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Unexpected Metabolic Versatility Among Type II Methanotrophs in the Alphaproteobacteria

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Biol. Chem. 2020; 401(12): 1469–1477 Minireview Anna Hakobyan and Werner Liesack* Unexpected metabolic versatility among type II methanotrophs in the Alphaproteobacteria https://doi.org/10.1515/hsz-2020-0200 greenhouse gas in the atmosphere with a 20-year global Received May 30, 2020; accepted August 4, 2020 warming potential (GWP20) 84 times greater than CO2 (Allen 2016). With its current atmospheric concentration of Abstract: Aerobic methane-oxidizing bacteria, or meth- 1.87 ppmv, CH4 contributes approx. 15% to the total green- anotrophs, play a crucial role in the global methane cycle. house effect (Saunois et al. 2016). Therefore, the methane Their methane oxidation activity in various environmental cycle is one of the most important biogeochemical processes settings has a great mitigation effect on global climate in the Earth’s system. Starting from the industrial era, but in change. Alphaproteobacterial methanotrophs were among particular over the past 15 years, the atmospheric concen- the first to be taxonomically characterized, nowadays uni- tration of methane has significantly increased, thereby Methylocystaceae Beijerinckiaceae fied in the and families. leading to an imbalance in the global methane budget (Allen Originally thought to have an obligate growth requirement 2016; Saunois et al. 2016). This budget is defined by the for methane and related one-carbon compounds as a source methane sources and sinks on which the aerobic methane- of carbon and energy, it was later shown that various oxidizing bacteria, or methanotrophs, have a major impact. alphaproteobacterial methanotrophs are facultative, able to Methanotrophs are a subset of a physiological group grow on multi-carbon compounds such as acetate. Most known as methylotrophs, microorganisms that grow on recently, we expanded our knowledge of the metabolic one-carbon compounds such as methanol and methylated versatility of alphaproteobacterial methanotrophs. We amines. A common characteristic of all aerobic methano- Methylocystis showed that sp. strain SC2 has the capacity for trophs is their ability to oxidize methane to carbon dioxide mixotrophic growth on H2 and CH4. This mini-review will and water with the formation of methanol, formaldehyde, summarize the change in perception from the long-held and formate as intermediates. Methanol, formed from ’ paradigm of obligate methanotrophy to today s recognition methane, is subsequently oxidized to formaldehyde by the of alphaproteobacterial methanotrophs as having both methanol dehydrogenase located in the periplasmic space facultative and mixotrophic capabilities. of the cell. Most of the reducing equivalents for energy Keywords: acetate; hydrogen; hydrogenase; methano- conservation and growth are formed by the oxidation of trophs; pMMO; sMMO. formaldehyde to formate and finally to carbon dioxide. Alternatively, formaldehyde may be assimilated into cell carbon or used as a precursor for synthesis of key in- Introduction termediates of the central carbon metabolism (Dedysh and Knief 2018; Bodelier et al. 2019). Methanotrophic bacteria are found in three phyla: Pro- Methane (CH4) is the most abundant organic compound in teobacteria Verrucomicrobia the Earth’s atmosphere, and it is the second most important , , and candidate phylum NC10. While the first methanotroph was isolated early last century (Söngen 1907), it needed additional 60 years until Whitten- bury et al. (1970) characterized over 100 methanotroph iso- *Corresponding author: Werner Liesack, Research group Proteobacteria “Methanotrophic Bacteria and Environmental Genomics/ lates that later were shown to belong to the . Transcriptomics”, Max Planck Institute for Terrestrial Microbiology, This pioneering work, but also their ubiquitous distribution, Karl-von-Frisch-Str. 10, D-35043, Marburg, Germany, made proteobacterial methanotrophs to the most well- E-mail: [email protected]. https://orcid.org/0000- studied methane oxidizers. They will be discussed in 0002-9533-1552 greater detail below. Another 40 years had to pass before the Anna Hakobyan, Research group “Methanotrophic Bacteria and Environmental Genomics/Transcriptomics”, Max Planck Institute for known diversity of methane-oxidizing bacteria was Terrestrial Microbiology, Karl-von-Frisch-Str. 10, D-35043, Marburg, expanded beyond Proteobacteria. Methanotrophs in the Germany phylum Verrucomicrobia are specialized on living in Open Access. © 2020 Anna Hakobyan and Werner Liesack, published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 1470 A. Hakobyan and W. Liesack: Metabolic versatility of type II methanotrophs extremely acidic (pH 1.8–5.0) geothermal (up to 82 °C) sites, contribute to atmospheric methane oxidation (Figure 1). In as deduced from their habitat preferences. Members of the fact, high-affinity methanotrophs act as a biological sink for candidate phylum NC10 or, more specifically, cells of ‘Can- 28–38 Tg per year of atmospheric methane (Allen 2016; didatus Methylomirabilis oxyfera ’ carry out a nitrite- Saunois et al. 2016). The moderately acidophilic type IIb dependent anaerobic oxidation of methane by the intracel- methanotrophs of the family Beijerinkiaceae differ from type lular formation of oxygen through dismutation of two NO IIa methanotrophs in a number of cellular characteristics. molecules to N2 and O2. The intracellularly formed oxygen is For example, cells of Methylocella and Methyloferula do not used for oxidizing methane along the pathway known for possess ICMs, while in Methylocapsa, the ICMs are always conventional aerobic methanotrophs. Thus, “Ca. Methyl- located on one side of the cell (Dedysh et al. 2000; Vorobev omirabilis oxyfera” ismorelikelya crypticaerobe rather than et al. 2011). Furthermore, some members of the family Bei- a strict anaerobe, albeit residing in anoxic environments. jerinckiaceae contain, in addition to the serine pathway, the Unlike proteobacterial methanotrophs, which prefer to complete set of genes for the CBB cycle, though the func- assimilate carbon from reduced forms of C1 carbon, Verru- tional role remains unclear (Khmelenina et al. 2018). Since comicrobia and NC10 methanotrophs are autotrophs that use the first detailed methanotroph characterization in 1970, it methane only as energy source. These bacteria fix carbon was a long-held paradigm that proteobacterial methano- from carbon dioxide using the Calvin–Benson–Bassham trophs are defined by their obligate use of methane and (CBB)cycle(Khademetal.2011;Rasigrafetal.2014).Formore related one-carbon compounds as sole source of carbon and detailedinformation,wereferto(Opden Camp etal.2018)for energy. Research over the last two decades, however, has Verrucomicrobia methanotrophs and to (Ettwig et al. 2010; revealed that alphaproteobacterial methanotrophs are Versantvoort et al. 2018) for “Ca. Methylomirabilis oxyfera”. metabolically more versatile and have the ability for facul- Proteobacterial methanotrophs act as a natural biofilter tative growth (Figure 1). Most recently, we showed that these in diverse methanogenic environments, such as peat bogs, bacteria are also capable of growing mixotrophically on H2 rice paddies, freshwater sediments, and landfills. Inhabiting and CH4 (Figure 2) (Hakobyan et al. 2020). The following the oxic-anoxic interfaces, methanotrophs reoxidize 10 to sections will be devoted to how our perception on alphap- 90% of the methane produced by methanogenic archaea roteobacterial methane oxidizers changed from being obli- before its emission to the atmosphere. Proteobacterial gate methanotrophs towards having capabilities to grow methanotrophsformphylogeneticallydistinct groupswithin facultatively and mixotrophically. the Gammaproteobacteria (type Ia, type Ib, and type Ic) and Alphaproteobacteria (type IIa and typeIIb) (Knief 2015). Type I and type IIa methanotrophs have been historically differ- entiated by a set of characteristic features (Hanson and Biochemistry of obligate methane Hanson 1996) of which, apart from phylogenetic affiliation, only a very few are still considered valid (Knief 2015). In oxidation principle, type I methanotrophs use the ribulose mono- phosphate pathway (RuMP) for the assimilation of carbon The methane monooxygenase (MMO) enzyme, which is into cell biomass. Their cells contain intracytoplasmic only produced by methanotrophic bacteria, catalyzes the membranes (ICMs) organized in the form of stacks of flat- oxidation of methane to methanol. This enzyme exists in tened vesicles that fill most of the cytoplasmic space and are two forms, a particulate form (pMMO) and a soluble form oriented perpendicular to the cell membrane. In contrast, (sMMO). Both evolutionarily distinct forms of MMO require type IIa methanotrophs of the genera Methylocystis and an input of two electrons and two protons for the methane Methylosinus (Methylocystaceae) use the serine pathway for oxidation step. For sMMO, the possible source of electrons carbon assimilation. They possess the ethylmalonyl- is NADH/H+ (Semrau et al. 2010). In Gammaproteobacteria coenzyme A (EMC) pathway for glyoxylate regeneration methanotrophs, pMMO activity is directly coupled to the and an assimilatory network through which a substantial oxidation of methanol to formaldehyde (Kalyuzhnaya et al. fraction of methane-oxidation derived CO2 is incorporated 2015). The mechanism is different in Alphaproteobacteria back into the serine/EMC pathway (Yang et al. 2013). The methanotrophs. Here, the electrons for pMMO activity are ICMs of
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