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Metaproteome Analysis Reveals That Syntrophy, Competition, and Phage-Host Interaction Shape Microbial Communities in Biogas Plants R

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Metaproteome Analysis Reveals That Syntrophy, Competition, and Phage-Host Interaction Shape Microbial Communities in Biogas Plants R Heyer et al. Microbiome (2019) 7:69 https://doi.org/10.1186/s40168-019-0673-y RESEARCH Open Access Metaproteome analysis reveals that syntrophy, competition, and phage-host interaction shape microbial communities in biogas plants R. Heyer1†, K. Schallert1†, C. Siewert2, F. Kohrs1, J. Greve1, I. Maus3, J. Klang4, M. Klocke4, M. Heiermann5, M. Hoffmann2, S. Püttker1, M. Calusinska6, R. Zoun7, G. Saake7, D. Benndorf1,2* and U. Reichl1,2 Abstract Background: In biogas plants, complex microbial communities produce methane and carbon dioxide by anaerobic digestion of biomass. For the characterization of the microbial functional networks, samples of 11 reactors were analyzed using a high-resolution metaproteomics pipeline. Results: Examined methanogenesis archaeal communities were either mixotrophic or strictly hydrogenotrophic in syntrophy with bacterial acetate oxidizers. Mapping of identified metaproteins with process steps described by the Anaerobic Digestion Model 1 confirmed its main assumptions and also proposed some extensions such as syntrophic acetate oxidation or fermentation of alcohols. Results indicate that the microbial communities were shaped by syntrophy as well as competition and phage-host interactions causing cell lysis. For the families Bacillaceae, Enterobacteriaceae,andClostridiaceae, the number of phages exceeded up to 20-fold the number of host cells. Conclusion: Phage-induced cell lysis might slow down the conversion of substrates to biogas, though, it could support the growth of auxotrophic microbes by cycling of nutrients. Keywords: Metaproteomics, Phages, Anaerobic digestion, Anaerobic Digestion Model 1, Phage-host interactions, Microbiomes Background indicating that complete utilization of biomass by the The anaerobic digestion of organic waste and energy microbial community is impeded by so far unknown crops to biogas consisting of methane (CH4) and carbon mechanisms. Missing enzymes for specific biochemical re- dioxide (CO2) constitutes an important renewable actions or high generation times of essential microbial energy source. A multitude of different bacterial and species are discussed as an explanation [2]. In order to de- archaeal species catalyze the different degradation steps termine the specific causes of the low biomass degradation providing energy for biomass growth. efficiency and to develop strategies for increasing biogas In agricultural biogas plants (BGPs), biomass conversion yields, detailed knowledge about the abundances and the into biogas is incomplete. Based on the theoretical gas po- physiology of main microbial groups in the BGPs is re- tential, the conversion of volatile solids (VS) to biogas quired [3]. Overall, anaerobic conditions in BGPs provide from particulate organic matter is only about 30–60% [1] a smaller total energy gain for microorganisms in contrast to aerobic conditions. Furthermore, sequentially ferment- * Correspondence: [email protected] ing bacteria and archaea divide this energy into little †R. Heyer and K. Schallert contributed equally to this work. portions close to thermodynamic limits. The major con- 1 Bioprocess Engineering, Otto von Guericke University, Universitätsplatz 2, version steps carried out by different microbial groups are 39106 Magdeburg, Germany 2Max Planck Institute for Dynamics of Complex Technical Systems, hydrolysis, acidogenesis, acetogenesis, and methanogen- Bioprocess Engineering, Sandtorstraße 1, 39106 Magdeburg, Germany esis. During hydrolysis, extracellular enzymes hydrolyze Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Heyer et al. Microbiome (2019) 7:69 Page 2 of 17 biopolymers such as cellulose, proteins, and lipids into to detect due to their small size and low biomass. Further- their respective monomers. In subsequent acidogenesis, more, only a few phage sequences are known, and the these monomers are fermented to volatile organic acids dynamics of phage-host interaction were only studied for and alcohols, molecular hydrogen (H2), and CO2.Inthe few bacterial and archaeal species. For example, bacteria following acetogenesis, volatile organic acids and alcohols and archaea may defend phage attacks by the expression of are fermented to acetate, H2,andCO2.Fortheconserva- CRISPR proteins, which snip out phage genes from their tion of energy, these secondary fermentation reactions de- own genome [15]. In summary, all these issues impede the pend on subsequent homoacetogenesis or methanogenesis understanding of the microbial communities in BGPs and which both consume H2 changing the thermodynamic hamper process development and optimization. equilibrium towards its products. Finally, methanogenesis is Over the last years, various “omics” studies investigated the production of CH4 from acetate (acetoclastic methano- the taxonomic and functional structure of microbial com- genesis), H2,andCO2 (hydrogenotrophic methanogenesis) munities in BGPs. These studies focused on individual genes as well as from methylated compounds (methylotrophic [16–18], transcripts [19, 20], or used approaches such as methanogenesis) by methanogenic archaea. metagenomics [21–23], metatranscriptomics [24, 25], and So far, the majority of metabolic pathways have been metaproteomics [26–30] to assess the complexity of micro- characterized in pure culture experiments concerning bial communities. In contrast to metagenomics and meta- the involved enzymes and the thermodynamic condi- transcriptomics, the main advantage of metaproteomics is tions [4, 5]. Simplified structured models such as the that expressed enzymes can be detected and quantified. This Anaerobic Digestion Model 1 [6–8] are used for simula- also includes the detection of phages by the identification of tions to assist BGP operation. The Anaerobic Digestion phage proteins. This is in contrast to metagenomics and Model 1 is able to predict experimental results of biogas metatranscriptomics that both study only genes but cannot production and biogas composition based on multiple distinguish between the presence of phages and their steps describing biochemical as well as physicochemical inactive genes incorporated into host cell genomes. processes and the abundance of main microbial groups. The aim of our in-depth metaproteomics study was to However, the Anaerobic Digestion Model 1 does not identify which mechanisms shape the taxonomic and cover more complex biological interactions and mecha- functional composition of microbial communities in nisms such as the metabolic versatility of individual BGPs. Eleven BGPs were investigated at two time points microorganisms, the functional interchangeability of differ- using SDS-PAGE for pre-fractionation of proteins and ent microbial taxa, or the competition and syntrophic in- subsequent liquid chromatography (LC) coupled to a teractions between bacteria and archaea [4]. In particular, high-resolution Orbitrap Elite tandem mass spectrom- the impact of the presence of certain microorganisms as eter (MS/MS). Proteins were identified using the well as their specific metabolic pathways on the overall MetaProteomeAnalyzer software [31]. Subsequently, the process is still poorly understood and not covered by the taxonomic and functional compositions of the microbial Anaerobic Digestion Model 1. For example, syntrophic communities were analyzed. Mapping of identified meta- acetate oxidation is the reversed pathway of homoaceto- proteins to the different metabolic pathways confirmed genesis [9]. Depending on the conditions, the thermo- the Anaerobic Digestion Model 1 and revealed some dynamic equilibrium between CO2,H2, and acetate is indications for additional metabolites pathways such as shifted preferring either syntrophic acetate oxidation or syntrophic acetate oxidation and microbial interactions. homoacetogenesis [10]. Finally, competition may also have In particular, the presence of phages and antimicrobial a major effect on the taxonomic and functional compos- peptides and proteins was detected. Most likely both influ- ition of microbial communities. For example, species of the ence the microbial biomass turnover and are discussed archaeal family Methanosaetaceae possess enzymes with a regarding their impact on the microbial community and high acetate affinity and may suppress other acetate- on the process model. consuming microorganisms [11]. However, competition is not limited to substrates. For example, certain microbial Results species may kill other species by the expression of bacte- Operation parameters confirm stable operation of biogas riocins, which lyse or inhibit their competitors [12]. plant operation Another recent finding is the presence of phages shaping In this study, seven large-scale BGPs constructed as the microbial communities in anaerobic digestion [13, 14]. continuous stirred-tank reactors (CSTR) encompassing a Replication of phages results in the lysis of host microor- reactor volume range of 1100–3000
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