/13/1/173
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author Anna A. Nikitina
Anna Y. Kallistova
Denis S. Grouzdev
Tat’yana V. Kolganova
Andrey A. Kovalev
Dmitriy A. Kovalev
Vladimir Panchenko
Ivar Zekker
Alla N. Nozhevnikova
Yuriy V. Litti
author_facet Anna A. Nikitina
Anna Y. Kallistova
Denis S. Grouzdev
Tat’yana V. Kolganova
Andrey A. Kovalev
Dmitriy A. Kovalev
Vladimir Panchenko
Ivar Zekker
Alla N. Nozhevnikova
Yuriy V. Litti
author_sort Anna A. Nikitina
collection DOAJ
description In anaerobic digestion (AD), butyrate is degraded by syntrophic consortium, but can accumulate in highly loaded AD systems. The effect of butyrate on the AD process attracts much less attention than propionate or acetate. In this work, an enrichment culture of the thermophilic butyrate-oxidizing syntrophic consortium was obtained by gradually increasing the initial butyrate concentration from 20 to 170 mM. Surprisingly, even the highest butyrate concentration did not significantly inhibit the methanogenic community, and the stage of acetate degradation was the limiting overall rate of the process. At 170 mM butyrate, the bacterial community changed towards the dominance of syntrophic acetate-oxidizing (SAO) bacteria related to <i>Syntrophaceticus</i> (42.9%), <i>Syntrophomonas</i> (26.2%) and <i>Firmicutes</i> (26.2%), while the archaeal community experienced a sharp decrease in the abundance of <i>Methanosarcina thermophila</i> (from 86.0 to 25.0%) and increase in <i>Methanothermobacter thermautotrophicus</i> (from 3.2 to 53.1%) and <i>Methanomassiliicoccus</i> (from 3.2 to 21.9%). Thus, the shift from acetoclastic methanogenesis to SAO coupled to hydrogenotrophic methanogenesis occurred as an adaptive strategy to overcome high acetate (~200 mM) build-up. Bioaugmentation with the obtained enrichment culture was effective in mitigating the butyrate-dominated VFA build-up during the AD of readily biodegradable waste, increasing the methane production rate, methane yield and volatile solids removal by more than 3.5, 6.2 and 2.9 times, respectively. Our study revealed that the thermophilic butyrate-oxidizing consortia as bioaugmented culture could be the potential strategy to alleviate the high organic load and VFA stress of AD.
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spelling doaj.art-c19160efa33d43389d54648f0d61f30f2023-11-16T14:51:41ZengMDPI AGApplied Sciences2076-34172022-12-0113117310.3390/app13010173Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic DigestionAnna A. Nikitina0Anna Y. Kallistova1Denis S. Grouzdev2Tat’yana V. Kolganova3Andrey A. Kovalev4Dmitriy A. Kovalev5Vladimir Panchenko6Ivar Zekker7Alla N. Nozhevnikova8Yuriy V. Litti9Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/2, Moscow 117312, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/2, Moscow 117312, RussiaSciBear OU, Tartu Mnt 67/1-13b, Kesklinna Linnaosa, 10115 Tallin, EstoniaInstitute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/1, Moscow 117312, RussiaDepartment of Renewable Energy, Federal Scientific Agroengineering Center VIM, Moscow 109428, RussiaDepartment of Renewable Energy, Federal Scientific Agroengineering Center VIM, Moscow 109428, RussiaDepartment of Theoretical and Applied Mechanics, Russian University of Transport, Moscow 127994, RussiaFaculty of Science, Institute of Chemistry, University of Tartu, 14 Ravila St., 50411 Tartu, EstoniaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/2, Moscow 117312, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7/2, Moscow 117312, RussiaIn anaerobic digestion (AD), butyrate is degraded by syntrophic consortium, but can accumulate in highly loaded AD systems. The effect of butyrate on the AD process attracts much less attention than propionate or acetate. In this work, an enrichment culture of the thermophilic butyrate-oxidizing syntrophic consortium was obtained by gradually increasing the initial butyrate concentration from 20 to 170 mM. Surprisingly, even the highest butyrate concentration did not significantly inhibit the methanogenic community, and the stage of acetate degradation was the limiting overall rate of the process. At 170 mM butyrate, the bacterial community changed towards the dominance of syntrophic acetate-oxidizing (SAO) bacteria related to <i>Syntrophaceticus</i> (42.9%), <i>Syntrophomonas</i> (26.2%) and <i>Firmicutes</i> (26.2%), while the archaeal community experienced a sharp decrease in the abundance of <i>Methanosarcina thermophila</i> (from 86.0 to 25.0%) and increase in <i>Methanothermobacter thermautotrophicus</i> (from 3.2 to 53.1%) and <i>Methanomassiliicoccus</i> (from 3.2 to 21.9%). Thus, the shift from acetoclastic methanogenesis to SAO coupled to hydrogenotrophic methanogenesis occurred as an adaptive strategy to overcome high acetate (~200 mM) build-up. Bioaugmentation with the obtained enrichment culture was effective in mitigating the butyrate-dominated VFA build-up during the AD of readily biodegradable waste, increasing the methane production rate, methane yield and volatile solids removal by more than 3.5, 6.2 and 2.9 times, respectively. Our study revealed that the thermophilic butyrate-oxidizing consortia as bioaugmented culture could be the potential strategy to alleviate the high organic load and VFA stress of AD.https://www.mdpi.com/2076-3417/13/1/173bioaugmentationanaerobic digestionacetoclastichydrogenotrophicsyntrophic consortiumsyntrophic acetate oxidation
spellingShingle Anna A. Nikitina
Anna Y. Kallistova
Denis S. Grouzdev
Tat’yana V. Kolganova
Andrey A. Kovalev
Dmitriy A. Kovalev
Vladimir Panchenko
Ivar Zekker
Alla N. Nozhevnikova
Yuriy V. Litti
Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
Applied Sciences
bioaugmentation
anaerobic digestion
acetoclastic
hydrogenotrophic
syntrophic consortium
syntrophic acetate oxidation
title Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
title_full Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
title_fullStr Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
title_full_unstemmed Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
title_short Syntrophic Butyrate-Oxidizing Consortium Mitigates Acetate Inhibition through a Shift from Acetoclastic to Hydrogenotrophic Methanogenesis and Alleviates VFA Stress in Thermophilic Anaerobic Digestion
title_sort syntrophic butyrate oxidizing consortium mitigates acetate inhibition through a shift from acetoclastic to hydrogenotrophic methanogenesis and alleviates vfa stress in thermophilic anaerobic digestion
topic bioaugmentation
anaerobic digestion
acetoclastic
hydrogenotrophic
syntrophic consortium
syntrophic acetate oxidation
url https://www.mdpi.com/2076-3417/13/1/173
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