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Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions
During anaerobic digestion (AD) of protein-rich wastewater, ammonium (NH(4)(+)) is released by amino acid degradation. High NH(4)(+) concentrations disturb the AD microbiome balance, leading to process impairments. The sensitivity of the AD microbiome to NH(4)(+) and the inhibition threshold depend...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8510171/ https://www.ncbi.nlm.nih.gov/pubmed/34612672 http://dx.doi.org/10.1128/Spectrum.00805-21 |
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author | Hardy, Julie Bonin, Patricia Lazuka, Adele Gonidec, Estelle Guasco, Sophie Valette, Corinne Lacroix, Sébastien Cabrol, Léa |
author_facet | Hardy, Julie Bonin, Patricia Lazuka, Adele Gonidec, Estelle Guasco, Sophie Valette, Corinne Lacroix, Sébastien Cabrol, Léa |
author_sort | Hardy, Julie |
collection | PubMed |
description | During anaerobic digestion (AD) of protein-rich wastewater, ammonium (NH(4)(+)) is released by amino acid degradation. High NH(4)(+) concentrations disturb the AD microbiome balance, leading to process impairments. The sensitivity of the AD microbiome to NH(4)(+) and the inhibition threshold depend on multiple parameters, especially the previous microbial acclimation to ammonium stress. However, little is known about the effect of different NH(4)(+) acclimation strategies on the differential expression of key active microbial taxa. Here, we applied NH(4)(+) inputs of increasing intensity (from 1.7 to 15.2 g N-NH(4)(+) liters(−1)) in batch assays fed with synthetic wastewater, according to two different strategies: (i) direct independent inputs at a unique target concentration and (ii) successive inputs in a stepwise manner. In both strategies, along the NH(4)(+) gradient, the active methanogens shifted from acetoclastic Methanosaeta to Methanosarcina and eventually hydrogenotrophic Methanoculleus. Despite shorter latency times, the successive input modality led to lower methane production rate, lower soluble chemical oxygen demand (sCOD) removal efficiency, and lower half maximal inhibitory concentration, together with higher volatile fatty acid (VFA) accumulation, compared to the independent input modality. These differential performances were associated with a drastically distinct succession pattern of the active bacterial partners in both experiments. In particular, the direct exposure modality was characterized by a progressive enrichment of VFA producers (mainly Tepidimicrobium) and syntrophic VFA oxidizers (mainly Syntrophaceticus) with increasing NH(4)(+) concentration, while the successive exposure modality was characterized by a more dynamic succession of VFA producers (mainly Clostridium, Sporanaerobacter, Terrisporobacter) and syntrophic VFA oxidizers (mainly Tepidanaerobacter, Syntrophomonas). These results bring relevant insights for improved process management through inoculum adaptation, bioaugmentation, or community-driven optimization. IMPORTANCE Anaerobic digestion (AD) is an attractive biotechnological process for wastewater bioremediation and bioenergy production in the form of methane-rich biogas. However, AD can be inhibited by ammonium generated by protein-rich effluent, commonly found in agro-industrial activities. Insights in the microbial community composition and identification of AD key players are crucial for anticipating process impairments in response to ammonium stress. They can also help in defining an optimal microbiome adapted to high ammonium levels. Here, we compared two strategies for acclimation of AD microbiome to increasing ammonium concentration to better understand the effect of this stress on the methanogens and their bacterial partners. Our results suggest that long-term cumulative exposure to ammonia disrupted the AD microbiome more strongly than direct (independent) ammonium additions. We identified bioindicators with different NH(4)(+) tolerance capacity among VFA producers and syntrophic VFA oxidizers. |
format | Online Article Text |
id | pubmed-8510171 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-85101712021-11-08 Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions Hardy, Julie Bonin, Patricia Lazuka, Adele Gonidec, Estelle Guasco, Sophie Valette, Corinne Lacroix, Sébastien Cabrol, Léa Microbiol Spectr Research Article During anaerobic digestion (AD) of protein-rich wastewater, ammonium (NH(4)(+)) is released by amino acid degradation. High NH(4)(+) concentrations disturb the AD microbiome balance, leading to process impairments. The sensitivity of the AD microbiome to NH(4)(+) and the inhibition threshold depend on multiple parameters, especially the previous microbial acclimation to ammonium stress. However, little is known about the effect of different NH(4)(+) acclimation strategies on the differential expression of key active microbial taxa. Here, we applied NH(4)(+) inputs of increasing intensity (from 1.7 to 15.2 g N-NH(4)(+) liters(−1)) in batch assays fed with synthetic wastewater, according to two different strategies: (i) direct independent inputs at a unique target concentration and (ii) successive inputs in a stepwise manner. In both strategies, along the NH(4)(+) gradient, the active methanogens shifted from acetoclastic Methanosaeta to Methanosarcina and eventually hydrogenotrophic Methanoculleus. Despite shorter latency times, the successive input modality led to lower methane production rate, lower soluble chemical oxygen demand (sCOD) removal efficiency, and lower half maximal inhibitory concentration, together with higher volatile fatty acid (VFA) accumulation, compared to the independent input modality. These differential performances were associated with a drastically distinct succession pattern of the active bacterial partners in both experiments. In particular, the direct exposure modality was characterized by a progressive enrichment of VFA producers (mainly Tepidimicrobium) and syntrophic VFA oxidizers (mainly Syntrophaceticus) with increasing NH(4)(+) concentration, while the successive exposure modality was characterized by a more dynamic succession of VFA producers (mainly Clostridium, Sporanaerobacter, Terrisporobacter) and syntrophic VFA oxidizers (mainly Tepidanaerobacter, Syntrophomonas). These results bring relevant insights for improved process management through inoculum adaptation, bioaugmentation, or community-driven optimization. IMPORTANCE Anaerobic digestion (AD) is an attractive biotechnological process for wastewater bioremediation and bioenergy production in the form of methane-rich biogas. However, AD can be inhibited by ammonium generated by protein-rich effluent, commonly found in agro-industrial activities. Insights in the microbial community composition and identification of AD key players are crucial for anticipating process impairments in response to ammonium stress. They can also help in defining an optimal microbiome adapted to high ammonium levels. Here, we compared two strategies for acclimation of AD microbiome to increasing ammonium concentration to better understand the effect of this stress on the methanogens and their bacterial partners. Our results suggest that long-term cumulative exposure to ammonia disrupted the AD microbiome more strongly than direct (independent) ammonium additions. We identified bioindicators with different NH(4)(+) tolerance capacity among VFA producers and syntrophic VFA oxidizers. American Society for Microbiology 2021-10-06 /pmc/articles/PMC8510171/ /pubmed/34612672 http://dx.doi.org/10.1128/Spectrum.00805-21 Text en Copyright © 2021 Hardy et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Hardy, Julie Bonin, Patricia Lazuka, Adele Gonidec, Estelle Guasco, Sophie Valette, Corinne Lacroix, Sébastien Cabrol, Léa Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title | Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title_full | Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title_fullStr | Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title_full_unstemmed | Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title_short | Similar Methanogenic Shift but Divergent Syntrophic Partners in Anaerobic Digesters Exposed to Direct versus Successive Ammonium Additions |
title_sort | similar methanogenic shift but divergent syntrophic partners in anaerobic digesters exposed to direct versus successive ammonium additions |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8510171/ https://www.ncbi.nlm.nih.gov/pubmed/34612672 http://dx.doi.org/10.1128/Spectrum.00805-21 |
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