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Home , Dimethyl sulfide, Gas leak, Methanethiol, Methanethiol oxidase, Methyl group

Microbial Cycling of Hendrik Schäfer1* and Özge Eyice2

1 School of Sciences, University of Warwick, Coventry, UK. 2 School of Biological and Chemical Sciences, Queen Mary University of London, London, UK. *Correspondence: [email protected] htps://doi.org/10.21775/cimb.033.173

Abstract decaying biomass, it can be found widely in the Methanethiol (MT) is an organic sulfur compound environment, for instance as a compound emited with a strong and disagreeable odour. It has bio- from roting fruit and vegetables but it is also found geochemical relevance as an important compound in association with humans and animals where it is in the global , where it is produced as a a component of the smell of faeces, fatus and can reactive intermediate in a number of diferent path- be associated with (halitosis) (NCBI ways for synthesis and degradation of other globally Pubchem database, n.d.). Te human sense of smell signifcant sulfur compounds such as dimethylsul- has a low threshold for detection of MT at 1–2 ppb foniopropionate, dimethylsulfde and . (Devos et al., 1990), which is exploited in its use as With its low odour threshold and unpleasant smell, an additive to distribution systems in MT can be a signifcant cause of malodour originat- order to facilitate the detection of leaks. A leak of an ing from animal husbandry, composting, landfll unspecifed quantity of MT from a chemical factory operations, and wastewater treatment and is also in northern France in 2013 illustrated the potential associated with faeces, fatus and oral malodour of MT as a signifcant malodour. A bad smell was (halitosis). A diverse range of microorganisms reported in parts of northern France and as far away drives the production and degradation of MT, as across the Channel in parts of Southern England, including its aerobic and anaerobic metabolism. due to the chemical having been dispersed by the MT producing and degrading organisms are known wind (Reuters, 2013). to be present in terrestrial, freshwater and marine environments but may also be important in asso- ciation with plant and animal (including human) Environmental concentrations, hosts. Tis chapter considers the role of MT as an production and degradation intermediate of the global sulfur cycle and discusses of MT current knowledge of microbial pathways of MT production and degradation. Environmental concentrations of MT Only relatively few studies have measured MT concentrations in , anoxic environments Introduction and industrial setings. A detailed study of pro- Methanethiol (MT), also known as methylmercap- duction of volatile sulfur compounds in anoxic tan, is a one- organic sulfur compound with freshwater sediments in a peat bog by Lomans et al. the formula CH3SH. With a boiling point of 6ºC it (1997) showed that MT was one of the dominant is a colourless gas at room temperature character- volatile sulfur compounds in anoxic sediments. MT ized by a pungent and disagreeable odour that has concentrations ranged from 3–76 nM and its pro- been likened to roten cabbage. As a of duction pathway was biological as shown by heat

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killed controls. Accumulation of MT in sediment al., 2009; Todd et al., 2011; Curson et al., 2011a,b, slurries to which bromoethanesulfonate had been 2012; Sun et al., 2016). Once produced, DMS is added, suggested that methanogens were mainly degraded to MT by a DMS monooxygenase, which responsible for MT removal in these freshwater was reported in some strains of Hyphomicrobium sediments. Surface freshwater MT concentrations and Arthrobacter (De Bont et al., 1981; Borodina et in the peat bog were 1–8 nM and in a similar range al., 2000; Boden et al., 2011).

to those of H2S, DMS and CS2, demonstrating that MT production also occurs as an intermediate MT contributes to emission of S from such fresh- of microbial DMSP degradation via the demethyla- environments (Lomans et al., 1997). tion pathway. In a study of the sulfur metabolism of In marine environments, MT concentrations several isolates from the abundant marine roseo- have been reported to be in the range of 0.02–2 nM. bacter clade, Gonzales and colleagues noted the In a study primarily reporting carbonyl sulfde ability of several strains to produce MT from DMSP (COS) emissions from the Aegean Sea, MT con- and other precursors including DMS, dimethyl centrations detected at time zero in incubation (DMSO), 3-methylmercaptopropionate experiments with natural seawater samples were in (MMPA) and α-ketomethiol-butyrate (González a range of 50–500 pM and it was suggested that MT et al., 1999). Subsequent characterization of the was subject to photodegradation and could poten- metabolic pathway producing MT from DMSP tially be a precursor for COS photoproduction showed that, in this pathway, DMSP is initially (Ulshöfer et al., 1996). Measurements of MT were demethylated to MMPA by DMSP demethylase also reported for a sample transect of the Atlantic encoded by dmdA, which was frst discovered in by Ketle and colleagues, who reported average MT the marine roseobacter Ruegeria pomeroyi DSS-3 concentrations in surface seawater of 420 pM, with (Howard et al., 2006). Subsequently, Reisch et al. localized higher concentrations up to ≈ 1700 pM (2011) demonstrated that afer the demethylation in the North African upwelling area, around step, MMPA is catabolized frst to methylthioacr- ≈ 1500 pM in a coastal region close to Montevideo yloyl-CoA (MTA-CoA) and then to MT via the and up to ≈ 1000 pM on a transect between Monte- demethiolation pathway (Reisch et al., 2011b). video and the Falkland Islands (Ketle et al., 2001). Te genes designated as dmdB, dmdC and dmdD In addition to above mentioned photodegradation, were shown to encode the catalysing the the reaction of MT with sulfate, dissolved organic transformation from MMPA to MT in R. pomeroyi. mater (DOM) and trace metals to form sulfate– Te presence of these genes (with the exception of DOM–metal complexes has also been suggested as dmdD) in the genome of ubiquitous marine bacte- an abiotic degradation pathway (Kiene et al., 2000). rium Pelagibacter ubique, Pelagibacter HTCC1062 and Ruegeria lacuscaerulensis as well as in marine metagenomes reiterate the signifcance of this Biological Production of MT pathway in the marine environment (Reisch et al., Biological MT production is well known as an 2011b; Sun et al., 2016). Sun and colleagues also intermediate in metabolism of dimethylsulfonio- demonstrated that eight Pelagibacterales genomes propionate (DMSP) (Kiene and Taylor, 1988; contain homologues of the dmdABC genes, but not Kiene et al., 2000; Reisch et al., 2011a,b) and DMS dmdD, but Pelagibacter is still able to produce MT (De Bont et al., 1981; Suylen and Kuenen, 1986; from DMSP. Tis suggests that the MT formation Pol et al., 1994; Borodina et al., 2000; Schäfer, from MMPA is widespread in marine ecosystems, 2007) which itself can be produced through micro- however a novel may be catalysing the bial degradation of DMSP (Curson et al., 2011b). last step of MT production from DMSP in some In marine, estuarine and salt marsh environments, marine . DMSP, an abundant metabolite released by phyto- It was also noted that several aerobic bacteria and macroalgae, acts as a key precursor of from the genera Corynebacterium, Rhizobium, Fla- dimethylsulfde (DMS). Degradation of dissolved vobacterium, Erwinia, Aeromonas, Pseudomonas and DMSP releases DMS by the activity of DMSP- Yersinia isolated from soil, sediment and marine (Johnston et al., 2008), which are found in algae cultures have the capacity to methylate hydro- many aerobic and anaerobic organisms (Todd et gen sulfde to produce MT. Te activity of a

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S- was demonstrated in distinct aerobic/anaerobic interfaces of organic rich fractions of crude cell free extracts of Pseudomonas freshwater sediments as methoxylated aromatic fuorescens PF4 subjected to gel-fltration and - compounds are produced during the degradation exchange chromatography; S-adenosylmethionine of lignin, an abundant biopolymer (Lomans et al., was identifed as a methyl donor (Drotar et al., 2002). 1987). Te authors speculated that further meth- ylation of the product MT to DMS would be a possibility and might be carried out by the same Microbial degradation of MT enzyme, but they did not observe DMS produc- Te main sink for MT in the environment is its deg- tion in their activity assays, noting that this would radation by microorganisms. Owing to the toxicity depend on the Km of the second methyl transfer and foul odour of MT, only few studies have actually reaction (Drotar et al., 1987). atempted to enrich and grow microorganisms on MT as a sole source of carbon and energy source. Anaerobic mechanisms Terefore, most of what is known about microbial In anaerobic soils and sediments, MT is primarily MT degradation is based on isolates in which MT produced via the degradation of sulfur containing is degraded as an intermediate of the metabolism of amino and of sulfde (Lomans et other organic sulfur compounds. al., 2002). Degradation of methionine was shown to lead to formation of MT in anoxic lake sediments Aerobic mechanisms (Zinder and Brock, 1978). Similarly, in anoxic salt Aerobic degradation of MT was shown in Hypho- marsh sediments, addition of methionine and microbium sp. S, which was obtained from soil using S-methyl cysteine led to production of MT, less DMSO as the enrichment (De Bont et MT production was noted from DMSP (Kiene al., 1981). Following this, a wide range of aerobic and Capone, 1988). Te methyl-thiol group of bacteria that degrade MT have been isolated from methionine is cleaved (demethiolation) via the several environments including soil, peat bioflter, methionine-gamma- enzyme (MegL), which lake and marine sediments, seawater and marine has been purifed and characterised from various algal cultures. Tese methylotrophic and sulfur- bacteria such as Pseudomonas, Brevibacter and oxidizing species were afliated with the genera Trichomonas species (Bentley and Chasteen, 2004). Hyphomicrobium, Tiobacillus, Rhodococcus and Another route to anaerobic MT production is by Methylophaga (De Bont et al., 1981; Suylen et al., the activity of thiol S-methyltransferases, which 1987; Cho et al., 1991; Gould and Kanagawa, 1992; transfer methyl groups from S-adenosylmethionine Visscher and Taylor, 1993a,b; Pol et al., 1994; Boro- to sulfde resulting in MT formation or methylate dina et al., 2000; Schäfer, 2007; Boden et al., 2010). MT to form DMS (Bentley and Chasteen, 2004). Recently, Methylotenera mobilis JLW8 was shown to Methoxylated aromatic compounds are another degrade MT as the sole carbon and energy source precursor from which MT is produced in soil and (Carrión et al., 2017). sediments. Bak and colleagues (1992) isolated Aerobic bacteria degrade MT by methanethiol two anaerobic homoacetogenic species from the oxidase (MTO). Tis enzyme has been purifed genus Pelobacter that produce MT during growth from Hyphomicrobium and Tiobacillus species and on trimethoxybenzoate or syringate by transfer- shown to degrade MT to , hydro- ring the methyl group of the aromatic ring to gen sulfde and peroxide (Suylen et al., hydrogen sulfde via thiol S- 1987; Gould and Kanagawa, 1992). Recently, (Bak et al., 1992). Several anaerobic isolates have the MTO enzyme in Hyphomicrobium sp. VS has been described including members of the genera been characterised in more detail, showing that it Holophaga, Sporobacter, Sporobacterium and Par- requires Cu for activity and suggesting presence of asporobacterium that can methylate sulfde to MT a tryptophan-tryptophylquinone (TQ) co-factor. during the degradation of aromatic methoxylated Te identifcation of the encoding gene revealed compounds (Kref and Schink, 1993; Grech-Mora that MTO it is a homologue of the so-called sele- et al., 1996; Mechichi et al., 1999; Lomans et al., nium-binding whose function had 2001). Tis process is suggested to take place at previously been poorly constrained (Eyice et al.,

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2018). However, identifcation and characterisa- the MddA enzyme can be found abundantly in tion of the human form of selenium-binding protein metagenomes, particularly in soils. Te relatively SELENBP1 by Pol and colleagues demonstrated low conversion of MT to DMS observed in a that the human homologue is also a methanethiol grassland soil in the study could be due to compet- oxidase and that a genetic defect in this gene is the ing pathways of MT and DMS removal and the underlying cause of extra-oral, or -borne, hali- environmental signifcance of this pathway requires tosis (Pol et al., 2018). additional analysis (Carrión et al., 2017). Genes encoding MTO are present in genomes of a wide range of microorganisms known to degrade Anaerobic mechanisms DMS (e.g. Hyphomicrobium and Tiobacillus spp.), DMS and MT degradation by microorganisms has DMSP (Ruegeria pomeroyi and other roseobacter been studied in several ecosystems, yet, our knowl- clade bacteria), and indeed a number of methano- edge on microbial populations that degrade MT in trophic and methylotrophic bacteria. Detection of anoxic environments is very limited. mtoX in metagenomes as well as the application of MT is primarily used by -producing specifc PCR primers for mtoX demonstrated that archaea (methanogens) and sulfate-reducing mtoX and thus MT-degrading bacteria are present bacteria (SRB) in anoxic marine, freshwater and in a wide range of marine and terrestrial environ- terrestrial ecosystems (Fig. 9.1; Zinder and Brock, ments. Application of the stable isotope probing 1978; Lomans et al., 1999b). Te f rst study that method with 13C-labelled DMS has also been used showed that MT is degraded to methane and indirectly to identify active MT-degraders in soil was carried out on samples from and lake sediment samples (Eyice et al., 2018). Lake Mendota (Wisconsin, USA) using radiola- MT oxidases with diferent molecular weights to belled 14C-methyl-methionine (Zinder and Brock, that found in Hyphomicrobium sp. VS have been 1978). However, pure methanogenic species that reported in Rhodococcus and Tiobacillus strains, suggesting that other methanethiol oxidases may yet have to be characterized in detail at the bio- DMSP Methionine chemical and genetic level (Kim et al., 2000; Lee et Dmd MegL Ddd al., 2002). MddA Tmt CH -O-R An alternative sink for MT removal in aerobic DMS MT 3 Dmo SAM environments is MT-dependent DMS produc- tion. A recent study demonstrated that MT can be methylated to DMS in aerobic bacteria through the Mto Mts activity of a membrane bound methyltransferase CH2O CH4 H2S CO2 encoded by the gene mddA (Carrion et al., 2015). H2O2 H2S Te mddA gene was found widely distributed in phylogenetically diverse bacteria and several iso- Figure 9.1 Simplifed MT cycle and the key lates tested showed that the presence of the mddA synthesis/degradation enzymes/pathways identifed. gene correlated with the ability to form DMS Main MT sources include degradation of DMSP by from MT. Based on metagenomic datasets, it was the demethylation/demethiolation pathway (Dmd), degradation of methionine by methionine-gamma- estimated that the mddA gene may be present in lyase (MegL) or methyl transfer to sulfde by thiol 5–76% of soil bacteria (Carrión et al., 2015). In a methyltransferases (Tmt) from methoxylated aromatic

subsequent study, Carrion and colleagues showed compounds (CH3-O-R) or S-adenosylmethionine that although only a small proportion of MT (SAM). Cleavage of DMSP by DMSP-lyases (Ddd) produces DMS which can be oxidized to MT (≈ 0.1%) added to a grassland soil was converted by DMS monooxygenase (Dmo). Sinks include to DMS via this pathway, the soil microbial com- (Mto) which degrades MT to

munity contained a phylogenetically diverse group formaldehyde (CH2O), hydrogen sulfde (H2S) and (H O ), methylation of MT to of bacteria, mainly Pseudomonas, Acinetobacter, 2 2 DMS by methyltransferase (Mdd), and degradation Gemmobacter, Phyllobacterium, Rhizobium, Ensifer in methanogens to methane (CH4), carbon dioxide and Sinorhizobium that encoded mddA. (Carrión (CO2) and hydrogen sulfde (H2S) via activity of Mts et al., 2017). It is notable that the gene encoding methyltransferases.

Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Microbial Cycling of Methanethiol | 177 could utilize MT as the carbon and energy source growth of Methanosarcina acetivorans. Further char- were not isolated from the samples. Later, Kiene et acterization indicated that these were also required al. (1986) demonstrated that methane is produced for methylotrophic growth of M. acetivorans on in sediment samples from a variety of habitats DMS (Oelgeschläger and Rother, 2009). Work by including freshwater, alkaline and hypersaline lakes Fu and Metcalf (2015) further showed that MtsF, as well as estuarine salt marshes. Tey also obtained, which was highly up-regulated during growth on from an estuarine salt marsh sediment, the frst MT, and MtsH were capable of transferring the methanogenic , which was capable of metabo- methyl group from MT to coenzyme M, the later lizing MT as the sole source of carbon and energy, also seemed to accept DMS as a substrate (Fu yet did not identify this strain (Kiene et al., 1986). and Metcalf, 2015). Other methanogens that can Following this, Ni and Boone (1991) identifed grow on methylated sulfur compounds have been the frst pure methanogenic strain (Methanolobus described which appear to be obligately methylo- siciliae) from oilfeld water samples using DMS as trophic. Methanomethylovorans hollandica DMS1 is the substrate (Ni and Boone, 1991). Te cultures a MT-degrading methanogen that has been isolated were subsequently shown to use MT as the cata- from the sediment of a eutrophic freshwater pond bolic substrate (Ni and Boone, 1993; Table 9.1). in Nijmegen, Te Netherlands, using a chemostat, Another methanogenic strain, Methanosarcina sp. which enabled high DMS degradation rates by MTP4, was isolated from marine sediment using removing inhibitory metabolites (i.e. hydrogen MT as the sole carbon and energy source (Finster et sulfde) (Lomans et al., 1999a). A closely related al., 1992; Table 9.1). Te biochemical and genetic strain, Methanomethylovorans uponensis, was basis of methanethiol-dependent obtained from a wetland sediment and shared the of Methanosarcina spp. has recently been identifed. ability to grow using methylated sulfur compounds Tree fused methyltransferase-corrinoid enzymes MT and DMS (Cha et al., 2013). Methanogens (MtsD, MtsF and MtsH) were shown by mutational related to Methanomethylovorans hollandica as well analysis to be involved in formation of DMS as a as Methanolobus were also present in a lab-scale metabolic intermediate during carboxidotrophic bioreactor able degrade 6mM MT in the infowing

Table 9.1 Anaerobic archaea and bacteria that can utilize MT as a carbon and energy source Isolate Isolation source Reference Archaea Methanolobus siciliae HI350 Oil feld water Ni and Boone (1991) Methanolobus bombayensis B-1a Marine sediment Kadam et al. (1994) Methanolobus taylorii GS-16 Estuarine sediment Oremland and Boone (1994) Methanolobus sp. strain SODA Bioreactor treating MT at pH 10 van Leerdam et al. (2008a) Methanolobus sp. strain WR1 Bioreactor treating MT at pH ≥ 8 van Leerdam et al. (2008b) Methanosarcina sp. MTP4 Marine sediment Finster et al. (1992) Methanosarcina semesiae MD1 Mangrove sediment Lyimo et al. (2000) Methanomethylovorans hollandica DMS1 Lake sediment Lomans et al. (1999a) Methanohalophilus zhilinae WeN5Ta Alkaline lake sediment Mathrani et al. (1988) Methanohalophilus oregonense WAL1a Alkaline saline aquifer Liu et al. (1990) Bacteria Desulfotomaculum sp. MTS5 Anaerobic fermentor Tanimoto and Bak (1994) Desulfotomaculum sp. SDN4 Anaerobic fermentor Tanimoto and Bak (1994) Desulfosarcina sp. SD1 Mangrove sediment Lyimo et al. (2009) Thiobacillus sp. ASN1 Salt marsh Visscher and Taylor (1993b) aThese strains were isolated using DMS as the carbon and energy source but not tested directly for their ability to grow on MT.

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medium which had been inoculated with sludge of Tiobacillus ASN-1, which was isolated from a from a paper mill wastewater treatment plant Spartina-dominated salt marsh, were also shown to (de Bok et al., 2006). Further Methanolobus isolates metabolize MT with and nitrite as electron (strains WR1 and SODA) were obtained by van acceptor (Taylor and Visscher, 1993b). Leerdam and colleagues from bioreactors treating In a study that used cultivation-independent MT under alkaline conditions at pH of 8 and above methods to identify methanogen and SRB and pH10, respectively, and were shown to grow populations degrading MT (and DMS) in the on MT as sole carbon source (van Leerdam et al., environment, Lomans and colleagues found 2008a,b). Additionally, a number of methanogens methanogens closely related to Methanomethylo- from the genera Methanosarcina, Methanohalophilus vorans hollandica to be the dominant MT-degraders and Methanolobus, which can transform DMS to in freshwater sediments (Lomans et al, 2001). methane were isolated from anoxic environments Tis suggests that M. hollandica might be a major including alkaline lake and marine sediments player in the MT cycle in freshwater habitats. To (Table 9.1). Some of these were not tested for their our knowledge, there are as yet no studies focusing growth on MT directly; however, it appears likely on the characterization of anaerobic MT-degrading that because of MT being an intermediate of DMS populations using post-genomic approaches, which metabolism in other methanogens, that these spe- limits our understanding of the identity and distri- cies can also catabolize MT. bution of MT-degrading microorganisms in anoxic In high-sulfate ecosystems such as marine and environments. salt marsh sediments, SRB degrade MT to hydrogen sulfde and carbon dioxide using sulfate as the fnal electron acceptor (Kiene and Visscher, 1987; Kiene Conclusions and Capone, 1988; Tanimoto and Bak, 1994). A Te biogeochemical cycling of methylated sulfur relatively small number of SRB that grow on MT compounds is brought about by a wide range of and sulfate have been isolated so far. Tese belong interconnected and interacting metabolic path- to the genera Desulfotomaculum and Desulfosarcina, ways and microorganisms. Te intense study of which were obtained from laboratory scale metha- the metabolism of DMSP and DMS during recent nogenic fermenters (Tanimoto and Bak, 1994) and years has brought the role of MT as an intermedi- mangrove sediments (Lyimo et al., 2009). ate of their microbial degradation into focus. MT is A number of studies have been carried out to relevant as a malodourous compound in a range of understand the interaction between methanogens industries but also in a medical context, therefore a and SRB using 2-bromoethanesulfonic (BES) more detailed understanding of the , and molybdate as specifc inhibitors of methano- genetics and ecology of MT degrading micro- genesis and sulfate reduction, respectively (Kiene et organisms has considerable beneft to aid in the al., 1986; Lomans et al., 1997). MT was reported exploitation of the properties of microorganisms to be a non-competitive substrate for methanogens for removal of MT, and even to help understand the although competition between methanogens and role of organic sulfur metabolism in plants, animals SRB was observed for DMS at low substrate con- and humans. Te identifcation of several key genes centrations (< 10 μM DMS) (Kiene et al., 1986). that encode enzymes of MT metabolism facilitates Tis microbial interaction may have signifcant a more holistic analysis of the role of diverse bac- impact on the fate of MT in the environment, teria and archaea using metagenomics and related particularly in marine sediments which have high approaches in the future and will lead to a beter sulfate concentrations. understanding of MT cycling in the environment. In addition to sulfate, nitrate is also used as At the same time, advances in uncovering the role an electron acceptor by MT-degrading micro- of MT metabolism in human disease may only rep- organisms. One example for this metabolism is resent the beginning of a beter understanding how Desulfotomaculum sp. SDN4 that was isolated from sulfur metabolism afects human health, providing a methanogenic thermophilic fermentor and which an important scope to explore both host and micro- was able to use nitrate as terminal electron accep- biome associated pathways of MT production and tor (Tanimoto and Bak, 1994). DMS-grown cells degradation in more detail.

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