Size shapes the active microbiome of the methanogenic granules, corroborating a biofilm life cycle

Trego, Anna Christine, O'Sullivan, Sarah, Quince, Christopher, Mills, Simon, Ijaz, Umer Zeeshan and Collins, Gavin (2020) Size shapes the active microbiome of the methanogenic granules, corroborating a biofilm life cycle. mSystems, 5 (5). ISSN 2379-5077

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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.

Item Type: Article
Additional Information: Funding Information: C.Q. was supported by MRC fellowship MR/M50161X/1 as part of the CLoud Infrastructure for Microbial Genomics (CLIMB) consortium MR/L015080/1. U.Z.I. was supported by NERC IRF NE/L011956/1. A.C.T., S.O.S., S.M., and G.C. were supported by a European Research Council starting grant (3C-BIOTECH 261330) and by a Science Foundation Ireland Career Development Award (17/CDA/4658) to G.C. A.C.T. was further supported by a Thomas Crawford Hayes bursary from NUI Galway and a Short-Term Scientific Mission grant through the EU COST Action 1302. None of the funding bodies supporting this research had any role in the design of the study, in the collection, analysis, or interpretation of data, or in writing the manuscript. We have no competing interests to declare. Publisher Copyright: Copyright © 2020 Trego et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.
Uncontrolled Keywords: anaerobic digestion,biofilm,community assembly,methanogenic granules,microbial community assembly,microbiology,ecology, evolution, behavior and systematics,biochemistry,physiology,modelling and simulation,molecular biology,genetics,computer science applications,sdg 7 - affordable and clean energy ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 08 Sep 2022 13:30
Last Modified: 21 Oct 2022 01:39
DOI: 10.1128/mSystems.00323-20

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