Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome

ABSTRACT Biogas reactors operating with protein-rich substrates have high methane potential and industrial value; however, they are highly susceptible to process failure because of the accumulation of ammonia. High ammonia levels cause a decline in acetate-utilizing methanogens and instead promote t...

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Autores principales:	J. A. Frank, M. Ø. Arntzen, L. Sun, L. H. Hagen, A. C. McHardy, S. J. Horn, V. G. H. Eijsink, A. Schnürer, P. B. Pope
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	anaerobic digestion biogas metagenomics metaproteomics syntrophic acetate oxidation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b306cb5d666e4ad4ace0f2d6d2058459
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spelling	oai:doaj.org-article:b306cb5d666e4ad4ace0f2d6d20584592021-12-02T18:15:43ZNovel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome10.1128/mSystems.00092-162379-5077https://doaj.org/article/b306cb5d666e4ad4ace0f2d6d20584592016-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00092-16https://doaj.org/toc/2379-5077ABSTRACT Biogas reactors operating with protein-rich substrates have high methane potential and industrial value; however, they are highly susceptible to process failure because of the accumulation of ammonia. High ammonia levels cause a decline in acetate-utilizing methanogens and instead promote the conversion of acetate via a two-step mechanism involving syntrophic acetate oxidation (SAO) to H2 and CO2, followed by hydrogenotrophic methanogenesis. Despite the key role of syntrophic acetate-oxidizing bacteria (SAOB), only a few culturable representatives have been characterized. Here we show that the microbiome of a commercial, ammonia-tolerant biogas reactor harbors a deeply branched, uncultured phylotype (unFirm_1) accounting for approximately 5% of the 16S rRNA gene inventory and sharing 88% 16S rRNA gene identity with its closest characterized relative. Reconstructed genome and quantitative metaproteomic analyses imply unFirm_1’s metabolic dominance and SAO capabilities, whereby the key enzymes required for acetate oxidation are among the most highly detected in the reactor microbiome. While culturable SAOB were identified in genomic analyses of the reactor, their limited proteomic representation suggests that unFirm_1 plays an important role in channeling acetate toward methane. Notably, unFirm_1-like populations were found in other high-ammonia biogas installations, conjecturing a broader importance for this novel clade of SAOB in anaerobic fermentations. IMPORTANCE The microbial production of methane or “biogas” is an attractive renewable energy technology that can recycle organic waste into biofuel. Biogas reactors operating with protein-rich substrates such as household municipal or agricultural wastes have significant industrial and societal value; however, they are highly unstable and frequently collapse due to the accumulation of ammonia. We report the discovery of a novel uncultured phylotype (unFirm_1) that is highly detectable in metaproteomic data generated from an ammonia-tolerant commercial reactor. Importantly, unFirm_1 is proposed to perform a key metabolic step in biogas microbiomes, whereby it syntrophically oxidizes acetate to hydrogen and carbon dioxide, which methanogens then covert to methane. Only very few culturable syntrophic acetate-oxidizing bacteria have been described, and all were detected at low in situ levels compared to unFirm_1. Broader comparisons produced the hypothesis that unFirm_1 is a key mediator toward the successful long-term stable operation of biogas production using protein-rich substrates.J. A. FrankM. Ø. ArntzenL. SunL. H. HagenA. C. McHardyS. J. HornV. G. H. EijsinkA. SchnürerP. B. PopeAmerican Society for Microbiologyarticleanaerobic digestionbiogasmetagenomicsmetaproteomicssyntrophic acetate oxidationMicrobiologyQR1-502ENmSystems, Vol 1, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	anaerobic digestion biogas metagenomics metaproteomics syntrophic acetate oxidation Microbiology QR1-502
spellingShingle	anaerobic digestion biogas metagenomics metaproteomics syntrophic acetate oxidation Microbiology QR1-502 J. A. Frank M. Ø. Arntzen L. Sun L. H. Hagen A. C. McHardy S. J. Horn V. G. H. Eijsink A. Schnürer P. B. Pope Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
description	ABSTRACT Biogas reactors operating with protein-rich substrates have high methane potential and industrial value; however, they are highly susceptible to process failure because of the accumulation of ammonia. High ammonia levels cause a decline in acetate-utilizing methanogens and instead promote the conversion of acetate via a two-step mechanism involving syntrophic acetate oxidation (SAO) to H2 and CO2, followed by hydrogenotrophic methanogenesis. Despite the key role of syntrophic acetate-oxidizing bacteria (SAOB), only a few culturable representatives have been characterized. Here we show that the microbiome of a commercial, ammonia-tolerant biogas reactor harbors a deeply branched, uncultured phylotype (unFirm_1) accounting for approximately 5% of the 16S rRNA gene inventory and sharing 88% 16S rRNA gene identity with its closest characterized relative. Reconstructed genome and quantitative metaproteomic analyses imply unFirm_1’s metabolic dominance and SAO capabilities, whereby the key enzymes required for acetate oxidation are among the most highly detected in the reactor microbiome. While culturable SAOB were identified in genomic analyses of the reactor, their limited proteomic representation suggests that unFirm_1 plays an important role in channeling acetate toward methane. Notably, unFirm_1-like populations were found in other high-ammonia biogas installations, conjecturing a broader importance for this novel clade of SAOB in anaerobic fermentations. IMPORTANCE The microbial production of methane or “biogas” is an attractive renewable energy technology that can recycle organic waste into biofuel. Biogas reactors operating with protein-rich substrates such as household municipal or agricultural wastes have significant industrial and societal value; however, they are highly unstable and frequently collapse due to the accumulation of ammonia. We report the discovery of a novel uncultured phylotype (unFirm_1) that is highly detectable in metaproteomic data generated from an ammonia-tolerant commercial reactor. Importantly, unFirm_1 is proposed to perform a key metabolic step in biogas microbiomes, whereby it syntrophically oxidizes acetate to hydrogen and carbon dioxide, which methanogens then covert to methane. Only very few culturable syntrophic acetate-oxidizing bacteria have been described, and all were detected at low in situ levels compared to unFirm_1. Broader comparisons produced the hypothesis that unFirm_1 is a key mediator toward the successful long-term stable operation of biogas production using protein-rich substrates.
format	article
author	J. A. Frank M. Ø. Arntzen L. Sun L. H. Hagen A. C. McHardy S. J. Horn V. G. H. Eijsink A. Schnürer P. B. Pope
author_facet	J. A. Frank M. Ø. Arntzen L. Sun L. H. Hagen A. C. McHardy S. J. Horn V. G. H. Eijsink A. Schnürer P. B. Pope
author_sort	J. A. Frank
title	Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
title_short	Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
title_full	Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
title_fullStr	Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
title_full_unstemmed	Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome
title_sort	novel syntrophic populations dominate an ammonia-tolerant methanogenic microbiome
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/b306cb5d666e4ad4ace0f2d6d2058459
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Novel Syntrophic Populations Dominate an Ammonia-Tolerant Methanogenic Microbiome

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