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Methanogens: Biochemical Background and Biotechnological Applications Franziska Enzmann1, Florian Mayer1 , Michael Rother2 and Dirk Holtmann1*

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Methanogens: Biochemical Background and Biotechnological Applications Franziska Enzmann1, Florian Mayer1 , Michael Rother2 and Dirk Holtmann1* Enzmann et al. AMB Expr (2018) 8:1 https://doi.org/10.1186/s13568-017-0531-x MINI-REVIEW Open Access Methanogens: biochemical background and biotechnological applications Franziska Enzmann1, Florian Mayer1 , Michael Rother2 and Dirk Holtmann1* Abstract Since fossil sources for fuel and platform chemicals will become limited in the near future, it is important to develop new concepts for energy supply and production of basic reagents for chemical industry. One alternative to crude oil and fossil natural gas could be the biological conversion of ­CO2 or small organic molecules to methane via metha‑ nogenic archaea. This process has been known from biogas plants, but recently, new insights into the methanogenic metabolism, technical optimizations and new technology combinations were gained, which would allow moving beyond the mere conversion of biomass. In biogas plants, steps have been undertaken to increase yield and purity of the biogas, such as addition of hydrogen or metal granulate. Furthermore, the integration of electrodes led to the development of microbial electrosynthesis (MES). The idea behind this technique is to use CO­ 2 and electrical power to generate methane via the microbial metabolism. This review summarizes the biochemical and metabolic background of methanogenesis as well as the latest technical applications of methanogens. As a result, it shall give a sufcient overview over the topic to both, biologists and engineers handling biological or bioelectrochemical methanogenesis. Keywords: Methanogens, Genetic tools, Biogas, Microbial electrosynthesis, Electroactivity Introduction process involving methanogens. Tese archaea use CO­ 2 Methanogens are biocatalysts, which have the potential and ­H2 and/or small organic molecules, such as acetate, to contribute to a solution for future energy problems by formate, and methylamine and convert it to methane. producing methane as storable energy carrier. Te very Although the electrochemical production of methane is diverse archaeal group of methanogens is characterized still more energy efcient than the biological production by the ability of methane production (Balch et al. 1979). [below 0.3 kWh/cubic meter of methane (0.16 MPa, Bär Te fammable gas methane is considered to be a suit- et al. 2015)], the biological conversion may be advanta- able future replacement for fossil oil, which is about to geous due to its higher tolerance against impurities (H­ 2S be depleted during the next decades (Ren et al. 2008). and ­NH3) within the educt streams, especially if ­CO2 rich Methane can be used as a storable energy carrier, as fuel waste gas streams shall be used (Bär et al. 2015). Apart for vehicles, for the production of electricity, or as base from that, research is going on to increase the energy ef- chemical for synthesis and many countries do already ciency of the biological process, so that it might be the have well developed natural gas grids (Ren et al. 2008). In preferred way of methane production in the future (Bär terms of the necessary transition from chemical to bio- et al. 2015). Biological methanation occurs naturally in logical processes, methanotrophic bacteria can use meth- swamps, digestive systems of animals, oil felds and other ane as a carbon and energy source to produce biomass, environments (Garcia et al. 2000) and is already com- enzymes, PHB or methanol (Strong et al. 2015; Ge et al. monly used in sewage water plants and biogas plants. 2014). Te biological methanation is the main industrial New applications for methanogens such as electrometh- anogenesis are on the rise, and yet, there is still a lot of basic research, such as strain characterization and devel- *Correspondence: [email protected] opment of basic genetic tools, going on about the very 1 DECHEMA Research Institute, Industrial Biotechnology, Theodor‑Heuss‑Allee 25, 60486 Frankfurt am Main, Germany diverse, unique group of methanogens (Blasco-Gómez Full list of author information is available at the end of the article et al. 2017). Tis review will summarize important © The Author(s) 2018. 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. Enzmann et al. AMB Expr (2018) 8:1 Page 2 of 22 facts about the biological properties and possibilities of in a depth of 2000 m (Kurr et al. 1991). From a saline lake genetic modifcation of methanogenic organisms as well in Egypt the halophilic methanogen Methanohalophilus as the latest technical applications. It shall therefore give zhilinae was cultured (Mathrani et al. 1988). But metha- an overview over the applicability of methanogens and nogens also colonize non-extreme environments. Tey serve as a start-up point for new technical developments. can be isolated from anoxic soil sediments such as rice felds, peat bogs, marshland or wet lands. For example, Biochemical and microbial background Methanoregula boonei was obtained from an acidic peat Methanogens are the only group of microorganisms on bog (Bräuer et al. 2006, 2011) and several strains of Meth- earth producing signifcant amounts of methane. Tey anobacterium as well as Methanosarcina mazei TMA are unique in terms of metabolism and energy conserva- and Methanobrevibacter arboriphilus were isolated from tion, are widespread in diferent habitats and show a high rice felds (Asakawa et al. 1995). diversity in morphology and physiological parameters. Some methanogens can also associate with plants, animals and could be found in the human body. Metha- Phylogeny and habitats of methanogens nobacterium arbophilicum could be isolated from a tree For decades known methanogenic archaea belonged wetwood tissue and uses the H2 resulting from pectin exclusively to the phylum Euryarchaeota. Tere, metha- and cellulose degradation by Clostridium butyricum for nogens were classifed frst into fve orders, namely methanogenesis (Schink et al. 1981; Zeikus and Henning Methanococcales, Methanobacteriales, Methanosarci- 1975). From the feces of cattle, horse, sheep and goose nales, Methanomicrobiales and Methanopyrales (Balch the methanogens Methanobrevibacter thaueri, Metha- et al. 1979; Stadtman and Barker 1951; Kurr et al. 1991). nobrevibacter gottschalkii, Methanobrevibacter woli- Between the years 2008 and 2012 another two orders of nii and Methanobrevibacter woesei have been isolated, methanogens, namely Methanocellales (Sakai et al. 2008) respectively (Miller and Lin 2002). In addition, diferent and Methanomassiliicoccales (Dridi et al. 2012; Iino Methanobrevibacter species could be found in the intes- et al. 2013), were added to the phylum Euryarchaeota. tinal tract of insects such as termites (Leadbetter and Hydrogenotrophic methanogenesis from H2 and CO2 is Breznak 1996). Beside the intestinal tract of herbivorous found in almost all methanogenic orders with the excep- mammals also the rumen contains methanogens. One of tion of the Methanomassiliicoccales. Due to its broad the major species here is Methanobrevibacter ruminan- distribution it is postulated that this type of methano- tium (Hook et al. 2010). Methanogenic archaea are also genesis is the ancestral form of methane production present in the human body. Methanobrevibacter smithii (Bapteste et al. 2005). Methane formation from acetate, and Methanosphaera stadtmanae as well as Methano- called aceticlastic methanogenesis, can be found only in massiliicoccus luminyensis could be detected in human the order Methanosarcinales. In contrast to that, meth- feces (Dridi et al. 2009, 2012; Miller et al. 1982). Further ylotrophic methanogenesis, which is the methane for- Methanosarcina sp., Methanosphaera sp. and Metha- mation from diferent methylated compounds such as nobrevibacter oralis were discovered in human dental methanol, methylamines or methylated thiols, is found plaque (Belay et al. 1988; Ferrari et al. 1994; Robichaux in the orders Methanomassiliicoccales, Methanobacteri- et al. 2003). ales and Methanosarcinales. Extensive recent metagen- Methanogens can be also found in non-natural habi- omic analyses suggested that methanogens may no tats such as landfills, digesters or biogas plants. There, longer restricted to the Euryarchaeota. Two new phyla, the microbial community varies with the substrate. In namely the Bathyarchaeota (Evans et al. 2015) and the biogas plants, due to hydrolysis of complex polymers Verstraetearchaeota (Vanwonterghem et al. 2016) were to sugars and amino acids, followed by fermentation postulated. Genome sequences from both phyla indicate and acetogenesis, acetate, H2 and CO2 is produced as a methylotrophic methane metabolism in these -as of yet substrates for methanogenesis. Therefore, hydrogeno- uncultivated- potential methanogens. trophic and aceticlastic methanogens are prevalent Methanogens are a relative diverse group of archaea in mesophilic biogas plants, often dominated by spe- and can be found in various anoxic habitats (Garcia et al. cies of Methanosarcina (Methanothrix at low acetate 2000). For example, they can be cultured from extreme concentrations) or Methanoculleus (Kern et al. 2016b; environments such as hydrothermal vents or saline lakes. Karakashev et al. 2005; Lucas et al. 2015; Sundberg Methanocaldococcus jannaschii was isolated from a white et al. 2013).
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