Diversity of Methane-cycling Microorganisms in Soils and Their Relation to Oxygen

Claudia Knief*

Institute of Crop Science and Resource Conservation – Molecular Biology of the Rhizosphere, University of Bonn, Bonn, Germany. *Correspondence: [email protected] htps://doi.org/10.21775/cimb.033.023

Abstract Introduction Microorganisms are important players in the Methane cycling microorganisms are of interest global methane cycle. Anaerobic methanogenic for microbiologists since more than a century. archaea are largely responsible for methane pro- Research on these microorganisms was initially duction, while aerobic methanotrophic bacteria, largely driven by the curiosity to understand their as well as anaerobic methanotrophic bacteria particular physiology that leads to the production and archaea, are involved in methane oxidation. or consumption of methane. While this interest is In anoxic wetland soils, methanogens produce still a driver, the importance of methane as green- methane, while methanotrophs act as a flter house gas has become another important factor, and reduce methane emissions. In the predomi- promoting further research on methanogenic and nantly oxic upland soils, aerobic methanotrophs methanotrophic microorganisms. Tis leads to a oxidize atmospheric methane. Tis review gives continuously beter understanding of their physi- an overview of the diversity of methanogenic ology and ecology, and it becomes evident that and methanotrophic microorganisms, highlights the processes of microbial methane production recent discoveries and provides information and consumption are mediated by more com- concerning their occurrence in soils. Recent plex functional guilds than initially thought. Te fndings indicate that the methanogenic and improved understanding is not only due to the con- methanotrophic lifestyles are more widespread stantly increasing diversity of methanogenic and in microorganisms than previously thought, and methanotrophic microorganisms (e.g. Knief, 2015; that the metabolic versatility of some methane- Kallistova et al., 2017); additionally, the metabolic cycling organisms is broader than known from versatility of these organisms appears to be much well-characterized cultivated organisms. It also broader than previously thought. Tis became turned out that the control of methanogenic most evident during the last two decades, based and methanotrophic bacteria by oxygen is more on the study of enrichment cultures and isolates complex than previously thought. Te implica- representing novel lineages of methanogens and tions this fnding may have for the life of these methanotrophs, several of them with properties that microorganisms in soils and on soil methane have not been observed before in these organisms fuxes is discussed. (Welte, 2018). Te use of new high-throughput

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approaches for the analysis of organisms in culture atmospheric methane concentration was estimated or in situ, e.g. by deep metagenomic sequencing to be 7 ppb, afer emissions had transiently declined and the analysis of reconstructed genome informa- at the beginning of the 21st century (Dlugokencky, tion from individual organisms or near isogenic 2018). Te reasons for this increase are under dis- strains, allows the detection of methanogenic and cussion, but a contribution of biogenic emissions, methanotrophic potential in already known or probably due to agricultural activities, appears new microbial taxa (Chistoserdova, 2015). Tis likely (Saunois et al., 2016b). has resulted in the discovery of methanogenic and Increasing atmospheric methane concentrations methanotrophic pathways in organisms that were are critical, because methane is the most important

not known before to represent methanogens or greenhouse gas afer carbon dioxide (CO2), con- methanotrophs. Important for methane production tributing approximately 20% to global warming or uptake in an ecosystem is not only the presence (Dlugokencky et al., 2011; Kirschke et al., 2013). of methanogenic and methanotrophic organisms, Tis is related to its stronger global-warming poten- but also their activity. Both presence and activity tial, which is currently estimated to be 28 times

are largely controlled by diverse abiotic and biotic stronger compared with CO2 (Myhre et al., 2013). factors. Recent fndings indicate that a strict catego- Methane has a rather short lifetime of approxi- rization of the diverse organisms concerning their mately 9 years in the atmosphere (Saunois et al., responses to specifc environmental factors may not 2016a), so that efective mitigation strategies could always be possible. In the present review, this will lead to near-term reductions in atmospheric con-

be exemplifed focusing on oxygen dependence of centrations and could complement CO2 mitigation methanogenic and methanotrophic microorgan- strategies (Saunois et al., 2016b). Tus, methane isms. Overall, the aims of this review are: is an interesting and important target to reduce global warming processes. However, in order to put 1 provide an update on the global methane mitigation strategies in action, knowledge about the budget and describe the role of soils in global sources and sinks of atmospheric methane and the methane cycling, underlying processes leading to methane produc- 2 provide an update on the diversity of metha- tion and consumption is needed. nogenic archaea, aerobic methanotrophic Global budget calculations are performed based bacteria and anaerobic methanotrophic on diferent modelling approaches and with increas- archaea and bacteria, ing accuracy. For this review, two recent calculations 3 present knowledge about the occurrence of are considered (Kirschke et al., 2013; Saunois et these diferent groups of methane-cycling al., 2016a). According to these studies, the total

organisms in wetland and upland soils, global methane emissions are around 560 Tg CH4/ 4 synthesize present knowledge about oxygen year, while the total sink strength is 550 Tg CH4/ as a major environmental factor controlling year, resulting in an atmospheric growth of approxi-

the occurrence and activity of these groups of mately 10 Tg CH4/year. Tis growth is with very microorganisms. high confdence linked to anthropogenic activities, which have been estimated to contribute about 60% to global emissions (Ciais et al., 2013; Saunois The importance of soils et al., 2016a). as sources and sinks for Focusing on the sources, natural wetlands are atmospheric methane the strongest individual source, contributing with

Methane (CH4) is the most abundant hydrocarbon 25–32% to global emissions (Fig. 2.1). Moreover, in the atmosphere with a current mixing ratio of wetlands are assumed to be the main drivers of 1.85 ppmv (Dlugokencky, 2018). Tis exceeds global inter-annual variability of methane emis- the preindustrial levels of 0.7 ppmv by a factor of sions (Ciais et al., 2013). Estimates for freshwaters approximately 2.5 (Ciais et al., 2013) and is higher (lakes, ponds, rivers, estuaries) show still a high than concentrations recorded in ice cores during uncertainty (Saunois et al., 2016a). Further natu- the past 800,000 years (Loulergue et al., 2008). ral sources are of geological or oceanic origin or From 2007 to 2017, the average yearly increase in from animals (all ≤ 5%). Anthropogenic sources

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Saunois et al. 2016 Kirschke et al. 2013

Figure 2.1 Sources and sinks of atmospheric methane. Data were taken from two recent publications, in which emissions were estimated from 2000 to 2009 (Kirschke et al., 2013) and 2003 to 2012 (Saunois et al., 2016a) based on diferent modelling approaches. Kirschke et al. (2013) presents data as provided in the IPCC report 2013. Diferent sinks were not resolved by Saunois et al. (2016a). of atmospheric methane contribute between 50% they can be diferentiated based on the underly- and 60% to the total methane emissions and are ing processes leading to methane formation. predominantly from fossil fuel use and livestock Termogenic, pyrogenic and biogenic sources farming (each approximately 15%), followed by are diferentiated and their source contribution landflls and waste treatment (9%), rice cultiva- can be estimated based on stable isotope analysis tion (5%) and biomass and biofuel burning (5%). (Ciais et al., 2013). Biogenic methane shows the Most of the atmospheric methane is eliminated by strongest isotopic depletion and is the end product chemical reactions in the atmosphere (Fig. 2.1), of organic mater degradation in the absence of whereby the chemical reaction with OH radicals in oxygen or of other oxidants such as nitrate, sulfate the troposphere is the predominant process (84%). or ferric iron. It is produced by methanogenic Moreover, well-aerated soils serve as sink for atmos- microorganisms (Conrad, 1996). Tis process is pheric methane, contributing 4% to atmospheric responsible for methane production in natural wet- methane oxidation (Kirschke et al., 2013). Tese lands, freshwaters, organic waste deposits (landflls, global budget calculations reveal that soils play an waste, manure), rice paddies, ruminants, termites important role, especially as source of atmospheric and wild animals, so that about 69% of the total methane, but also as sink. As sources, natural wet- atmospheric methane originates from the activ- land soils are most relevant, followed by landfll ity of methanogenic microorganisms (Conrad, soils and rice paddies. In contrast, well-aerated 2009). Te presence and activity of methanogens upland soils represent a relevant sink. and therewith methane emissions are controlled by diverse environmental factors in soils, with substrate availability and concentration of oxygen Microbial processes leading to being among the most relevant factors. Tese are methane production to some extent linked to other factors such as the Besides the classifcation of methane sources concentration and type of organic mater, soil redox according to their natural or anthropogenic origin, potential, availability of electron acceptors, or water

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availability and water table. Moreover, temperature, lineages or based on genome reconstructions soil pH, availability of nutrients and trace metals, from metagenomic data, which were obtained salinity, vegetation, fertilizer and manure additions for enrichment cultures of uncultivated groups afect the development of methanogenic com- of methanogens that are merely known from the munities and their activity and therewith methane detection of specifc marker genes in environmental emissions (Dalal and Allen, 2008; Dalal et al., 2008; samples. Tese markers are the 16S rRNA gene or Serrano-Silva et al., 2014). the mcrA gene, which encodes a subunit of methyl coenzyme M reductase. It is the key enzyme of An update on the diversity of all methanogenic microorganisms and of some methanogenic Archaea anaerobic methane-oxidizing Archaea. Te cur- For decades, methane production was atributed to rently known diversity of methanogenic archaea is four specifc classes of methanogenic Euryarchaeota, illustrated in Fig. 2.2. the Methanomicrobia, Methanobacteria, Methano- cocci and Methanopyri. Te taxonomy, ecology and Recently discovered methanogenic taxa physiology of the members of these classes has been within the phylum Euryarchaeota extensively reviewed (Garcia et al., 2000; Conrad, Within the Euryarchaeota diferent new groups 2007; Liu and Whitman, 2008; Tauer and Shima, of methanogens were discovered during the last 2008; Tauer et al., 2008; Ferry, 2010; Nazaries et years. Te well-known rice cluster I (RC-I) organ- al., 2013; Costa and Leigh, 2014; Serrano-Silva et isms, which are important methane producers in al., 2014). Many methanogens grow on hydrogen rice paddies (Lu and Conrad, 2005; Conrad et al., and carbon dioxide as substrates, while members 2006), were brought into culture a decade ago and of the genera Methanosaeta and Methanosarcina are in the meantime represented by three diferent grow on acetate. Te family Methanosarcinaceae is species within the genus Methanocella, i.e. Metha- most versatile, i.e. most members are able to grow nocella paludicola, Methanocella arvoryzae and methylotrophically, for example on methanol or Methanocella conradii, all isolated from rice feld soil methylated compounds (Oren, 2014). Hydrogeno- (Lü and Lu, 2012). trophic and aceticlastic methanogenesis are most Recently, rice cluster II (RC-II) (Großkopf et al., relevant for biogenic methane production (Conrad, 1998) has been characterized in more detail based 2005), and the relative contribution of each of these on reconstructed genome data from a population processes to methane production can vary sub- inhabiting thawing permafrost soil. Te family stantially (Conrad, 1999). Methanogenic archaea name ‘Candidatus Methanoforentaceae’ has been that are typically found in anoxic soils include proposed for this group of organisms, belonging Methanosaetaceae, Methanosarcinaceae (especially to the order Methanocellales (Fig. 2.2) (Mondav Methanosarcina), Methanomicrobiaceae (especially et al., 2014). Similar as the other Methanocellales, Methanoculleus, Methanomicrobium and Methano- ‘Candidatus Methanoforens stordalenmirensis’ genium), Methanoregulaceae, Methanospirillaceae, is predicted to be hydrogenotrophic. It appears to Methanocellaceae, Methanobacteriaceae (especially be an important player in diferent ecosystems, but Methanobacterium and Methanobrevibacter) and especially in cold wetlands (McCalley et al., 2014; ‘Candidatus Methanoforentaceae’ (Garcia et al., Mondav et al., 2014; Kao-Knifn et al., 2015). 2000; Conrad, 2007; Liu and Whitman, 2008). With the description of Methanomassiliicoccus Te candidate status of the family ‘Ca. Methano- luminyensis the frst and currently only metha- forentaceae’ indicates that cultured representatives nogenic isolate of the class Termoplasmata was that underwent a formal description are currently identifed (Dridi et al., 2012). It represents the lacking. new order Methanomassiliicoccales within this class Recent discoveries indicate that the diversity (Iino et al., 2013) and was formerly known as rice and physiological versatility of methanogenic cluster III (RC-III) (Großkopf et al., 1998). Te microorganisms is actually broader than previ- class Termoplasmata is the frst one that harbours a ously thought, as highlighted by Welte (2018) and methanogenic order as well as a non-methanogenic reviewed by Kallistova et al. (2017). Knowledge order. Besides the isolate M. luminyensis, several can- has either been gained due to cultivation of novel didate genera representing Methanomassiliicoccales

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Figure 2.2 16S rRNA gene sequence based phylogenetic tree summarizing the diversity of methanogenic archaea (shown in black) and anaerobic methanotrophic archaea (marked in red). Sequences from type strains and a representative subset of sequences from uncultivated organisms are included in the tree as available in the SSURef_NR99_132_SILVA database. The tree was calculated in ARB using the neighbour joining algorithm with Jukes-Cantor correction and an archaeal flter (1450 nucleotide positions). Sequences were grouped at family level and the diferent orders of methanogenic Euryarchaeota are indicated as far as they have been classifed at order level. For predicted methanogens outside of the phylum Euryarchaeota the candidate phylum name is given. have been characterized based on metagenomic diverse terrestrial habitats such as sediments, land- sequencing of highly enriched cultures, includ- fll leachates, wetland soils, hot springs, permafrost ing ‘Candidatus Methanogranum caenicola’, sediment, and rice paddies (Borrel et al., 2013b; ‘Candidatus Methanomethylophilus alvus’, ‘Candi- Iino et al., 2013; Chojnacka et al., 2015; Lang et datus Methanoplasma termitum’ and ‘Candidatus al., 2015; W. Li et al., 2016; Merkel et al., 2016; Methanomassiliicoccus intestinalis’ (Borrel et al., Söllinger et al., 2016; Winkel et al., 2018). In con- 2013a,b; Iino et al., 2013; Lang et al., 2015). Tese trast to the other methanogenic Euryarchaeota, all methanogens were mostly obtained from the (meta-)genome sequenced Methanomassiliicoccales intestinal tract of humans or animals. 16S rRNA lack the pathway for CO2 reduction to methyl coen- and mcrA gene sequence analyses including those zyme M and gain energy by a hydrogen-dependent from public databases indicate that methanogenic reduction of methanol or methylamines (Lang et Methanomassiliicoccales form two distinct clades, al., 2015; Y. Li et al., 2016; Söllinger et al., 2016). the host-associated and the free-living clade (Paul et Te class Methanonatronarchaeia was only al., 2012; Söllinger et al., 2016; Borrel et al., 2017). recently discovered, including the species Metha- Te free-living clade includes the isolate Methano- nonatronarchaeum thermophilum and ‘Candidatus massiliicoccus luminyensis as well as sequences from Methanohalarchaeum thermophilum’ (Sorokin

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et al., 2018). Tey represent the formerly uncul- the Euryarchaeaota. Reconstructed genomes from tivated halophilic SA1 euryarchaeal group (Eder metagenomic datasets revealed the presence of et al., 2002). As implemented in the names, these methanogenetic pathways in representatives from organisms are adapted to hypersaline and moder- the archaeal candidate phyla ‘Candidatus Bath- ately thermophilic conditions and were obtained yarchaeota’ and ‘Candidatus Verstraetearchaeota’ from soda lakes. Tey are not monophyletic to (Evans et al., 2015; Vanwonterghem et al., 2016). other classes of methanogens, but are most closely Tese are representatives of a group of archaea related to the class Halobacteria. Likewise as the with broad environmental distribution, harbouring Methanomassiliicoccales, these organisms show a species with diverse physiologies and ecological methylotrophic lifestyle, but in this case hydrogen functions, also known as Miscellaneous Crenar- or formate serve as electron donors and diferent chaeotal Group or Group 1.3 archaea (Lloyd, 2015).

C1-compounds such as methanol or methylamines Near-complete genome data from two distinct as acceptor (Sorokin et al., 2017). Tese organisms lineages of ‘Ca. Bathyarchaeota’ were obtained in

lack some genes of the CO2-reduction pathway, samples from formation water of deep coalbed which is relevant for the formation of methane from methane wells in Australia (Evans et al., 2015).

CO2. Te genome-sequenced representatives of ‘Ca. Te uncultivated methanogenic lineage WSA2 Verstraetearchaeota’ were assigned to two new can- (or Arc I), which occurs in a wide range of natural didate genera, i.e. ‘Candidatus Methanomethylicus’ and engineered environments but especially in and ‘Candidatus Methanosuratus’ (Vanwonterghem wastewater treatment plants and marine sediments, et al., 2016). Tey were detected in experimental is meanwhile represented by one candidate genus, anaerobic digesters set up with inocula from dif- proposed based on metagenome sequence analysis ferent natural and engineered anoxic environments of four WSA2 populations, which were obtained with high methane fux (rumen, lake sediment, from methanogenic bioreactors treating wastewater anaerobic digester and lagoon). From the recon- (Nobu et al., 2016). It is referred to as ‘Candidatus structed genomes the authors of both studies Methanofastidiosum methylothiophilus’ and suggested that the organisms are methylotrophic represents a distinct class, ‘Candidatus Methano- methanogens. Remarkably for these organisms is fastidiosa’ (Nobu et al 2016). Likewise, as observed the presence of metabolic pathways that appear in several of the aforementioned new classes and to enable them to carry out fermentation pro-

orders, a complete pathway for CO2 reduction cesses using amino acids, faty acids or sugars as to methane and for aceticlastic methanogenesis substrates, a feature that has not been observed appears to be absent. Instead, these organisms seem among archaeal methanogens. Moreover, Evans et to dependent on hydrogen as electron donor and al. (2015) stated that it might be possible that these methyl groups obtained from demethylation of organisms gain energy from anaerobic oxidation of methylated thiols, e.g. methylsulfde, as electron methane. To further validate these predictions and acceptors. Moreover, no carbon fxation pathway prove the metabolic versatility, it will be necessary was identifed, and a heterotrophic lifestyle with to study these organisms in more detail directly in acetate, malonate or propionate as carbon sources the environment or afer enrichment and, if pos- was proposed for these organisms. Furthermore, sible, isolation of representative strains. A detailed they lack biosynthetic pathways for several amino analysis of the metabolic capabilities appears of acids. Tese peculiarities have likely contributed particular relevance concerning the methane- to the fact that these methanotrophs eluded cycling capabilities of ‘Ca. Bathyarchaeota’, due cultivation so far, likewise as the host-associated to the fnding that mcrA sequences of ‘Candidatus Methanomassiliicoccales. Syntrophoarchaeum’, which are similar to those of ‘Ca. Bathyarchaeota’, encode an MCR-like protein Novel potential methanogenic taxa catalysing the formation of butyl-coenzyme M beyond the phylum Euryarchaeota from butane (Laso-Pérez et al., 2016). Similarly as Besides the isolation of new lineages of methano- the organisms sequenced by Evans et al. (2015), gens within the Euryarchaeota, metagenomic studies ‘Ca. Syntrophoarchaeum’ possesses an almost- point to the existence of methanogens outside complete methanogenesis-related pathway and four

Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Methane-cycling Microorganisms in Soils | 29 complete mcr gene sets, but grows on butane, which mcrA sequences highly similar to those of ‘Ca. is converted to butyl-coenzyme M, in analogy to Verstraetearchaeota’ in metagenomic datasets from the activation of methane to methyl-coenzyme M terrestrial mud volcanoes and palm oil mill efuent by anaerobic methanotrophic arachaea (ANME). point to a broader distribution of these organisms However, formation of methyl-coenzyme M in the (Vanwonterghem et al., 2016). Moreover, mcrA presence of methane was not observed for ‘Ca. Syn- genes of ‘Ca. Verstraetearchaeota’ were found in trophoarchaeum’. Tus, it can at the moment not be geothermal spring sediments and at low abundance excluded that members of the ‘Ca. Bathyarchaeota’ in a boreal lake sediment (McKay et al., 2017; may actually be non-methane alkane oxidizers and Rissanen et al., 2017). Even mcrA gene expres- the involvement in methane production or possibly sion was proven in these studies. Remarkably, no oxidation needs to be carefully proven. corresponding 16S rRNA gene sequences of ‘Ca. Te occurrence of these two archaeal groups Verstraetearchaeota’ were detected in the respec- with methane-cycling potential in nature was fur- tive geothermal spring samples, indicating that ther assessed by screening public databases for the the detected mcrA sequences are either present in presence of 16S rRNA genes in datasets from other another phylogenetic taxon besides ‘Ca. Vertraeter- studies. Sequences being similar to the sequenced achaota’, or that the 16S rRNA gene based primer members of both phyla, ‘Ca. Bathyarchaeota’ and was biased concerning the amplifcation of ‘Ca. ‘Ca. Verstraetearchaeota’ were indeed detected Vertraetearchaota’. Te mcrA genes highly similar to in diferent methane-rich habitats including those of ‘Ca. Bathyarchaeota’ were found in diferent freshwater wetland soils (Vanwonterghem et al., high-methane fux environments, including other 2016; Narrowe et al., 2017). Vanwonterghem et hydrocarbon seep samples, tar sand tailing ponds, al. (2016) concluded that anoxic conditions, high petroleum reservoir sediments, several aquatic methane fuxes and a likelihood for increased con- environments and geothermal spring sediments centrations of methylated compounds are common (Evans et al., 2015; McKay et al., 2017). Several of characteristics of the habitats in which members of these habitats will provide other alkanes such as ‘Ca. Verstraetearchaeota’ are found. Te phylum butane as carbon source, so that the function of this ‘Ca. Bathyarchaeota’ includes diverse non-meth- group of archaea in these habitats remains currently anogenic members, which can even be present in unclear. methanogenic environments (He, Y. et al., 2016; Lazar et al., 2016; Maus et al., 2018), so the mere Methane production in soils under detection of 16S rRNA gene sequences represent- oxic conditions ing this phylum is not indicative for the presence Recent fndings indicate that methane production of potential methane cycling microorganisms. can also occur under oxic conditions, i.e. in upland Conclusions about the presence of these potential soils or wetland soils that become temporarily methane-cycling microorganisms should thus be or partially oxic. However, methanogens have drawn carefully and are most reliable if 16S rRNA long been considered to be strictly anaerobic and gene sequences are found that are highly similar to most of them are known to be sensitive to oxygen those of the genome sequenced methane-cycling (Fetzer et al., 1993; Whitman et al., 2014). Despite organisms. this assumption, methanogenic archaea have been Alternatively to the 16S rRNA gene, the mcrA found in diverse upland soils, including soils from gene is a useful target for the detection of metha- forests, meadows and grasslands, agricultural land, nogenic archaea. Te mcrA gene was detected in savannas, as well as cold and warm desert and sub-/ all reconstructed genomes of ‘Ca. Bathyarchaeota’ alpine ecosystems (e.g. Peters and Conrad, 1995; and ‘Ca. Verstraetearchaeota’ (Evans et al., 2015; Angel et al., 2012; Aschenbach et al., 2013; Praeg Vanwonterghem et al., 2016), with sequences of et al., 2014; Hofmann et al., 2016; Hernández et al., ‘Ca. Bathyarchaeota’ being clearly distinct from 2017; Xie et al., 2017). Moreover, methane produc- those of the methanogenic Euryarchaeota, while tion was observed upon incubation of these soils those of ‘Ca. Verstraetearchaeota’ are quite similar under anoxic conditions, indicating that the activ- to those of other methanogenic Euryarchaeota ity of the methanogenic archaea can be stimulated (Vanwonterghem et al., 2016). Te detection of under appropriate conditions, and some studies

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reported methane production from oxic soils (Teh sequenced methanogenic archaea and revealed that et al., 2005; Kammann et al., 2009). It is assumed the methanogens can be divided into two classes, that the activity of methanogens in these soils those that have accumulated genes involved in is temporally and spatially limited, occurring in oxygen resistance (Methanocellales, Methanomicro- anoxic microniches, which are formed by the soil biales and Methanosarcinales) and those that lack structure or are provided by the soil fauna (Conrad, most of these genes (Methanobacteriales, Methano- 1995; Kammann et al., 2009, 2017). Teir activ- coccales and Methanopyrales) (Lyu and Lu, 2018). ity may support atmospheric methane-oxidizing In agreement with this classifcation, nearly all taxa bacteria, which rely otherwise on the very low con- that were found in upland soils or in wetland soils centrations of atmospheric methane. under oxygen stress conditions belong to the group Molecular analysis revealed that Methanocella with the higher number of antioxidant features in and Methanosarcina were most commonly detected the genome. Similarly, Lyu and Lu (2018) reported in upland soils. Besides, Methanomassiliicoccus, that the taxa with accumulation of antioxidant genes Methanobacterium, Methanosaeta and Methanobre- were more frequently detected in microaerophilic vibacter were repeatedly detected (e.g. Angel et al., or oxic environments, including oceans, rice soils, 2011, 2012; Aschenbach et al., 2013; Hu et al., 2013; subsurface soils, and diverse upland and wetland Praeg et al., 2014; Hofmann et al., 2016; Hernández soils. Teir observation was based on a meta-anal- et al., 2017; Xie et al., 2017). Te activity of these ysis, in which the occurrence of publicly available genera in upland soils remains largely unexplored. 16S rRNA genes was evaluated. Remarkably, the Activity studies of methanogens have only been genera Methanobrevibacter and Methanobacterium, performed in diferent drained wetland soils. In which were detected in some upland soils, do not oxic paddy soil, the same genera, i.e. Methanosaeta, belong to the group of methanogens harbouring Methaosarcina, Methanobacterium and Methano- a diverse set of antioxidant genes. Nevertheless, cella, were shown to be involved in organic mater Methanobrevibacter has been shown to remain degradation in a 13C-labelling experiment (Lee et active in the presence of oxygen, being even able to al., 2012). Other studies with paddy soils revealed reduce oxygen, as long as the concentration does that oxygen exposure resulted in a strong decrease not exceed the capacity for its removal (Tolen et in mcrA gene expression (Yuan et al., 2011; Liu et al., 2007). Tis indicates that the methanogenic al., 2018). Afer the aeration event, several of the archaea must have developed diferent strategies to above mentioned genera showed the best recovery, survive oxic conditions in soils and may contribute i.e. highest mcrA gene expression (Yuan et al., 2011; to methane production even in environments that Reim et al., 2017; Liu et al., 2018). In a freshwater are mostly oxic. Methane production under appar- wetland from a lakeshore, substantial methane pro- ently oxic conditions has not only been observed in duction was reported from the oxygenated soil layer soils, but also in lakes, where methane production and atributed to the activity of ‘Candidatus Metha- was observed in the oxygenated water column, a nothrix paradoxum’ (Angle et al., 2017). Te genus phenomenon that is referred to as ‘the methane name Methanothrix is supposed to replace the genus paradox’ (Grossart et al., 2011; Bogard et al., 2014; name Methanosaeta (Garrity et al., 2011), thus the Tang et al., 2014; Donis et al., 2017). fnding is also in agreement with the observation Besides the activity of methanogenic archaea in concerning the presence of Methanosaeta in upland oxic soils, fungi were recently reported to release soils. Te activity of this methanogen was assumed methane from methionine as precursor and may to be restricted to anoxic microsites within the contribute to methane production (Lenhart et al., overall oxic soil layer. Tis was concluded from the 2012). Moreover, diferent non-biogenic methane fnding that gene expression analyses of the strain production processes are known to occur in soils did not indicate the activation of genes involved in (Wang et al., 2013, 2017). Tese result from deg- oxygen detoxifcation mechanisms, although this radation processes of organic material, including strain possesses a set of such genes. photodegradation, thermal degradation, oxidation Te presence of genes involved in adapta- by reactive oxidation species, extracellular oxidative tion mechanisms to oxidative environments metabolism or inorganic chemical reactions. How- was recently analysed systematically in genome ever, the contribution of these processes to methane

Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Methane-cycling Microorganisms in Soils | 31 emissions in upland soils or aerated wetland soils abundance and activity of these microorganisms remains currently uncertain, but may be rather low (Dalal and Allen, 2008; Dalal et al., 2008; Semrau (Lenhart et al., 2012; Gu et al., 2016; Wang et al., et al., 2010; Aronson et al., 2013; Serrano-Silva et 2017). Te methane-oxidizing bacteria in the soils al., 2014). While the efect of these environmental may be able to metabolize most of this methane factors on methane oxidation rates has been studied before it reaches the atmosphere. Further work is quite intensively, knowledge about the responses of needed to assess the importance of these diferent the microbial groups involved in methane oxida- processes in the diverse continental ecosystems. tion is less advanced.

An update on the diversity of Microbial methane oxidation cultivated aerobic methanotrophic by aerobic methanotrophic bacteria bacteria Aerobic methanotrophic bacteria are found within Biological aerobic methane oxidation is exclu- three bacterial classes, the Alphaproteobacteria, sively performed by bacteria. Te methanotrophic Gammaproteobacteria and Methylacidiphilae, the bacteria, which gain carbon and energy from the later being members of the phylum Verrucomicro- oxidation of methane, inhabit diverse terrestrial, bia. An overview of the currently known diversity aquatic and marine habitats. Terrestrial ecosystems of cultivated methanotrophic bacteria is given that are known to act as sources for atmospheric in the phylogenetic tree (Fig. 2.3). Besides the methane host diverse methane-oxidizing bacteria. classifcation of aerobic methanotrophic bacteria Tese methanotrophic bacteria are found in high based on their phylogeny, grouping into type I Arctic and tundra wetlands, peat bogs, rice pad- (Gammaproteobacteria), type II (Alphaproteobac- dies, landfll covers, sewage sludge and foodplains teria) and sometimes type III (Methylacidiphilae) (Knief, 2015). In these ecosystems, aerobic metha- methanotrophs is quite common, especially in notrophic bacteria usually inhabit the oxic/anoxic cultivation-independent studies. Tis grouping interfaces, where they oxidize the methane that is into diferent types is not meant to encode specifc released by the methanogenic archaea. Te flter phylogenetic information. Te type I methano- capacity of the methanotrophic bacteria can lead trophs are further diferentiated into type Ia to Id to more than 80% reduction in methane emissions, methanotrophs, whereby type Ia and Ib represent especially in oceans, freshwaters and rice paddies, Methylococcaceae, type Ic Methylothermaceae and while the flter efect appears less efcient in wet- type Id an uncultivated lineage of methanotrophs, lands and landfll soils (Conrad, 1996; Reeburgh, defned based on their pmoA sequences (Knief, 2003). 2015). Major characteristics of these methano- In upland soils aerobic methanotrophic bacteria trophs were compiled in recent reviews (Knief, are responsible for atmospheric methane oxidation 2015; Dedysh and Knief, 2018). Tus, the focus (Bender and Conrad, 1992; Dunfeld, 2007; Kolb, in this section will be on recently obtained metha- 2009; Knief, 2015). Tey live on the expense of notrophic isolates that represent new genera of this atmospheric methane and, if available, endog- methanotrophic bacteria and their occurrence in enously produced methane in soil (see previous soils. section). Moreover, some of them may proft from Within the group of methanotrophic Gam- multi-carbon compounds (Pratscher et al., 2011, maproteobacteria, a couple of diferent new isolates 2018). Te presence and activity of methanotrophic or enrichment cultures were recently obtained. bacteria in soils is controlled by diverse environ- Methyloterricola oryzae strain 73aT was isolated from mental factors. As for the methanogenic archaea, the lower part of stems from rice plants and is the substrate availability and concentration of oxygen frst cultured representative of rice paddy cluster 1 are considered to be the most important factors, (RPC1) (Frindte et al., 2017). Te isolate is a typi- while water availability and water table, soil pH, cal member of the Methylococcaceae, most closely availability of nutrients and trace metals (especially related to the genera Methylococcus and ‘Candidatus copper), temperature, salinity, vegetation, ferti- Methylospira’ (Fig. 2.2). RPC1 represents metha- lizer and manure additions will further afect the notrophic bacteria that are frequently detected

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Figure 2.3 16S rRNA gene sequence based phylogenetic tree summarizing the diversity of aerobic methanotrophic bacteria and anaerobic methanotrophic bacteria and archaea. All type strains of validated aerobic methanotrophic species are included as well as methanotrophs that have been described as new species but have not yet been formally validated (names are hyphenated). Moreover, methanotrophs with candidate status are included, which are mostly available as enrichment culture, but not as pure culture isolates. This rules out their validation as new species based on current regulations. The tree was calculated in ARB using the neighbour joining algorithm with Jukes-Cantor correction and a bacterial flter (1565 nucleotide positions). Shorter sequences were added using the ARB parsimony quick-add tool. The assignment of the strains to diferent families is indicated as far as a classifcation at this taxonomic rank has been done.

Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Methane-cycling Microorganisms in Soils | 33 in rice paddies, but also in aquatic ecosystems appears to colonize predominantly diferent aquatic and wetlands (Knief, 2015). Te cluster has been and wetland ecosystems. Moreover, it was found as defned based on the detection of pmoA sequences. a dominant member within the methanotrophic Te pmoA gene encodes a subunit of the particulate community in a lichen-dominated patch of a boreal methane monooxygenase and is the most widely peatland ecosystem (Danilova et al., 2016a). Char- used molecular marker for aerobic methanotrophic acteristic for this genus are the spiral-shaped cells, bacteria due to its presence in the fast majority of which are so far unique among methanotrophs, aerobic methanotrophs (Knief, 2015). and the preference to growth under micro-oxic Te methanotrophic isolate strain Sn10-6 is conditions. Te detection of this genus in diferent proposed to represent a new genus and species, wetlands suggests that a microaerophilic lifestyle ‘Methylocucumis oryzae’ (Rahalkar et al., 2016; along with motility may be an important trait for Pandit et al., 2018). It is distantly related to other this genus to establish a population in peatlands. type Ia methanotrophic bacteria and it was isolated from the rice rhizosphere. Te preferred habitat Recent insights obtained for of this genus remains currently largely unknown, major uncultivated groups of because highly similar 16S rRNA or pmoA gene methanotrophic bacteria sequences are not present in the NCBI nucleotide Besides ‘Candidatus Methylospira mobilis’, which collection database. A more specifc search for exists as enrichment culture and has been described similar sequences (> 95% sequence identity) of in detail, some further taxa of putative methano- these two marker genes in datasets obtained from trophs with Candidatus status have been proposed rice ecosystems via high-throughput amplicon to exist. Tey were characterized based on informa- sequencing resulted in a few hits for both genes in tion from genome reconstructions derived from two studies (Lee et al., 2015; J. Liu et al., 2017). In metagenomic data. Considering the necessary several other studies analysing paddy soil or the requirements to refer to a taxon as Candidatus, rice rhizosphere, it was not detected despite the these organisms should not be termed Candidatus, higher sensitivity that is achieved when using next likewise as several of the above mentioned metha- generation sequencing technologies (e.g. Lüke and nogens, because limited information is available Frenzel, 2011; Knief et al., 2012; Ahn et al., 2014; concerning structural, metabolic or reproductive Vaksmaa et al., 2017c; Shiau et al., 2018). Such a features. In some cases, a nearly complete 16S rRNA rare detection of a newly isolated genus in cultiva- sequence is also lacking, although the availability tion-independent studies has previously been seen of this sequence is currently another prerequisite for a few other genera, mostly from marine environ- for taxa with Candidatus status according to taxo- ments (Knief, 2015). Te relevance of these genera nomic rules (Murray and Stackebrandt, 1995). All for global methane cycling remains thus largely groups of uncultivated methanotrophs that include unclear. a recently described strain or an uncultivated but Another new candidate genus representing genome sequenced representative are compiled in methanotrophic Gammaproteobacteria, ‘Candidatus Table 2.1. Methylospira’, could not yet be obtained in pure culture and has therefore the ‘Candidatus’ status Upland soil cluster α (USCα) and MHP (Danilova et al., 2016b). It was enriched from clade a Sphagnum dominated peat bog and is a repre- Te best-described group of uncultivated aerobic sentative of the pmoA OSC cluster, which is closely methanotrophic organisms is USCα, which is related to RPC I, as refected by the relatedness known as major player involved in atmospheric of the 16S rRNA gene sequences of ‘Candidatus methane oxidation in upland soils (Dunfeld, Methylospira mobilis’ and Methyloterricola oryzae 2007; Kolb, 2009; Knief, 2015). For a genome (Fig. 2.3). Sequences of this cluster were detected analysis of this group of methanotrophs, cells were in diferent fen and bog ecosystems, but also in obtained upon artifcial enrichment from forest an organic-rich and a mineral soil. Te study of soil samples known to harbour these organisms as Danilova et al. (2016b) reported its presence in dominant group of methanotrophs (Pratscher et al., diferent freshwater and lake sediments, thus it 2018). Phylogenetic placement of the 16S rRNA

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Table 2.1 Recent insights obtained for major pmoA and pmoA-like sequence clusters pmoA/amoA sequence cluster Gained knowledge Predominant habitat Reference RPC1 Isolate Methyloterricola oryzae strain Rice paddies and Frindte et al. (2017) 73aT characterized, member of the aquatic habitats Methylococcaceae OSC Enrichment culture ‘Candidatus Methylospira Peat bogs Danilova et al. (2016b) mobilis’ characterized, member of the Methylococcaceae USCα Genome reconstruction of a representative Upland soils, caves Pratscher et al. (2018) organism, member of the Beijerinckiaceae, and lava tubes proposition of the name ‘Candidatus Methyloafnis lahnbergensis’ USCα, MHP clade Genome reconstruction of two representative Peatlands Singleton et al. (2018) organisms, member of the Beijerinckiaceae USCγ Genome reconstruction of a Upland soils, caves Edwards et al. (2017) representative organism, member of the and lava tubes Gammaproteobacteria LWs Genome reconstruction of a representative Aquatic habitats Rissanen et al. (2018) organism, member of the Methylococcaceae, proposition of the name ‘Candidatus Methyloumidiphilus alinensis’ Crenothrix (pmoA/ Sequence cluster with ‘unusual pmoA’ of Diverse terrestrial Van Kessel et al. (2015), amoA) Crenothrix represents amoA sequences of and aquatic habitats Daims et al. (2015), Nitrospira species capable of comammox; Oswald et al. (2017) Crenothrix harbour gammaproteobacterial pmoA gene sequences

gene sequence and multi-locus sequence analyses name ‘Candidatus Methyloafnis lahnbergensis’ for indicated that this methanotroph represents a new this group of organisms. genus within the family Beijerinckiacea, most closely Two further reconstructed genomes for USCα related to Methylocapsa species, as already assumed organisms were obtained from metagenomic data based on pmoA gene sequence analysis (Fig. 2.4) from permafrost soils (Singleton et al., 2018). and pmo operon analyses (Ricke et al., 2005). Fur- Here, the USCα methanotrophs appeared to be thermore, genome analysis revealed the presence of the predominant methanotrophs in palsa and were

a complete set of genes needed for C1 metabolism also abundant in the thawed bog samples. Te and confrmed the possibility to grow on acetate palsa was mainly oxic and methane production was as carbon source, as already proposed in an earlier reported to be minimal (McCalley et al., 2014), so study based on stable isotope incorporation with that atmospheric methane oxidation by USCα is acetate as carbon substrate (Pratscher et al., 2011). conceivable, while the detection of USCα in a bog With the availability of a frst known 16S rRNA sample is rather uncommon for USCα sequence gene sequence of USCα, the global distribution of types, with the exception of the MHP clade. Te this organism was reassessed, largely confrming MHP clade is a subgroup within the large USCα pmoA-based fndings, i.e. the recovery from diverse cluster, which is typical for peatlands (Knief, 2015). upland soils, in particular forest soils. Interestingly, Indeed, the most closely related pmoA sequences of highly similar 16S rRNA sequences were also recov- the USCα contigs given in the study of Singleton ered from subterranean environments, including et al. (2018) indicate that their USCα genomes caves and lava tubes, where they contributed up represent this MHP clade. Tus, they represent a to 10% to the bacterial community composition, distinct subgroup of USCα methanotrophs com- while this is ≤ 1% in upland soils (Kolb et al., 2003; pared to the organisms analysed by Pratscher et al. Pratscher et al., 2018). Te authors propose the (2018). Analysis of the two reconstructed genomes

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Figure 2.4 Phylogenetic tree showing the diversity of cultured methanotrophs and defned clusters of uncultivated aerobic methanotrophic bacteria based on pmoA gene sequence analysis. A backbone tree was used as presented earlier (Knief and Dedysh, 2018) and updated with sequences of recently published novel groups of methanotrophs using the ARB parsimony quick-add tool. The diferent groups of methanotrophic bacteria are labelled according to their grouping into type I to type IV.

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confrmed the relationship of these USCα metha- of this group of organisms was reconstructed notrophs to Methylocapsa species. Furthermore, from metagenomic data obtained from a mineral the presence of genes for pXMO homologue cryosoil sample. Only a partial 16S rRNA gene and a lanthanide-dependent XoxF-type methanol sequence is available, which indicates that USCγ dehydrogenase as well as the absence of genes methanotrophs are members of the class Gam- for a calcium-dependent MxaFI-type methanol maproteobacteria (Fig. 2.3). In the SILVA database dehydrogenase, which were reported by Pratscher used for tree reconstruction, the sequence clusters et al. (2018), were confrmed in this study based most closely to sequences of uncultured organ- on both genomes. Additionally, Singleton et al. isms, which form a branch separate from known (2018) report the presence of hydrogenase genes families of Gammaproteobacteria. Interestingly, and genes involved in carbon monoxide oxida- these closely related 16S rRNA sequences from tion, suggesting further metabolic versatility of environmental samples indicate its presence in these organisms besides a potential for growth caves and lava tubes, likewise as reported for on acetate. A hydrogenotrophic lifestyle was just USCα. Besides, some sequences were recovered recently reported for methanotrophic Verrucomi- from soils, especially from cold ecosystems. Tis crobia (Carere et al., 2017; Mohammadi et al., is in agreement with the detection of the USCγ 2017). Te presence and activity of hydrogenases pmoA sequences, which were predominantly in methanotrophs is known since a long time (e.g. found in pH neutral and alkaline soils, and in Chen and Yoch, 1987; Hanczár et al., 2002). Tey soils from cold or dry ecosystems (Knief, 2015). were assumed to contribute to the generation Carbon assimilation of this group of organisms of reductants, e.g. for methane monooxyge- remains currently enigmatic, as neither a complete nase, but not considered to allow growth under ribulose monophosphate pathway nor a complete chemolithotrophic conditions, which demands a serine cycle was reconstructed from the available

pathway for CO2 fxation. Tus, it may only be genomic data. Te presence of Calvin cycle genes, an option for those type Ib methanotrophs that which could be another alternative for carbon possess the capability to assimilate carbon via the assimilation, was not evaluated by Edwards et al. Calvin cycle. While Pratscher et al. (2018) could (2017). not reconstruct a complete Calvin cycle for their organism, Singleton et al. (2018) report the pres- Lake Washington cluster (LWs) ence of all relevant genes. As in other examples, Another methanotrophic organism, proposed the relevance of this predicted metabolic capability as ‘Candidatus Methyloumidiphilus alinensis’, remains to be proven. Similarly, the involvement has recently been described based on genome of the MHP clade in atmospheric methane oxida- reconstructions from a metagenomic dataset, tion has not yet been demonstrated. Te study of which was obtained from a small oxygen-stratifed Singleton et al., 2018 included metatranscriptomic humic lake (Rissanen et al., 2018). A 16S rRNA analyses, which did not reveal strong pmoA gene gene sequence is not available from the recon- expression for these methanotrophs, so that the structed genome. Its phylogenetic placement was conditions under which they may be actively assessed based on a genomic comparison includ- involved in methane oxidation in peatlands remain ing a number of diferent genes, which indicated currently unclear. its relatedness to the genome sequenced Methy- loterricola oryzae strain 73aT. However, as other Upland soil cluster γ related organisms such as ‘Candidatus Methy- Likewise as for USCα, a reconstructed genome lospira mobilis’ are not yet genome sequenced, sequence was recently reported for USCγ its exact phylogenetic placement remains vague. (Edwards et al., 2017). Tis pmoA sequence Interestingly, its pmoA sequence indicates that the cluster is also known to be involved in atmos- organism is a representative of the LWs cluster, pheric methane oxidation, but more frequently which contains sequences from several diferent detected in pH neutral upland soils, while USCα studies and is known to represent predominantly is predominant in acidic soils (Knief et al., 2003; methanotrophs that inhabit freshwater lakes Knief, 2015). A draf genome of a representative (Dumont et al., 2014; Knief, 2015).

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The Crenothrix cluster and a re- them obtained from freshwater methane seeps. evaluation of the phylogenetic However, it does not consistently fall into a specifc placement of Crenothrix pmoA well-known cluster of uncultivated methanotrophs. sequences Terefore, it is not highlighted in the phylogenetic A sequence cluster distantly related to pmoA tree in Fig. 2.4, where it is part of lake cluster 1. sequences as well as to amoA sequences of nitrifying Tis inconsistent clustering is explained by a high bacteria has been identifed as Crenothrix cluster, number of sequences with equal similarities to each based on the fnding that pmoA sequences of the other among the type Ia methanotrophs. Tus, methane-oxidizing ‘Candidatus Crenothrix poly- the clustering of sequences varies to some extent spora’ fall into this cluster (Stoecker et al., 2006). in dependence on the dataset and algorithm used However, the identity and metabolic potential of for tree calculation. Tis also explains why the the organisms represented by this sequence cluster combination of sequences into larger clusters as has to be questioned based on two recent fndings. presented in Fig. 2.4 is not in full agreement with First, diferent Nitrospira isolates were identifed trees shown in previous studies (Dedysh and Knief, that possess an amoA gene with a sequence falling 2018; Knief, 2015). Oswald et al. (2017) speculate into this Crenothrix cluster (Daims et al., 2015; that the freshwater lake Crenothrix has acquired van Kessel et al., 2015). Tese Nitrospira species the pmoCAB operon laterally from another metha- oxidize ammonia to nitrate, a process referred to notrophic Gammaproteobacterium, as the operon is as ‘complete ammonium oxidation to nitrate’, or fanked by transposase genes. comammox. Tis fnding suggests that the sequence cluster is representing comammox bacteria of the Evidence for methanotrophs in genus Nitrospira. Second, a recent study reanalysed genera not yet known to include samples from the waterworks sand flter system, in aerobic methanotrophic bacteria which the ‘unusual pmoA’ sequences assigned to Te diversity of methanotrophic Alphaproteobacte- ‘Ca. Crenothrix polyspora’ had initially been found. ria has recently been extended with the discovery Genome reconstructions from metagenomic data of the methanotrophic strain ‘Methyloceanibacter revealed that the system harbours Nitrospira species methanicus’ strain R-67174, a member of the order with the comammox type of amoA sequence, and Rhizobiales (Vekeman et al., 2016). Besides the Crenothrix species with a gammaproteobacterial Methylocystaceae and Beijerinckiacae, it represents a pmoA sequence (Oswald et al., 2017). Such pmoA third group of methanotrophs within this order (the sequences were also detected in the initial study by genus has not yet been classifed at class level). Te Stoecker et al. (2006), but not linked to ‘Ca. Creno- strain was isolated from a marine sediment sample. thrix polyspora’ due to their low abundance. Taken While the genus Methyloceanibacter is known to be together, these fndings indicate that the ‘Creno- methylotrophic, ‘Methyloceanibacter methanicus’ thrix cluster’ represents amoA-like sequences of strain R-67174 is currently the only known metha- comammox organisms, while Crenothrix species notrophic species and strain within this genus. Tis harbour pmoA sequences similar to those of metha- is the frst example of a methanotroph within a non- notrophic Gammaproteobacteria. Tey are actually methanotrophic though methylotrophic genus. Te similar to the pmoA sequences of Methyloglobulus methane oxidation capacity of this strain is realized morosus (Fig 2.4). by the presence of a soluble methane monooxy- Besides the detection of a Crenothrix metha- genase, while genes encoding a membrane bound notroph with a pmoA sequence similar to that of methane monooxygenase, which occurs almost M. morosus, Oswald et al. (2017) reported the consistently among methanotrophic bacteria, are existence of another ‘Ca. Crenothrix polyspora’ absent. Besides Methylocella and Methyloferula, it is organism from a stratifed lake, which has a gam- thus the third genus that possesses only the soluble maproteobacterial pmoA sequence that is only form of the enzyme methane monooxygenase. Te distantly related to sequences of cultivated type mmoX gene, which serves as molecular marker Ia methanotrophs. Instead, its pmoA sequence for methanotrophs harbouring a soluble methane clusters most closely to pmoA sequences of diverse monooxygenase, was related to those of Methylocella uncultivated type Ia methanotrophs, several of and Methyloferula, which are both representatives

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of the methanotrophic Beijerinckiacea. Te authors in wetlands including peat and bog ecosystems. speculate that Methyloceanibacter may have Moreover, 16S rRNA gene sequences related to acquired the genes encoding the soluble methane Rhodomicrobium or Hyphomicrobium were detected monooxygenase by horizontal gene transfer. Te in diferent 13C-methane stable isotope labelling occurrence of the genus Methyloceanibacter appears studies performed in peatlands (Morris et al., 2002; to be largely limited to marine environments, all Gupta et al., 2012; Putkinen et al., 2014; Deng et al., isolates were obtained from marine environments 2016). Owing to the methylotrophic lifestyle real- (Takeuchi et al., 2014; Vekeman et al., 2016), and ized by some members of the Hyphomicrobiaceae, closely related 16S rRNA gene sequences were labelling of these organisms was assumed to be

predominantly detected in marine environments. the result of cross-feeding on partially oxidized C1 Tis is in agreement with the general fnding that compounds in such labelling experiments. most marine methanotrophs are clearly distinct Te results obtained for the Mehyloceanibac- from methanotrophic taxa found in terrestrial or ter isolate and the genome information of the aquatic environments (Knief, 2015; Vekeman et Hyphomicrobiaceae strain suggest that methane al., 2016). Tus, this methanotroph may not play oxidation must be more widespread among the a major role in soil. However, the observation that Alphaproteobacteria than previously thought. As individual methylotrophs gain the capability to for USCα (family Beijerinckiaceae), these organisms oxidize methane by acquiring genes encoding the appear to be metabolically more versatile than the soluble or particulate methane monooxygenase Methylocystaceae, so that their impact on methane may apply to terrestrial microorganisms as well, cycling in an ecosystem cannot yet be assessed, but especially if microorganisms reside in habitats it deserves more detailed studies to evaluate under where methanol as well as methane are available which conditions these organisms may contribute as carbon and energy sources, thus supporting the to the methane oxidation process. Singleton et al. growth of methylotrophic and methanotrophic (2018) reported very weak expression of the genes microorganisms. for methane monooxygenases by the Hyphomicro- Evidence for putative methanotrophic strains biaceae strain, based on metatranscriptomic data. in another non-methanotrophic genus comes from the metagenomic study of Singleton et al. (2018), Oxygen dependence of aerobic in which reconstructed genomes related to the pho- methanotrophic bacteria toheterotrophic Rhodomicrobium spp., members of Methanotrophic bacteria are considered to be the Hyphomicrobiaceae, were reported to harbour obligately aerobic due to their need of oxygen for operons for both, the particulate and soluble meth- respiration and for methane oxidation by the meth- ane monooxygenase. Te pmoA sequences found in ane monooxygenase. However, studies accumulate this group of organisms cluster basal to those of the that report the presence of aerobic methanotrophic Methylocystaceae and Beijerinckiaceae (Fig. 2.4) and Gammaproteobacteria in habitats with very low refect thus the 16S rRNA gene based phylogeny. oxygen concentrations, especially in suboxic and Similarly, the MmoX sequences formed a novel anoxic layers or the sediments of stratifed lakes (e.g. cluster related to the Beijerinckiaceae. Likewise as Biderre-Petit et al., 2011; Blees et al., 2014; Kojima some other alphaproteobacterial methylotrophs, et al., 2014; Crevecoeur et al., 2015; Hernandez et this Hyphomicrobiaceae strain has genes for a thiol- al., 2015; Oswald et al., 2016; Martinez-Cruz et al., dependent pathway for formaldehyde oxidation 2017; Naqvi et al., 2018; Singleton et al., 2018). In and the necessary equipment to perform carbon particular type Ia methanotrophs are consistently assimilation via the Calvin cycle. Furthermore, detected in these studies. More specifcally, these are hydrogenase genes and a complete dissimilatory ofen reported to represent Methylobacter species. A sulphate reduction pathway were identifed, with specifc assignment to the genus Methylobacter may dsr genes similar to those of Rhodomicrobium, in some cases be questionable, because the diferent indicating a broader metabolic versatility also for species of Methylobacter are not forming monophy- this group of organisms. In public sequence data- letic clusters in 16S rRNA and pmoA based trees, bases, its pmoA sequence type was available from so that diverse sequence types exist in public data- a couple of metagenomes, indicating the presence bases that are termed ‘uncultured Methylobacter’.

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Such pmoA sequences cluster with the recently information, assembled from metagenomic data- detected genera Methylovulum and Methylosoma, sets. Te activity and afnity of this oxidase in but are also similar to those of Methylomicrobium aerobic methanotrophic bacteria remains to be and Methylosarcina, or they fall into major groups studied to validate its involvement in adaptation of of uncultivated organisms, representing the pmoA methanotrophs to oxygen-limited conditions. lake cluster or diferent aquatic clusters (Dumont et Furthermore, several aerobic methanotrophs al., 2014; Knief, 2015). Tus, the adaptation to low- have the genetic equipment to perform anaerobic oxygen conditions is most likely not strictly limited respiration by denitrifcation. Methane-dependent to the genus Methylobacter. denitrifcation activity using nitrate or nitrite Focusing on soils, Methylobacter was reported as substrate was reported for ‘Methylomonas to be the dominant active methanotroph with denitrifcans’ and Methylomicrobium album BG8, increasing depth and thus decreasing oxygen con- respectively (Kits et al., 2015a,b) and relevant genes centrations in an arctic peat soil (Tveit et al., 2014). have been found in further gammaproteobacterial Moreover, Methylobacter was the dominant active methanotrophs including Methylobacter or Creno- methanotroph in the anoxic zone just below the thrix (Campbell et al., 2011; Kalyuzhnaya et al., oxic/anoxic interface in a rice paddy soil micro- 2015; Skennerton et al., 2015; Oswald et al., 2017). cosm. Actually, a higher pmoA transcript to gene Moreover, the alphaproteobacterial Methylocystis ratio was observed in the anoxic soil layer com- sp. strain SC2 was shown to perform complete pared with the oxic top soil layer, and highest pmoA denitrifcation from nitrate to dinitrogen under transcription was observed at the interface (Reim et anoxic conditions in the presence of methanol as al., 2012). Tese fndings indicate that pmoA gene growth substrate (Dam et al., 2013). Since some expression and, linked to it, the activity of aerobic Methylocystis strains are known to be faculta- methanotrophic bacteria under microaerophilic or tive methanotrophs, even though with reduced even anoxic conditions is not restricted to aquatic growth capacities compared with growth on ecosystems, but occurs also in diferent wetland methane (Belova et al., 2011; Im et al., 2011), the soils. Tus, aerobic methanotrophs in diferent combination of facultative methanotrophy with ecosystems appear to be less dependent on (high) denitrifcation could be a way to overcome oxygen oxygen concentrations and oxygen availability may limitation for members of this genus. Besides be a less strict regulatory factor for the occurrence anaerobic respiration, fermentation has recently and activity of at least some aerobic methanotrophs been reported as an adaptation strategy for Methyl- than initially thought. omicrobium alcaliphilum strain 20Z (Kalyuzhnaya et In agreement with these observations is the al., 2013). Te authors observed the production of enrichment and isolation of methanotrophs from diferent organic acids in the presence of very low lake sediment and a peat bog ecosystem that grow oxygen concentrations, which were still sufcient preferentially under microaerophilic conditions, to perform methane oxidation. Finally, aerobic i.e. Methylosoma difcile, Methyloglobulus morosus methanotrophic bacteria were reported to survive and ‘Candidatus Methylospira mobilis’ (Rahalkar extended periods of anoxic conditions (Roslev and et al., 2007; Deutzmann et al., 2014; Danilova et King, 1994). al., 2016b). While the adaptation mechanisms to All these observations demonstrate that aerobic microaerophilic conditions of these specifc taxa methanotrophic bacteria have developed diferent are not yet known, diferent mechanisms are known strategies to live or at least to survive under condi- from other aerobic methanotrophic bacteria. One tions of severe oxygen limitation. However, the strategy appears to be the use of alternative terminal relevance of these diferent mechanisms under in oxidases with high afnity to oxygen. Te presence situ conditions remains currently largely unclear. of a cytochrome bd oxidase (Km value for oxygen Likewise, mechanisms to overcome the need between 3 and 8 nM) has been reported for a strain for oxygen for the initial methane oxidation step of the family Methylothermaceae, related to Methy- remain unknown (Chistoserdova, 2015). A putative lohalobius crimeensis and Crenothrix (Skennerton oxygen scavenging protein was recently discussed et al., 2015; Oswald et al., 2017). Te genes for in this context, due to the fact that gene expres- this oxidase were found in reconstructed genome sion of a cyanoglobin homologue was upregulated

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under hypoxic conditions and detected in ‘Methylo- methane is oxidized by these organisms per year monas denitrifcans’ and the reconstructed genome (Hu et al., 2014; Segarra et al., 2015), which would of the Methylothermaceae strain (Kits et al., 2015b; correspond to a reduction in emissions between 2% Skennerton et al., 2015). Since bacterial globins can and 50%, assuming a source strength of approxi- have diferent functions (Vinogradov et al., 2013), mately 200 Tg of methane per year (Fig. 2.1). A this protein and its possible role in methanotrophs global estimation for peatlands resulted also in a remains to be studied. 50% reduction of global methane emissions due For freshwater ecosystems, further possibili- to anaerobic methane oxidation, corresponding ties are under discussion to explain the activity of to 41 Tg of methane per year that are anaerobi- aerobic methanotrophs under anoxic conditions: cally oxidized (Smemo and Yavit, 2011). Another (i) methanotrophic bacteria living in association study reported an average of 24 Tg of methane with phototrophic microorganisms that produce consumption per year by anaerobic methanotrophs oxygen, which is instantaneously consumed and in peatlands, with very high variation between sites thus not detectable (Milucka et al., 2015; Oswald (Gupta et al., 2012). Based on these frst estimates, et al., 2015), linked to it (ii) oxygen concentrations it appears that anaerobic methane oxidation con- are below the detection limit of standard oxygen tributes signifcantly to a reduction in methane sensors and thus not detectable (Blees et al., 2014), emissions in wetlands and should therefore be (iii) oxygen may episodically be transported into considered as a relevant process. anoxic layers and therewith support aerobic metha- In marine ecosystems, anaerobic methane notrophs (Blees et al., 2014), (iv) the sedimentation oxidation is usually coupled with sulfate reduc- of inactive cells from oxic layers (Schubert et al., tion and mediated by anaerobic methanotrophic 2006), and (v) perhaps the use of alternative elec- archaea, which are ofen found in a consortium tron acceptors such as Mn(IV) or Fe(III) (Oswald with sulfate-reducing bacteria (Knitel and Boetius, et al., 2016). However, these hypotheses remain to 2009). Tese anaerobic methane-oxidizing archaea be proven and diferent explanations may be valid are Euryarchaeota that are phylogenetically related under diferent conditions. to methanogenic archaea and referred to as ANME clusters (Fig. 2.2). In contrast, microorganisms per- forming anaerobic methane oxidation coupled with Anaerobic methanotrophic denitrifcation are more common in continental archaea and bacteria ecosystems. Two major groups of microorganisms Besides the aerobic methanotrophic bacteria, have been characterized that are involved in this anaerobic methane-oxidizing archaea and bacteria process, represented by ‘Candidatus Methylomi- contribute to the reduction of methane emissions rabilis oxyfera’ and ‘Candidatus Methanoperedens in ecosystems that act are sources for atmospheric nitroreducens’ (Etwig et al., 2010; Haroon et al., methane. Tis is well known to be of particular rel- 2013). Moreover, a methanotrophic archaeon evance in marine ecosystems, where > 90% of the coupling anaerobic methane oxidation with iron produced methane is oxidized by anaerobic metha- reduction ‘Candidatus Methanoperedens ferriredu- notrophs (Knitel and Boetius, 2009). Knowledge cens’ has been described (Cai et al., 2018). All these about the flter efect of anaerobic methanotrophs diferent anaerobic methanotrophs can be suc- in terrestrial ecosystems is still limited, although cessfully enriched in bioreactors despite their slow evidence is accumulating concerning the relevance growth rates, but pure cultures are not available. of this process. Te process of anaerobic methane Characteristics of the diferent anaerobic metha- oxidation has been detected in diverse soils, espe- notrophs have been summarized in diverse review cially in diferent natural wetlands (e.g. Smemo and articles (e.g. Chistoserdova, 2015; Cui et al., 2015; Yavit, 2007; Gupta et al., 2012; Hu et al., 2014; Kallistova et al., 2017), some of them with a focus on Gauthier et al., 2015; Segarra et al., 2015). methanotrophs that oxidize methane coupled with First global estimates about the relevance of sulfate reduction (Knitel and Boetius, 2009) and anaerobic methane oxidation are available for others with a focus on those that couple methane natural wetlands, but still imprecise. According to oxidation with denitrifcation (Shen et al., 2015a; two independent studies, between 4 and 200 Tg of Welte et al., 2016). Yet others discuss in detail the

Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Methane-cycling Microorganisms in Soils | 41 particular physiology of these organisms (Caldwell while ANME-3 has been predominantly detected et al., 2008; McGlynn, 2017; Timmers et al., 2017). in submarine mud volcanoes and marine methane Within this review, relevant basic information seeps, indicating ecological niche separation (Knit- about these organisms is given, but the focus will be tel and Boetius, 2009; Cui et al., 2015; Timmers et on aspects related to their occurrence in soils. al., 2017). Te ANME organisms are frequently found in association with sulfate-reducing Del- Anaerobic methane oxidation taproteobacteria, ANME-1 and -2 with members coupled with sulfate reduction of the Desulfosarcina-Desulfococcus group and ANME-3 preferentially with Desulfobulbus (Knit- Diversity and physiology of anaerobic tel and Boetius, 2009; Cui et al., 2015). While methane oxidizers dependent on sulfate the ANME organisms are performing methane reduction oxidation to carbon dioxide, the sulfate reducers Tree phylogenetic groups of anaerobic methane- are responsible for sulfate reduction. Terefore, oxidizing archaea are known that couple methane reducing equivalents are channelled between the oxidation with sulfate reduction, ANME-1 to -3 two partners (McGlynn et al., 2015; Wegener et al., (Knitel and Boetius, 2009; Timmers et al., 2017). 2015). However, sometimes ANME groups have Tey were defned based on distinct clustering also been found in association with other bacterial of their 16S rRNA and mcrA gene sequences in taxa, and an association between sulfate reducers phylogenetic trees. Te ANME-1 group has been and ANME-1 is not consistently observed (Knit- reported to be distantly related to the Methano- tel and Boetius, 2009; Timmers et al., 2017). Tis sarcinales and Methanomicrobiales. It now appears suggests that some ANME groups may perform the that they are also related to the recently described complete process alone, as proposed for ANME-2 Methanonatronarchaeales (Fig. 2.2). Te ANME-2 organisms (Milucka et al., 2012). Alternatively, group is related to the Methanosarcinales and they may couple methane oxidation to other not ANME-3 to the genus Methanococcoides within the yet known reduction processes, either in associa- order Methanosarcinales. tion with a bacterial partner or possibly even alone. Te ANME-1 group consists of subgroups a and Moreover, it has been discussed that ANME-1 and b, ANME-2 of subgroups a, b and c. Te groups ANME-2 organisms can perform methanogenesis ANME-2a and -2b form a coherent clade and are instead of methane oxidation (House et al., 2009; ofen grouped together as ANME-2a/b. Further- Bertram et al., 2013). Tis metabolic versatility is more, an ANME-2d group has been proposed to the result of a genetic makeup that allows reverse exist, including ‘Candidatus Methanoperedens methanogenesis for methane oxidation (Hallam nitroreducens’, which couples methane oxida- et al., 2004; Scheller et al., 2010), but which can tion with denitrifcation (Haroon et al., 2013). obviously still operate in the direction known Earlier, this group was referred to as AOM associ- from methanogenic archaea. Tus, the presence of ated archaea (AAA) group (Knitel and Boetius, ANME organisms can be linked to both, methane 2009). In the literature, the name ANME-2d had oxidation as well as methane production activity. been introduced once before for the related GOM Te relative importance of a methanogenic activity Arc I sequence cluster, but the name was replaced needs to be studied in more detail in the future. by GOM Arc I because of missing evidence for anaerobic methane oxidation potential (Lloyd et Evidence for anaerobic methane al., 2006). Today, the two clusters are sometimes oxidation coupled to sulfate reduction in combined again into a larger ANME–2d cluster, terrestrial ecosystems and soils despite the missing evidence for methanotrophy In continental ecosystems, anaerobic methane in the GOM Arc I group, and this larger ANME-2d oxidation coupled with sulfate reduction is mostly cluster is meanwhile divided into three subgroups considered to be of minor relevance, because sul- based on 16S rRNA gene sequences (Welte et al., fate concentrations are usually much lower than 2016). in marine ecosystems, rendering this process ther- Te ANME-1 and ANME-2 groups show a modynamically unfavourable (Smemo and Yavit, wide distribution in diverse marine environments, 2011). However, internal redox-cycling of sulfur

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compounds, e.g. due to fuctuating water levels, sulfate reducers were identifed in the studies of might support this type of methane oxidation even Takeuchi et al. (2011), where ANME 1 sequences in continental ecosystems at lower sulfate con- were found in the freshwater subsurface, and of centrations. Indirect evidence from mass balance Chang et al. (2012), who detected ANME-1a and approaches and measurements of methane oxida- -2a in a mud volcano and proposed a coupling to tion rates in combination with sulfate reduction metal reduction rather than to sulfate. A detec- rates points to the existence of this process, e.g. tion of (active) ANME organisms in soils from in natural wetlands, rice paddies and groundwater natural wetlands or rice paddies remained usually at a landfll leachate plume (Murase and Kimura, unsuccessful (Miyashita et al., 2009), indicating 1994; Grossman et al., 2002; Segarra et al., 2015). that the occurrence of ANME organisms in con- However, fnal proof for a coupling of anaerobic tinental environments is largely limited to some methane oxidation with sulfate reduction is not freshwater systems and particular habitats such as given in most of these studies and oxidation rates mud volcanoes. were ofen considered to be quantitatively unim- portant. To further validate the existence of this Anaerobic methane oxidation process in continental ecosystems, the presence of coupled with denitrification anaerobic methane-oxidizing microorganisms and Te coupling of anaerobic methane oxidation with their active involvement in the methane oxidation denitrifcation was frst detected in an enrichment process need to be carefully proven (Timmers et culture obtained from an anoxic freshwater sedi- al., 2016). ment rich in nitrate (Raghoebarsing et al., 2006). Te detection of anaerobic methanotrophic Te microorganisms being responsible for this archaea of the clusters ANME-1, -2 and -3 process were identifed as bacteria of the candidate was initially limited to anoxic, methane-rich, phylum NC10 and referred to as ‘Ca. Methy- sulfate-containing marine sediments (Knitel et lomirabilis oxyfera’ (Etwig et al., 2010). Tese al., 2005). In the meantime, 16S rRNA gene so-called ‘NC10 bacteria’ couple the oxidation of sequences of ANME-1 and -2, especially those of methane with nitrite reduction to dinitrogen. the ANME-1a and -2a sub-clusters, have repeat- A few years afer the discovery of ‘Ca. Methy- edly been detected in some specifc continental lomirabilis oxyfera’ it turned out that anoxic environments such as freshwater subsurfaces and incubations with methane and nitrate (and nitrite methane seeps, oilfeld production waters and or ammonium in addition) for the enrichment mud volcanoes (e.g. Knitel and Boetius, 2009; of denitrifying anaerobic methanotrophic bacteria Niederberger et al., 2010; Chang et al., 2012). support the establishment of another anaerobic Moreover, their presence has been shown in the methanotroph, the archaeal ‘Ca. Methanopere- terrestrial subsurface, in soils from natural gas dens nitroreducens’, representing the ANME-2d felds and a eutrophic freshwater lake (Eller et group (Haroon et al., 2013). Tis organism is al., 2005; Fry et al., 2009; Miyashita et al., 2009). a member of the order Methanosarcinales, class As presence does not necessarily imply activity, ‘Candidatus Methanoperedenaceae’. It couples anaerobic methane oxidation was demonstrated methane oxidation with nitrate reduction to to be an active process in freshwater sediment nitrite. Depending on the nitrogen sources that samples based on 16S rRNA recovery and meth- are provided, ‘Ca. Methanoperedens nitroredu- ane oxidation rate measurements, which were cens’ can form syntrophic associations either with shown to be stimulated by sulfate amendments ‘Ca. Methanoperedens nitroreducens’ or with (Takeuchi et al., 2011; Timmers et al., 2016). Te anaerobic ammonium-oxidizing (anammox) bac- strongest evidence for a coupling of anaerobic teria (Raghoebarsing et al., 2006; Haroon et al., methane oxidation with sulfate reduction was 2013; Arshad et al., 2015; Vaksmaa et al., 2017a; provided in the study by Timmers et al. (2016), Gambelli et al., 2018). It is assumed that ‘Ca. who evaluated methane oxidation and sulfate Methylomirabilis oxyfera’ or the anammox bacte- reduction activity and detected ANME-2a/b ria support the growth of ‘Ca. Methanoperedens sequences along with sequences of sulfate reduc- nitroreducens’ by eliminating nitrite, which is ers in freshwater sediment samples. In contrast, no toxic at high concentrations (Welte et al., 2016).

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Physiology of ‘Ca. Methylomirabilis in the meantime, ‘Candidatus Methylomirabilis oxyfera’ and ‘Ca. Methanoperedens sinica’, enriched from paddy soil (He et al., 2016). nitroreducens’ Several further reports describe the enrichment Physiological properties of ‘Ca. Methanoperedens of bacteria coupling anaerobic methane oxidation nitroreducens’ were derived from reconstructed with denitrifcation from diverse environmental genome information, which is meanwhile avail- samples, including paddy soils, peatland, river able for a couple of enrichment cultures (Haroon sediments, coastal sediments, wastewater and bio- et al., 2013; Arshad et al., 2015; Berger et al., 2017; reactor sludges (Zhu et al., 2012; He et al., 2015; Vaksmaa et al., 2017a). Tis indicates the coupling Bhatacharjee et al., 2016; Chen et al., 2016; Welte of nitrate reduction to nitrite with reverse metha- et al., 2016; Vaksmaa et al., 2017a). Furthermore, nogenesis. Nitrate reduction is performed by a bacteria of the NC10 phylum were identifed in membrane-bound nitrate reductase that appears several cultivation-independent studies (Shen et to be of bacterial origin, possibly obtained via hori- al., 2015d; Chen et al., 2016; Welte et al., 2016). zontal gene transfer. A membrane-bound nitrite Such studies use the 16S rRNA or the pmoA gene reductase may be involved in the conversion of as marker. Data interpretation of 16S rRNA gene nitrite to ammonium, which may contribute to the marker based results has to be done with care, elimination of nitrite. because the NC10 phylum includes four diferent Similarly as for ‘Ca. Methanoperedens nitrore- 16S rRNA gene sequence clusters, but it is not ducens’, metagenomic sequencing helped to get yet clear whether all clusters represent anaerobic insight into the metabolism of ‘Ca. Methylomira- methanotrophic bacteria (Welte et al., 2016). Te bilis oxyfera’. Tese organisms have established a use of pmoA as marker demands specifc pmoA completely diferent mechanism to couple methane primers due to the distinct clustering of their oxidation with nitrite reduction to dinitrogen. A pmoA sequences in phylogenetic trees (Fig. 2.4), methane oxidation pathway as known from aerobic and several diferent pmoA primer sets have been methanotrophic bacteria is present, while reverse developed (Shen et al., 2015d; Chen et al., 2016). methanogenesis does not play a role. Te aerobic Analyses based on the 16S rRNA and pmoA marker methane oxidation pathway includes methane oxi- genes indicate that methanotrophs of the NC10 dation via a particulate methane monooxygenase, phylum are present in diverse environments. Te which demands oxygen. It is assumed that this detection was successful in freshwater lake and river oxygen is derived from an intra-aerobic pathway, sediments, in diferent wetlands including peatlands in which dinitrogen and oxygen are obtained by and swamps, in paddy soils and a few times in other a dismutation reaction of two molecules of nitric agricultural soils, in wastewater systems, in some oxide (Etwig et al., 2010, 2012). Oxygen that is marine and coastal sediments, and recently for the not used for methane oxidation may be reduced frst time in the rumen fuid from goats (Chen et al., by a terminal oxidase, allowing to gain additional 2016; Shen et al., 2016b; Welte et al., 2016; L. Liu energy by oxygen respiration (Wu et al., 2011). et al., 2017). Despite the need for oxygen, ‘Ca. Methylomirabilis Tis broad occurrence is in line with predic- oxyfera’ is an anaerobic organism. In the presence tions stating that anaerobic methane oxidation of ≥ 2% oxygen, methane oxidation and nitrite coupled to denitrifcation should be relevant in reduction activity decreased substantially and the ecosystems with methane supply from anoxic cells encountered oxidative stress (Luesken et compartments and availability of oxidized nitrog- al., 2012). However, it remains currently unclear enous compounds (Tauer and Shima, 2008). whether they proft from external oxygen when Such conditions are found, for example, in waste- available in trace amounts. water treatment systems or near the oxic/anoxic interphase in paddy soils or freshwater ecosystems, Diversity and environmental distribution especially when located in agricultural landscapes of ‘Ca. Methylomirabilis oxyfera’ and with high nitrogen input. Indeed, ‘Ca. Methylomi- ‘Ca. Methanoperedens nitroreducens’ rabilis oxyfera’ can be detected at such oxic/anoxic Besides ‘Ca. Methylomirabilis oxyfera’, a second interfaces in various wetlands (Raghoebarsing et al., species of this candidate genus has been proposed 2006; Zhu et al., 2015). However, several studies

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report the predominant occurrence in deeper layers 2015c) and ‘Ca. Methanoperedens nitroredu- of wetlands and paddy soils (Zhu et al., 2012; Hu cens’ (Vaksmaa et al., 2016) in the corresponding et al., 2014; Shen et al., 2015b,c), where anoxic samples. In the paddy soil study the determined conditions are more stable. Moreover, NC10 methane uptake rates were substantially higher than methanotrophs were more abundant in freshwater reported in an earlier study, indicating that anaero- samples such as reservoir and pond sediments with bic methane oxidation may play a signifcant role in rather stable anoxic conditions than in wetland sedi- these soils (Vaksmaa et al., 2016). Diferences con- ments or paddy soils (Shen et al., 2016b). However, cerning the activity of these methanotrophs were if ‘Ca. Methylomirabilis oxyfera’ colonizes indeed also reported for natural wetlands, i.e. an activity preferably habitats that provide stable anoxic con- of anaerobic methanotrophs could not always be ditions, the detection in upland soils is surprising, proven (Tveit et al., 2013). In general, the potential as reported for tropical forest samples in 5–20 cm contribution of anaerobic denitrifying methano- depth (Meng et al., 2016) and agricultural soil sam- trophs in carbon and nitrogen cycling needs to be ples in 50–60 cm depth (Hu and Ma, 2016; Shen studied in more detail in the diverse environments et al., 2016a). However, a detection in upland soils to assess their relevance more precisely. was not consistently observed (Zhu et al., 2015). Te relevance of ‘Ca. Methylomirabilis oxyfera’ in Alternative electron acceptors for such soils remains currently completely unclear. anaerobic methane oxidation Similarly as ‘Ca. Methylomirabilis oxyfera’, ‘Ca. Besides sulfate, nitrate and nitrite, further electron Methanoperedens nitroreducens’, shows a broad acceptors have been discussed to be of relevance occurrence. It has been detected in lake and river in combination with anaerobic methane oxida- sediments, aquifers, paddy soils, peatlands, mud tion. A coupling with iron reduction has been volcanoes, sewage treatment plants and, to limited demonstrated in ‘Candidatus Methanoperedens extent, in the marine and brackish environment ferrireducens’ (Cai et al., 2018). Tis archaeon (Ding et al., 2015; Welte et al., 2016; Narrowe et al., was enriched in a bioreactor fed with methane 2017). Te cultivation-independent detection is and ferrihydrite, which was set up with material done using group-specifc 16S rRNA gene primers from a freshwater reservoir. Metagenomic analysis or mcrA gene primers (Ding et al., 2015; Vaksmaa predicts that methane oxidation occurs via reverse et al., 2017b; Xu et al., 2018). Te obtained 16S methanogenesis and iron reduction by multi- rRNA gene sequences can be classifed into three haem c-type cytochromes. Te exact mechanism diferent subgroups, which are not all represented of the electron transfer to iron remains currently by enrichment cultures, so that the methane oxida- unclear. Earlier, a coupling of methane oxidation tion potential of some sequence clusters remains to iron reduction was already reported for an currently unclear (Welte et al., 2016). enrichment culture of ‘Candidatus Methanopere- As presence does not necessarily imply activity, dens nitroreducens MPEBLZ’, obtained from a studies are needed to assess the activity of these freshwater sample and cultured in a reactor with methanotrophs in the diferent ecosystems. Tis methane and nitrate as substrates (Etwig et al., has so far only been done in a few studies, either at 2016). Tis culture was able to couple methane the transcript (Padilla et al., 2016) or protein level oxidation with nitrate or iron, but the rate of (Hanson and Madsen, 2015) in a marine and fresh- iron-based oxidation was 10-fold lower than in water environment, respectively, demonstrating ‘Ca. Methanoperedens ferrireducens’ (Cai et al., metabolic activity of ‘Ca. Methylomirabilis oxyfera’. 2018). Besides the use of nitrate and iron, ‘Ca. Some other studies demonstrated by isotope exper- Methanoperedens nitroreducens MPEBLZ’ was iments that an anoxic conversion of methane in the shown to reduce manganese. Obviously, ‘Ca. presence of nitrite or nitrate as electron acceptor Methanoperedens’ shows versatility concern- is occurring in wetlands, lake sediment and a rice ing the use of electron acceptors, but may have paddy soil. Tese analyses were combined with substrate preferences. It remains currently unclear molecular approaches, confrming the presence of how commonly iron-reduction occurs within this ‘Ca. Methylomirabilis oxyfera’ (Deutzmann and candidate genus and how versatile the individual Schink, 2011; Hu et al., 2014; Shen et al., 2014, members are indeed.

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Te coupling of anaerobic methane oxidation (2015) observed diferent dependencies on elec- with iron reduction has been demonstrated in tron acceptors in diferent wetland systems. It can incubation experiments with deep sea sediment thus be concluded that anaerobic methane oxida- material harbouring ANME-2c organisms (Scheller tion is of relevance in diverse terrestrial ecosystems. et al., 2016) and by geochemical profling or iso- Te coupling of anaerobic methane oxidation with tope tracer studies in environmental samples from specifc reduction processes and the identity of the lake water and sediment, marine sediments, paddy involved microorganisms appears to be ecosystem felds, a terrestrial mud volcano and a contaminated specifc and requests a good understanding of the aquifer (Zandt et al., 2018). Te detection of the geochemical processes in combination with the process and the presence of ‘Ca. Methanoperedens’ physiology of the microorganisms inhabiting the species in such environments (Welte et al., 2016; respective ecosystems. Narrowe et al., 2017) suggests a high ecological relevance, especially in marine and freshwater ecosystems, where iron oxides are present in the Conclusions and future sediments (Cai et al., 2018), but more studies are perspectives needed that link the geochemical processes with Microbiological processes leading to methane microbiological data to demonstrate this relevance production and consumption are major drivers of and identify the involved microorganisms. the global methane cycle. For a long time, meth- In peatlands, methane oxidation coupled with ane production was atributed to the activity of a iron reduction has also been discussed as an option few orders of methanogenic Euryarchaeota, while because of low concentrations of available sulfate methane oxidation activity was ascribed to specifc and nitrate, but could not yet be proven (Smemo families of methanotrophic Alpha- and Gammapro- and Yavit, 2007, 2011; Gupta et al., 2012). Alter- teobacteria. Research of the last two decades has natively, humic substances are considered to be of substantially extended the list of players in both possible relevance, knowing that ANME organisms groups. As described in this review, a couple of new can transfer electrons to external acceptors (Schel- orders of methanogens within the Euryarchaeota ler et al., 2016) and that humic substances can act as were discovered during the last years and metagen- electron acceptors (Scot et al., 1998). Further evi- omic analyses suggest that methanogens may even dence is provided by the observations that humic exist beyond the phylum Euryarchaeota. Likewise, substances accumulate in peatlands and anaerobic the methanotrophic lifestyle appears to be more methane oxidation was detected, but without widespread among microorganisms within the strong evidence for a coupling with nitrate, sulfate Alpha- and Gammaproteobacteria but also among or iron reduction (Smemo and Yavit, 2007; Gupta other taxa, exemplifed by the discovery of metha- et al., 2012). Such a weak coupling with the known notrophy in the phylum Verrucomicrobia. Work of inorganic electron acceptors was also reported by the last years also indicates that anaerobic meth- Reed et al. (2017) for an eutrophic reservoir, along ane oxidation plays an important role not only in with the suggestion that organic acids, which are marine ecosystems, but also in continental environ- major constituents of organic mater, may serve as ments including natural as well as anthropogenic electron acceptors during anaerobic methane oxi- wetlands, which are known to represent major dation in eutrophic lakes and reservoirs. sources of atmospheric methane. Distinct groups Tese fndings indicate that the geochemical of methanotrophs such as ‘Ca. Methylomirabilis’ characteristics of an ecosystem will have a major and ‘Ca. Methanoperedens’ appear to be the major impact on the overall rate of anaerobic methane types responsible for this process in terrestrial eco- oxidation and the dominant type of methane oxi- systems. In order to beter understand the methane dation process taking place. Tis is exemplifed by sink or source capacity of an ecosystem and the the observation that anaerobic methane oxidation variation of emissions or uptake in space and over activity was quantitatively more important in nutri- time, the activities of all groups involved in meth- ent-rich (minerotrophic) fens than in nutrient-poor ane cycling need to be considered. Tus, there is a (ombrotrophic) bogs (Smemo and Yavit, 2007; clear need for studies that integrate the activities of Gupta et al., 2012). Furthermore, Segarra et al. all players.

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Te spatial distribution, abundance and activity still used in many models (Gauthier et al., 2015). of the individual players is controlled by diverse Besides an improvement of current models, the environmental factors. Recent fndings indicate efect of oxygen on the distribution and activity of that more controls need to be considered. Several of aerobic methanotrophs needs to be studied in more the recently discovered groups of methanogens and detail in soils. It has so far mostly been analysed in methanotrophs but also some of the well-known well-stratifed ecosystems, especially lakes, but may players show a broader metabolic versatility than be of equal relevance for the control of methano- previously thought. Tus their presence alone or trophs and methanogens in wetland soils, which their general metabolic activity does not necessarily show a higher variation in oxygen availability in allow direct conclusions about their involvement in space and over time. methane cycling under given conditions. Te meth- As evident from this review, work of the last ane oxidation activity of facultative or mixotrophic years has substantially extended the known methanotrophs may for example be suppressed or diversity of methanotrophic and methanogenic modulated dependent on the availability of alterna- microorganisms as well as knowledge about their tive carbon and energy sources such as acetate or metabolic capabilities. Te discovery of new puta- dihydrogen. Similarly, the activity of anaerobic tive methanogenic and methanotrophic organisms methanotrophs is largely dependent on the avail- in taxonomic groups not yet known to include ability of suitable electron acceptors. Tis in turn such organisms was mostly the result of genome can depend on the activities of other groups of sequencing eforts. Physiological capabilities of organisms. Nitrite availability for ‘Ca. Methylomi- uncultured organisms can now be derived quite rabilis’ will for example depend on the organisms easily from such genome reconstructions. Tou- that produce nitrite, e.g. aerobic nitrifers in nearby sands of genomes are meanwhile available (e.g. oxic habitats or ‘Ca. Methanoperedens’ in the Whitman et al., 2015; Anantharaman et al., 2016; same anoxic habitat, as well as on the presence and Parks et al., 2017) and many more datasets can activity of potential competitors such as anammox be expected to be generated in the near future, bacteria. A good understanding of such dependen- either by de novo sequencing of isolates, single-cell cies helps to defne the ecological niche of these based approaches for the analysis of uncultivated bacteria in natural as well as in artifcial ecosystems bacteria or assembly of genomes from metagen- such as wastewater treatment systems, where they omic data. Te analysis of these data will provide could be introduced to reduce methane emissions further insight into the metabolic versatility of (van Kessel et al., 2018). known methane cycling microorganisms and very Tis review also demonstrates that the control of likely lead to the identifcation of further groups methanotrophic activity by specifc environmental of microorganisms harbouring methane cycling factors has to be assessed at a fner scale, at least potential in phylogenetic groups that are not yet for some factors. Exemplarily, the dependency on known to include methanogens or methanotrophs. oxygen is highlighted, due to the fact that recent It will be a major task to validate the methane studies revealed interesting new insights. On the production or oxidation capabilities of these organ- one hand, several methanogenic archaea appear to isms. Some of these microorganisms may have a be less sensitive to oxygen than previously thought broader metabolic versatility compared with the and methane production may even occur under canonical methanotrophs and methanogens, so apparently oxic conditions, on the other hand, that their activities and therewith their contribu- some aerobic methanotrophic bacteria seem to be tion to methane cycling in an ecosystem needs to less dependent on oxygen and may remain active be assessed carefully, e.g. by applying multi-omics under apparently anoxic conditions. Considering approaches including metatransriptomics, -prot- that anaerobic methane oxidation is a process that eomics and possibly -metabolomics. Such studies occurs in terrestrial ecosystems such as wetlands, should be complemented by laboratory analyses of the general and rather simple assumption that oxic microcosms, enrichment cultures or isolates under conditions support methane oxidation activity and controlled conditions to identify and to under- anoxic conditions methane production appears stand the regulatory mechanisms that determine to be too simple. Such general assumptions are methanogenic or methanotrophic activity rates of

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