Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress
Microorganisms in anaerobic digestion (AD) are easily affected by ammonia, especially acetoclastic methanogens. Thus, in ammonia-suppressed AD systems, acetate degradation is reported to be carried out mainly by the cooperation of syntrophic acetate oxidizers and hydrogenotrophic methanogens. Previo...
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1098814/full |
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| author | Gao Feng Yan Zeng Hui-Zhong Wang Ya-Ting Chen Yue-Qin Tang Yue-Qin Tang Yue-Qin Tang |
| author_facet | Gao Feng Yan Zeng Hui-Zhong Wang Ya-Ting Chen Yue-Qin Tang Yue-Qin Tang Yue-Qin Tang |
| author_sort | Gao Feng |
| collection | DOAJ |
| description | Microorganisms in anaerobic digestion (AD) are easily affected by ammonia, especially acetoclastic methanogens. Thus, in ammonia-suppressed AD systems, acetate degradation is reported to be carried out mainly by the cooperation of syntrophic acetate oxidizers and hydrogenotrophic methanogens. Previous studies have revealed ammonia inhibition on microbial flora by AD performance, but the effect mechanism of ammonia on microbial metabolism remains poorly understood. In this study, we constructed a mesophilic chemostat fed with acetate as the sole carbon source, gradually increased the total ammonia nitrogen (TAN) concentration from 1 g L−1 to 6 g L−1, and employed the 16S rRNA gene, metagenomics, and metatranscriptomics analysis to characterize the microbial community structure and metabolic behavior. The results showed that even at the TAN of 6 g L−1 (pH 7.5), the methanogenesis kept normal, the biogas production was approximately 92% of that at TAN of 1 g L−1 and the acetate degradation ratio reached 99%, suggesting the strong TAN tolerance of the microbial community enriched. 16S rRNA gene analysis suggested that the microbial community structure changed along with the TAN concentration. Methanothrix predominated in methanogens all the time, in which the dominant species was gradually replaced from M. soehngenii to M. harundinacea with the increased TAN. Dominant bacterial species also changed and Proteiniphilum showed a significant positive correlation with increased TAN. Meta-omics analysis showed that the absolute dominant microorganisms at TAN of 6 g L−1 were M. harundinacea and Proteiniphilum, both of which highly expressed genes for anti-oxidative stress. M. harundinacea and the second dominant methanogen Methanosarcina highly expressed both acetate cleavage and CO2 reduction pathways, suggesting the possibility that these two pathways contributed to methanogenesis together. Proteiniphilum and some other species in Firmicutes and Synergistetes were likely acetate oxidizers in the community as they highly expressed genes for syntrophic acetate oxidization, H2 generation, and electron transfer. These results suggested that Proteiniphilum as well as M. harundinacea have strong ammonia tolerance and played critical roles in acetate degradation under ammonia-suppressed conditions. The achievements of the study would contribute to the regulation and management of the AD process. |
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| spelling | doaj.art-d4818cf63736427aa2dfeb43e3e5fcc22023-01-06T17:35:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-01-011310.3389/fmicb.2022.10988141098814Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stressGao Feng0Yan Zeng1Hui-Zhong Wang2Ya-Ting Chen3Yue-Qin Tang4Yue-Qin Tang5Yue-Qin Tang6College of Architecture and Environment, Sichuan University, Chengdu, Sichuan, ChinaInstitute of New Energy and Low-Carbon Technology, Sichuan University, Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, Chengdu, Sichuan, ChinaInstitute for Disaster Management and Reconstruction, Sichuan University, Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, Chengdu, Sichuan, ChinaSichuan Environmental Protection Key Laboratory of Organic Wastes Valorization, Chengdu, Sichuan, ChinaEngineering Research Center of Alternative Energy Materials & Devices, Ministry of Education, Chengdu, Sichuan, ChinaMicroorganisms in anaerobic digestion (AD) are easily affected by ammonia, especially acetoclastic methanogens. Thus, in ammonia-suppressed AD systems, acetate degradation is reported to be carried out mainly by the cooperation of syntrophic acetate oxidizers and hydrogenotrophic methanogens. Previous studies have revealed ammonia inhibition on microbial flora by AD performance, but the effect mechanism of ammonia on microbial metabolism remains poorly understood. In this study, we constructed a mesophilic chemostat fed with acetate as the sole carbon source, gradually increased the total ammonia nitrogen (TAN) concentration from 1 g L−1 to 6 g L−1, and employed the 16S rRNA gene, metagenomics, and metatranscriptomics analysis to characterize the microbial community structure and metabolic behavior. The results showed that even at the TAN of 6 g L−1 (pH 7.5), the methanogenesis kept normal, the biogas production was approximately 92% of that at TAN of 1 g L−1 and the acetate degradation ratio reached 99%, suggesting the strong TAN tolerance of the microbial community enriched. 16S rRNA gene analysis suggested that the microbial community structure changed along with the TAN concentration. Methanothrix predominated in methanogens all the time, in which the dominant species was gradually replaced from M. soehngenii to M. harundinacea with the increased TAN. Dominant bacterial species also changed and Proteiniphilum showed a significant positive correlation with increased TAN. Meta-omics analysis showed that the absolute dominant microorganisms at TAN of 6 g L−1 were M. harundinacea and Proteiniphilum, both of which highly expressed genes for anti-oxidative stress. M. harundinacea and the second dominant methanogen Methanosarcina highly expressed both acetate cleavage and CO2 reduction pathways, suggesting the possibility that these two pathways contributed to methanogenesis together. Proteiniphilum and some other species in Firmicutes and Synergistetes were likely acetate oxidizers in the community as they highly expressed genes for syntrophic acetate oxidization, H2 generation, and electron transfer. These results suggested that Proteiniphilum as well as M. harundinacea have strong ammonia tolerance and played critical roles in acetate degradation under ammonia-suppressed conditions. The achievements of the study would contribute to the regulation and management of the AD process.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1098814/fullanaerobic digestionammonia inhibitionmicrobial communitysyntrophic acetate oxidationmethanogenic pathwaysenergy conservation |
| spellingShingle | Gao Feng Yan Zeng Hui-Zhong Wang Ya-Ting Chen Yue-Qin Tang Yue-Qin Tang Yue-Qin Tang Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress Frontiers in Microbiology anaerobic digestion ammonia inhibition microbial community syntrophic acetate oxidation methanogenic pathways energy conservation |
| title | Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| title_full | Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| title_fullStr | Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| title_full_unstemmed | Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| title_short | Proteiniphilum and Methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| title_sort | proteiniphilum and methanothrix harundinacea became dominant acetate utilizers in a methanogenic reactor operated under strong ammonia stress |
| topic | anaerobic digestion ammonia inhibition microbial community syntrophic acetate oxidation methanogenic pathways energy conservation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1098814/full |
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