Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

ABSTRACT Methanogenic archaea are key players in cycling organic matter in nature but also in engineered waste treatment systems, where they generate methane, which can be used as a renewable energy source. In such systems in the built environment, complex methanogenic consortia are known to aggrega...

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Autores principales:	Anna Christine Trego, Sarah O’Sullivan, Christopher Quince, Simon Mills, Umer Zeeshan Ijaz, Gavin Collins
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	community assembly anaerobic digestion biofilm methanogenic granules microbial community assembly Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/16119107754644a280cf70c6648e3dc4
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spelling	oai:doaj.org-article:16119107754644a280cf70c6648e3dc42021-12-02T18:15:46ZSize Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle10.1128/mSystems.00323-202379-5077https://doaj.org/article/16119107754644a280cf70c6648e3dc42020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00323-20https://doaj.org/toc/2379-5077ABSTRACT Methanogenic archaea are key players in cycling organic matter in nature but also in engineered waste treatment systems, where they generate methane, which can be used as a renewable energy source. In such systems in the built environment, complex methanogenic consortia are known to aggregate into highly organized, spherical granular biofilms comprising the interdependent microbial trophic groups mediating the successive stages of the anaerobic digestion (AD) process. This study separated methanogenic granules into a range of discrete size fractions, hypothesizing different biofilm growth stages, and separately supplied each with specific substrates to stimulate the activity of key AD trophic groups, including syntrophic acid oxidizers and methanogens. Rates of specific methanogenic activity were measured, and amplicon sequencing of 16S rRNA gene transcripts was used to resolve phylotranscriptomes across the series of size fractions. Increased rates of methane production were observed in each of the size fractions when hydrogen was supplied as the substrate compared with those of volatile fatty acids (acetate, propionate, and butyrate). This was connected to a shift toward hydrogenotrophic methanogenesis dominated by Methanobacterium and Methanolinea. Interestingly, the specific active microbiomes measured in this way indicated that size was significantly more important than substrate in driving the structure of the active community in granules. Multivariate integration studywise discriminant analysis identified 56 genera shaping changes in the active community across both substrate and size. Half of those were found to be upregulated in the medium-sized granules, which were also the most active and potentially of the most important size, or life stage, for precision management of AD systems. IMPORTANCE Biological wastewater conversion processes collectively constitute one of the single biggest worldwide applications of microbial communities. There is an obvious requirement, therefore, to study the microbial systems central to the success of such technologies. Methanogenic granules, in particular, are architecturally fascinating biofilms that facilitate highly organized cooperation within the metabolic network of the anaerobic digestion (AD) process and, thus, are especially intriguing model systems for microbial ecology. This study, in a way not previously reported, provoked syntrophic and methanogenic activity and the structure of the microbial community, using specific substrates targeting the key trophic groups in AD. Unexpectedly, granule size more strongly than substrate shaped the active portion of the microbial community. Importantly, the findings suggest the size, or age, of granules inherently shapes the active microbiome linked to a life cycle. This provides exciting insights into the function of, and the potential for additional modeling of biofilm development in, methanogenic granules.Anna Christine TregoSarah O’SullivanChristopher QuinceSimon MillsUmer Zeeshan IjazGavin CollinsAmerican Society for Microbiologyarticlecommunity assemblyanaerobic digestionbiofilmmethanogenic granulesmicrobial community assemblyMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	community assembly anaerobic digestion biofilm methanogenic granules microbial community assembly Microbiology QR1-502
spellingShingle	community assembly anaerobic digestion biofilm methanogenic granules microbial community assembly Microbiology QR1-502 Anna Christine Trego Sarah O’Sullivan Christopher Quince Simon Mills Umer Zeeshan Ijaz Gavin Collins Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
description	ABSTRACT Methanogenic archaea are key players in cycling organic matter in nature but also in engineered waste treatment systems, where they generate methane, which can be used as a renewable energy source. In such systems in the built environment, complex methanogenic consortia are known to aggregate into highly organized, spherical granular biofilms comprising the interdependent microbial trophic groups mediating the successive stages of the anaerobic digestion (AD) process. This study separated methanogenic granules into a range of discrete size fractions, hypothesizing different biofilm growth stages, and separately supplied each with specific substrates to stimulate the activity of key AD trophic groups, including syntrophic acid oxidizers and methanogens. Rates of specific methanogenic activity were measured, and amplicon sequencing of 16S rRNA gene transcripts was used to resolve phylotranscriptomes across the series of size fractions. Increased rates of methane production were observed in each of the size fractions when hydrogen was supplied as the substrate compared with those of volatile fatty acids (acetate, propionate, and butyrate). This was connected to a shift toward hydrogenotrophic methanogenesis dominated by Methanobacterium and Methanolinea. Interestingly, the specific active microbiomes measured in this way indicated that size was significantly more important than substrate in driving the structure of the active community in granules. Multivariate integration studywise discriminant analysis identified 56 genera shaping changes in the active community across both substrate and size. Half of those were found to be upregulated in the medium-sized granules, which were also the most active and potentially of the most important size, or life stage, for precision management of AD systems. IMPORTANCE Biological wastewater conversion processes collectively constitute one of the single biggest worldwide applications of microbial communities. There is an obvious requirement, therefore, to study the microbial systems central to the success of such technologies. Methanogenic granules, in particular, are architecturally fascinating biofilms that facilitate highly organized cooperation within the metabolic network of the anaerobic digestion (AD) process and, thus, are especially intriguing model systems for microbial ecology. This study, in a way not previously reported, provoked syntrophic and methanogenic activity and the structure of the microbial community, using specific substrates targeting the key trophic groups in AD. Unexpectedly, granule size more strongly than substrate shaped the active portion of the microbial community. Importantly, the findings suggest the size, or age, of granules inherently shapes the active microbiome linked to a life cycle. This provides exciting insights into the function of, and the potential for additional modeling of biofilm development in, methanogenic granules.
format	article
author	Anna Christine Trego Sarah O’Sullivan Christopher Quince Simon Mills Umer Zeeshan Ijaz Gavin Collins
author_facet	Anna Christine Trego Sarah O’Sullivan Christopher Quince Simon Mills Umer Zeeshan Ijaz Gavin Collins
author_sort	Anna Christine Trego
title	Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
title_short	Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
title_full	Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
title_fullStr	Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
title_full_unstemmed	Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle
title_sort	size shapes the active microbiome of methanogenic granules, corroborating a biofilm life cycle
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/16119107754644a280cf70c6648e3dc4
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_version_	1718378318331379712

Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

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