Skip to main content
NCBI home page
Environmental Microbiology Reports logoLink to Environmental Microbiology Reports
. 2024 Sep 4;16(5):e70002. doi: 10.1111/1758-2229.70002

Metabolic versatility of aerobic methane‐oxidizing bacteria under anoxia in aquatic ecosystems

Biao Li 1,2, Zhendu Mao 3, Jingya Xue 4, Peng Xing 1,2, Qinglong L Wu 1,2,3,5,6,✉
PMCID: PMC11374530  PMID: 39232853

Abstract

The potential positive feedback between global aquatic deoxygenation and methane (CH4) emission emphasizes the importance of understanding CH4 cycling under O2‐limited conditions. Increasing observations for aerobic CH4‐oxidizing bacteria (MOB) under anoxia have updated the prevailing paradigm that MOB are O2‐dependent; thus, clarification on the metabolic mechanisms of MOB under anoxia is critical and timely. Here, we mapped the global distribution of MOB under anoxic aquatic zones and summarized four underlying metabolic strategies for MOB under anoxia: (a) forming a consortium with oxygenic microorganisms; (b) self‐generation/storage of O2 by MOB; (c) forming a consortium with non‐oxygenic heterotrophic bacteria that use other electron acceptors; and (d) utilizing alternative electron acceptors other than O2. Finally, we proposed directions for future research. This study calls for improved understanding of MOB under anoxia, and underscores the importance of this overlooked CH4 sink amidst global aquatic deoxygenation.

Besides conventional aerobic oxidation pathway, MOB has four underlying metabolic strategies under anoxia: (i) forming a consortium with oxygenic microorganisms; (ii) self‐generation/storage of O2 by MOB; (iii) forming a consortium with non‐oxygenic heterotrophic bacteria that use other electron acceptors; (iv) and utilizing alternative electron acceptors other than O2, such as NOX −, N2O, and Fe(III).

graphic file with name EMI4-16-e70002-g002.jpg

INTRODUCTION

Dissolved oxygen (DO) in aquatic ecosystems has declined over the past half‐century, primarily because of global warming (Breitburg et al., 2018; Jane et al., 2021; Schmidtko et al., 2017; Zhi et al., 2023). Besides reducing the solubility of O2, greenhouse gas‐driven warming raises metabolic rates and results in accelerating aquatic O2 consumption (Keeling et al., 2010). Meanwhile, warming‐induced intensified stratification accounts for significant O2 loss by impeding ventilation, hindering O2 transport from the surface to deeper layers (Helm et al., 2011). Moreover, once exposed to hypoxic or anoxic conditions due to deoxygenation, methanogens potentially activate the production of CH4, a greenhouse gas which is 28 times more potent in holding heat than carbon dioxide (CO2) on a centennial timescale (Tollefson, 2022). This means that deoxygenation is likely to exert positive feedback on CH4 emission (Bonaglia et al., 2022; Chronopoulou et al., 2017). Given that aquatic ecosystems contribute nearly half of global CH4 emission (Rosentreter et al., 2021), even slight deoxygenation may trigger serious ecological consequences.

CH4 emission is a balance between production and oxidation (He et al., 2018; Zhu et al., 2020). Depending on whether the electron acceptor is O2, CH4 oxidation can be divided into aerobic and anaerobic CH4 oxidation. Since O2 is a thermodynamically favourable electron acceptor for CH4 oxidation, aerobic CH4‐oxidizing bacteria (MOB), a group of bacteria that grow on CH4 as their sole source of carbon and energy (Kalyuzhnaya et al., 2019), are considered a critical biofilter to mitigate CH4 emission (Mao et al., 2022). In the absence of O2, anaerobic CH4‐oxidizing archaea (ANME) consume CH4 via a reverse methanogenic pathway coupled with other electron acceptors like sulfate (SO4 2−), nitrate (NO3 −), and metal oxides (Boetius et al., 2000; Raghoebarsing et al., 2006; Beal et al., 2009; Haroon et al., 2013), and the NC10‐bacteria related to Candidatus Methylomirabilis oxyfera (M. oxyfera) produce O2 intracellularly from nitrite (NO2 −) for CH4 oxidation (Ettwig et al., 2010). The established norm in microbial ecology is that CH4 metabolisms by MOB are O2‐dependent; thus, MOB are traditionally believed to thrive only in oxic environments, especially at the oxic–anoxic interface where diffusion of CH4 from below and DO from above provide a suitable niche for them (Reim et al., 2012). Nevertheless, increasing studies have demonstrated that MOB can survive and even actively metabolize CH4 in environments with very low or even undetectable O2 concentrations (Figure S1). These unexpected findings have substantially updated the understanding that the ecological amplitude of MOB is broader than previously recognized, and that the role of MOB in mitigating global warming under anoxia may be neglected (Reis et al., 2024). However, our understanding of the metabolic strategies employed by MOB under anoxia remains limited.

To fill the knowledge gap, we mapped the presence of MOB in global anoxic environments, summarized four metabolic strategies for MOB survival under anoxia, and proposed directions for future research.

UBIQUITOUS PRESENCE OF MOB IN ANOXIC ENVIRONMENTS

An absolute anoxic environment (i.e., zero O2 concentration) cannot be directly detected because no assay has detection limit low enough, typically reaching only nanomolar level (Berg et al., 2022). However, many bacteria can sense and utilize O2 in nanomolar concentrations that escape most detection attempts, making a vague boundary between aerobes and anaerobes (Bristow et al., 2016; Kalvelage et al., 2015; Stolper et al., 2010; Trojan et al., 2021). This capability among traditionally considered aerobes indicates that they play a broader environmental role and possess more versatile metabolic pathways than those currently recognized (Berg et al., 2022; Trojan et al., 2021). Here, we operationally define the “apparent anoxic” conditions as those where DO levels drop below the detection limit of O2 sensing technologies (Canfield & Kraft, 2022). Recent studies have identified MOB in anoxic environments globally, especially in aquatic ecosystems including oceans, hydrothermal vents, lakes, and reservoirs (Figure 1 and Table 1). Some cultures and strains enriched or isolated from these habitats also have shown that MOB actively consume CH4 under O2‐limited or depleted conditions (Figure 1 and Table 1). Intriguingly, several studies have identified MOB as the sole CH4 consumer with no detection of anaerobic methanotrophs (e.g., ANME‐type archaea and NC10‐bacteria) (Dershwitz et al., 2021; Milucka et al., 2015). Moreover, Gammaproteobacterial‐MOB, such as Methylobacter and Methylomonas, are frequently found in anoxic environments (He et al., 2022; Li et al., 2023; Thamdrup et al., 2019). These MOB under anoxia play an unexpected important role in mitigating CH4 emission. For instance, MOB were identified as responsible for 40.3% of CH4 reduction in the anoxic sediments of Lake Fuxian (Li et al., 2023), and nearly complete consumption of CH4 in the anoxic waters of Lake Lago di Cadagno (Milucka et al., 2015). Although these types of MOB sometimes catalyse CH4 under anoxia non‐syntrophically (e.g., Kits et al., 2015), in more cases they appear to aggregate with other microorganisms (e.g., Shi et al., 2021), indicating elaborate metabolic mechanisms are involved.

FIGURE 1.

FIGURE 1

Open in a new tab

Global distribution of MOB under anoxia in typical aquatic ecosystems. The purple, brown, blue, black, green, and red filled circle represent observations from the ocean, hydrothermal vent, lake water, lake sediment, reservoir, and enrichment culture or isolated strain from the above habitats respectively.

TABLE 1.

Aerobic methane‐oxidizing bacteria (MOB) under anoxia in typical aquatic ecosystems and laboratory systems.

Habitats Depth (W/S) a Temp (°C) O2 detection limits (μmol/L) Key MOB taxa Electron acceptors Metabolic pathways b Accession number c References
Lake Constance S: 0.5–9 ‐ 0.3 γ‐MOB ‐ ‐ ‐ Rahalkar et al. (2009)
Lake Pavin W: 65 4 1 Methylobacter ‐ ‐ ‐ Biderre‐Petit et al. (2011)
Lake Lugano W: 135–220 ‐ 1 Methylobacter ‐ ‐ ‐ Blees et al. (2014)
Strain obtained from Jay Gulledge ‐ 30 0.05 Methylomonas NO3 − c/d PRJNA258394 Kits et al. (2015)
Lake Lago di Cadagno W: 13 ‐ 1 γ‐MOB O2 a ‐ Milucka et al. (2015)
Tu'i Malila hydrothermal vent W: 1876 10–12 ‐ Methylothermaceae NO3 − c/d IMG2623620619 Skennerton et al. (2015)
Lake Zug W: 180–190 ‐ 0.02 Methylococcales O2, NO3 −, NO2 −, Fe(III), Mn(IV) ‐ PRJNA977988 Oswald et al. (2016) and Schorn et al. (2024)
Lake Fryxell S: 10 2.1–2.4 ‐ Dehalococcoides Humic acids ‐ ‐ Saxton et al. (2016)
Lake Kinneret S: 26–41 20 0.03125 Methylobacter Fe(III) c ‐ Bar‐Or et al. (2017)
Lake Vault S: 0–2.5 ‐ ‐ Methylobacter Fe(III), Mn(IV) ‐ ‐ Martinez‐Cruz et al. (2017)
Markandeya Reservoir W: 12–22 23 2 d Methylocaldum, Methylomonas NO3 −, NO2 − a/c/d ‐ Naqvi et al. (2018)
Eastern tropical North Pacific W: 100–400 14 0.001–0.01 e Methylcoccales ‐ ‐ PRJNA263621 Thamdrup et al. (2019)
Lake L1‐L4 W: 7–9.6 3.4–3.9 0.3125 Methylobacter, Crenothrix NO3 −, NO2 − a/c/d ‐ Cabrol et al. (2020)
Enrichment from wastewater treatment plant ‐ ‐ ‐

Methylocaldum,

Methylocystis, Methylobacter

O2 a ‐ Chai et al. (2020)
Lake Lacamas W: 5–18 10–20 ‐ Methylobacter NO3 − c PRJNA524776 van Grinsven et al. (2020, 2021)
Enrichment from Lake Taihu ‐ 30 ‐ Methylomonas O2 a ‐ Chang et al. (2021)
Stains purified from the spent medium ‐ 25 ‐ Methylocystis, Methylosinus O2 b ‐ Dershwitz et al. (2021)
A meander bend of the Red River S: 3000 26 ‐ Methylomicrobium, Methylobacillus ‐ a/c/d ‐ Pienkowska et al. (2021)
Lake Lovojärvi W: 11 7.5 1 Methylococcales NO3 −, NO2 − d PRJEB38681 Rissanen et al. (2021)
Enrichment from wetland sediment in Hangzhou ‐ ‐ ‐ Methylocystis, Methylosinus SeO4 2− c SRP136677, SRP136696, SRP136790, SRP136859 Shi et al. (2021)
Lake Qalluuraq S: 25–50 10 ‐ Methylobacter, Methylocaldum Fe(III) c MN788533‐MN788604, SRP234857 He et al. (2022)
Lake Sempach S: 0–10 ‐ ‐ Methylococcaceae, Methylocystis, Crenothrix O2 a/b ‐ Su et al. (2022)
Lake Fuxian S: 0–10 13 0.625 Methylomonas Fe(III) c OEP002958 Li et al. (2023)
Strains isolated from hot spring in Italy ‐ ‐ ‐ Methylacidiphilum N2O d CP065957 Awala et al. (2024)
Open in a new tab
a

Depth (W/S): depth for MOB present in the anoxic zone of water column (W) or sediment (S), with unit of m and cm, respectively.

b

Metabolic pathways: (a) forming a consortium with oxygenic microorganisms; (b) self‐generation/ storage of O2 by MOB; (c) forming a consortium with non‐oxygenic heterotrophic bacteria that use other electron acceptors; (d) utilizing alternative electron acceptors other than O2.

c

Accession number is only for (meta)genomic sequencing data but not for amplicon sequencing data.

d

O2 detection limit from Labasque et al. (2004).

e

O2 detection limit from Revsbech et al. (2009).

METABOLIC VERSATILITY OF MOB UNDER ANOXIA

The conventional aerobic oxidation pathway of MOB has been extensively reviewed in previous studies (Hanson & Hanson, 1996; Kalyuzhnaya et al., 2019). Briefly, initiated by CH4 monooxygenase (MMO) to split the O—O bonds under the presence of O2, MOB activate and oxidize CH4 to methanol (Hanson & Hanson, 1996; Murrell et al., 2000), followed by oxidation to formaldehyde by methanol dehydrogenase (MDH) with a subunit of MxaF or XoxF (Chistoserdova, 2016; McDonald & Murrell, 1997). Formaldehyde oxidation can be catalysed by several enzymes, including the tetrahydromethanopterin‐ (H4MPT‐) or tetrahydrofolate linked and formaldehyde dehydrogenases (FADH, possibly also XoxF) (Kalyuzhnaya et al., 2019). Besides being oxidized via formate to CO2 by FADH and formate dehydrogenase (FDH), another part of formaldehyde is assimilated into the biomass via the Serine pathway or the ribulose monophosphate (RuMP) pathway (Chistoserdova et al., 2005). However, MMO inhibition under anoxia suppresses the initial oxidation step in CH4 transformation to methanol (Roslev & King, 1995). Therefore, MOB require distinct strategies to use CH4 as a carbon and energy source under anoxia, as summarized below (Figure 2).

FIGURE 2.

FIGURE 2

Open in a new tab

Conventional aerobic metabolic pathway in oxic environments and four potential metabolic strategies under anoxia for MOB: (i) forming a consortium with oxygenic organisms; (ii) self‐generation/storage of O2 by MOB; (iii) forming a consortium with non‐oxygenic heterotrophic bacteria that use other electron acceptors; (iv) utilizing alternative electron acceptors other than O2, such as NOX −, N2O, and Fe(III).

Forming a consortium with oxygenic microorganisms (Figure 2i)

Coupling CH4 oxidation with O2 respiration yields more energy for MOB relative to other electron acceptors except for NO2 − (Table S1). Since only few MOB types possess key genes encoding NOx − reduction (Kits et al., 2015; Rissanen et al., 2021) and O2 is toxic to NOx − reducers (Lu & Imlay, 2021), MOB will be thermodynamically favourable to utilize O2 as the electron acceptors when trace O2 is simultaneously present with other electron acceptors. Consequently, MOB are frequently found to aggregate with oxygenic organisms under anoxia (Milucka et al., 2015; Oswald et al., 2015; Thamdrup et al., 2019). To date, only few biological pathways are known to produce O2 (Ettwig et al., 2012; Kraft et al., 2022): photosynthesis (Dismukes et al., 2001), nitric oxide (NO) dismutation (Ettwig et al., 2010), chlorate respiration (van Ginkel et al., 1996), detoxification of reactive oxygen species (ROS) (Apel & Hirt, 2004), and a new pathway by ammonia‐oxidizing archaea (AOA) which has not been completely resolved (Kraft et al., 2022). The O2 produced by these oxygenic pathways can be immediately consumed by aerobic microorganisms (including MOB) through a conventional aerobic respiration, making O2 undetectable (Figure 3, Milucka et al., 2015).

FIGURE 3.

FIGURE 3

Open in a new tab

Metabolic pathway for MOB under anoxia. CH4 oxidation module: MMO, methane monooxygenase; MDH, methanol dehydrogenase; FADH, formaldehyde dehydrogenase; FDH, formate dehydrogenase; LMW‐OC, low molecular weight organic carbon. O2 generation/storage module: Mbn, methanobactin synthetase; BcHr, bacteriohemerythrin. EET (extracellular electron transfer) module: Rib, riboflavin synthetase; Phz, phenazine synthetase; PilA, the key protein to constitute electrically conductive pili (e‐pili); MHC, putative multiheme c‐type cytochromes; T1SS, Type 1 secretion system. Nitrogen cycle module: ON, Organic nitrogen; Nif, nitrogenase; AMO, ammonia monooxygenase; HAO, hydroxylamine dehydrogenase; NAP, nitrate reductase; Nrt, nitrate/nitrite transporter; NIR, nitrite reductase; NOR, nitric oxide reductase; NOD, nitric oxide dismutase; NOZ, nitrous oxide reductase. Sulfur cycle module: TauD, taurine dioxygenase; Hyd, sulfhydrogenase; SOX, sulfite oxidase. ClO4 − respiration module: Pcr, perchlorate reductase; Clr, chlorate reductase; Cld, chlorite dismutase.

In the permanently stratified Lake Lago di Cadagno, where the euphotic layer extends below the oxic–anoxic interface, abundant MOB affiliated to Gammaproteobacteria were attached to photosynthetic algae and actively consume CH4 in the anoxic water column (Milucka et al., 2015). Likewise, Methylomonas was also enriched alongside the oxygenic NC10‐bacteria in a NO2 −‐dependent anaerobic CH4 oxidation system, indicating that Methylomonas was fuelled by O2 through NO2 −‐derived NO dismutation pathway (Chang et al., 2021). A recent study found abundant and diverse nitric oxide dismutase (NOD) genes affiliated not only with NC10‐bacteria but also with diverse heterotrophic bacteria, such as Flavihumibacter, Pseudomonas and a new order (UBA11136) of Alphaproteobacteria (Elbon et al., 2024; Zhu et al., 2017). This implies that different combinations between MOB and oxygenic bacteria may widely occur in anoxic environments. Additionally, in a CH4‐based membrane biofilm batch reactor that used perchlorate (ClO4 −) as the electron acceptor for anaerobic CH4 oxidation, multiple MOB genera, including Methylococcus, Methylomonas, and Methylocystis accounted for 20%–27% of the total bacteria and were likely involved in CH4 oxidation (Lv et al., 2019). Since perchlorate‐reducing bacteria reduce ClO4 − to chlorite (ClO2 −), which is further intracellularly disproportionated to chloride (Cl−) and O2 (Miller et al., 2014), MOB could use O2 produced by perchlorate respiration to oxidize CH4 and instant O2 recycling would maintain anoxic conditions. Because numerous heterotrophic bacteria have a capacity to produce ROS (Diaz et al., 2013), which can be detoxified to O2 by superoxide dismutase (SOD) and catalase (CAT) with hydrogen peroxide (H2O2) as the intermediate product (Apel & Hirt, 2004), it is speculated that MOB can use ROS‐detoxified O2 to oxidize CH4 under anoxia. However, to the best of our knowledge, the detoxification of ROS coupled with CH4 oxidation mediated by MOB has not been reported up to now.

Self‐generation/storage of O2 by MOB (Figure 2ii)

Self‐generation of O2 by MOB is dependent on the extracellular copper‐binding peptides called methanobactins (MBs, Figure 3) (Dershwitz et al., 2021). Based on MBs, some Alphaproteobacterial‐MOB have novel acquisition systems for copper ions (Cu2+) (DiSpirito et al., 2016), that are critical for regulating MMO expression (Murrell et al., 2000). Intriguingly, MBs can bind with multiple metal ions besides Cu2+ and reduce some bound ions (Choi et al., 2006; Lu et al., 2017). By using an H2 18O tracing method, two Alphaproteobacterial‐MOB strains, Methylosinus trichosporium OB3b and Methylocystis sp. strain SB2, were found to produce 36O2 when incubated in the presence of either Au3+, Cu2+, or Ag+ (Dershwitz et al., 2021). Furthermore, 36O2 was generated by coupling Fe3+ reduction and H2 18O oxidation with the help of MBs (Dershwitz et al., 2021). This is the first evidence verifying “self‐generation” of O2 by MOB and the ability to express MBs (thereby generate O2) may be an important pathway for facilitating CH4 removal under anoxia. Notably, most MOB found in anoxic zones are affiliated to Gammaproteobacteria (Figure 1 and Table 1). Although some Gammaproteobacterial‐MOB can secrete copper‐binding compounds (Choi et al., 2010), none of these have been verified to have genes encoding MBs biosynthesis as of yet (Semrau et al., 2020). Therefore, it is possible that Gammaproteobacterial‐MOB generate O2 via some unknown mechanism or utilize O2 produced by others through MBs production. Similarly, AOA, which have long been considered O2‐dependent, were also recently found to self‐produce O2 (Kraft et al., 2022). These studies indicate that “self O2 generation” maybe an overlooked capacity for conventional aerobic microorganisms surviving anoxic environments.

Storage of O2 by MOB mainly relies on the O2‐carrier bacteriohemerythrin (Figure 3), which shuttles O2 from the cytoplasm of the cell to the intra‐cytoplasmic membranes for consumption by particulate MMO (Chen et al., 2012). Under O2‐limited conditions, one notable change in the transcriptomes of MOB, such as Methylomonas denitrificans FJG1, Methylococcus capsulatus (Bath), and Methylomicrobium buryatense 5GB1C, is the upregulation of genes encoding bacteriohemerythrin (Chen et al., 2012; Gilman et al., 2017; Kits et al., 2015). This means that O2 from episodically inputs like turbidity currents from surface water into the anoxic zone, is likely stored or consumed quickly instead of being detected during sampling campaigns (Blees et al., 2014). However, further field evidences are required to reveal the importance of O2 storage by MOB for CH4 removal under anoxic conditions.

Forming a consortium with non‐oxygenic heterotrophic bacteria that use other electron acceptors (Figure 2iii)

MOB can transform CH4 to low molecular weight compounds via the pyrophosphate‐mediated glycolytic pathway under micro‐oxic conditions (Kalyuzhnaya et al., 2013; Khanongnuch et al., 2023). These compounds can be utilized as carbon sources by heterotrophic bacteria, establishing a syntrophic link between methanotrophy and heterotrophy (He et al., 2015). Moreover, trace O2 seems to only trigger the reaction instead of acting as an electron acceptor for CH4 oxidation, because the amount of O2 consumption is much lower than that of CH4 oxidation. In a membrane biofilm reactor, MOB transformed CH4 to methanol and excreted part of it out of the cells, which was further assimilated by methanol‐utilizing denitrifiers at a low O2:CH4 ratio (0.06, Xu et al., 2020).

Syntrophy is not limited to micro‐oxic environments. Even under anoxic conditions, MOB can still form a consortium with heterotrophic bacteria. Some field investigations found that MOB may couple CH4 oxidation with NOx − reduction in the anoxic water columns of freshwater lakes (Rissanen et al., 2018; van Grinsven et al., 2021). An in situ observation also revealed the co‐existence of MOB and iron reducers below the sulfate–methane transition zone (SMTZ) in the sediment of a boreal estuary, indicating a potential linkage between them by using Fe(III) as an alternative electron acceptors (Myllykangas et al., 2020). When solid electron acceptors such as Fe(III) oxides dominate anoxic environments, extracellular electron transfer (EET), including putative multiheme c‐type cytochromes (MHCs), electrically conductive pili (e‐pili), and electron shuttles (such as flavins, phenazine, and rebredoxin), is likely to play a critical role (Shi et al., 2016). Our recent study showed that the pilA gene encoding e‐pili, the genes encoding putative and extracellular periplasmic MHCs, and the genes encoding electron shuttles particularly riboflavin, including ribA, ribBA, ribD, ribE, ribF, and ribH, were all present in Methylomonas (Figure 3, Li et al., 2023). Furthermore, MOB form a consortium with some heterotrophic bacteria to utilize ferrihydrite as an alternative electron acceptor under anoxia with the help of riboflavin (Li et al., 2023). Given the ubiquitous presence of electron shuttles and low molecular weight compounds in natural anoxic sediments, it is possible that similar MOB consortia exist and function in situ. This has been further verified in Arctic lake sediments, where MOB actively oxidize 13CH4 and generate intermediates like methanol, formaldehyde, and formate, which fuel ferric reduction via dissimilatory iron‐reducing bacteria (He et al., 2022). In an anoxic membrane biofilm batch reactor, MOB excrete some fermentation by‐products including formate, acetate, propionate, butyrate, and lactate for heterotrophic bacteria (such as Pseudoxanthomonas, Piscinibacter, and Rhodocyclaceae), and the latter reduce selenate to selenite and elemental selenium by proteins annotated as periplasmic NO3 − reductases (Shi et al., 2021).

Utilizing alternative electron acceptors other than O2 (Figure 2iv)

Previous studies have shown that anaerobic methanotrophs can link CH4 oxidation to the reduction of alternative electron acceptors under anoxia (Cai et al., 2021; Oni & Friedrich, 2017). In addition to the conventional O2‐dependent pathway for CH4 oxidation, some MOB have the potential to use alternative electron acceptors such as NOx − and Fe(III) under anoxia when oxygenic organisms are absent (Kits et al., 2015; Zheng et al., 2020). It has been reported that a Gammaproteobacterial‐MOB Methylomonas denitrificans sp. nov. strain FJG1T, couples CH4 oxidation to NO3 − reduction when DO was undetectable, releasing N2O as a terminal product (Kits et al., 2015). Transcriptomic analysis further revealed the upregulation of genes encoding the denitrification pathway upon NO3 − amendment under anoxia within this MOB strain (Kits et al., 2015). Some acidophilic Alphaproteobacterial‐MOB strains, such as Methylocella tundrae T4 and Methylacidiphilum caldifontis IT6, possess N2O reductase genes and were recently shown to consume CH4 under anoxia using N2O as the terminal electron acceptor (Awala et al., 2024). However, the genetic potential for N2O respiration by Gammaproteobacterial‐MOB, which are ubiquitously distributed in anoxic aquatic systems, remains constrained. Besides coupling CH4 oxidation and NO3 −/N2O reduction, key genes encoding N2 fixation (nifDHK) were present within the genome of MOB in freshwater lakes and oxygen minimum zones of the oceans (Figure 3, Jayakumar & Ward, 2020; Rissanen et al., 2021; Khanongnuch et al., 2022), indicating that MOB also have genetic potential for nitrogen fixation under O2‐limited environments (Murrell & Dalton, 1983). Additionally, MOB strains belonging to Alpha‐ and Gammaproteobacteria, Methylosinus sp. LW4 and Methylomonas sp. LW13, were found to couple ferrihydrite reduction with CH4 oxidation under O2 limitation (initial DO of 0.89 mg/L). Although genes encoding outer membrane cytochromes were absent within Methylomonas sp. LW13, the expression of one conspicuous gene cluster encoding the Type 1 secretion system (T1SSs) was upregulated (Figure 3, Zheng et al., 2020), which is characterized by the transport of proteins from the cytoplasm to the outside of the cell and is potentially involved in EET (Kanonenberg et al., 2013; Thomas et al., 2014). Recently, a repertoire of genes encoding sulfur oxidation (Figure 3, soxYZAB, dsrABEFHCMKLJOPN, sqr, sorAB, tetH, and doxAD) within the genome of Methylovirgula thiovorans strain HY1 suggested potential utilization of various reduced sulfur compounds for growth (Gwak et al., 2022). However, no genetic or experimental evidence of SO4 2− reduction has been found in MOB until now, perhaps because of the low thermodynamic energy yield to support life from this reaction under anoxia (Table S1, Knittel & Boetius, 2009).

FUTURE PERSPECTIVES

Firstly, new branches of MOB have been found continuously over the past two decades (Schmitz et al., 2021), indicating that the full complement of methanotroph diversity is not yet known (Ahmadi & Lackner, 2024). Observations of MOB in anoxic aquatic ecosystems have updated the paradigm that MOB can only inhabit oxic conditions (Reis et al., 2024). Thus, it is necessary to expand investigations in global anoxic areas to unveil new members, especially the oxygen minimum zone of oceans and anoxic hypolimnion layers of deep lakes. Secondly, the source of the oxygen atom remains enigmatic when CH4 is transformed to CO2 using alternative electron acceptors by MOB independently or in combination with other microorganisms (Shi et al., 2021) (Figure 2iii,iv). Given the ancient atmosphere was characterized by limited O2 but abundant CH4 (Kasting, 1993), metabolic flexibility under anoxia besides conventional aerobic pathway maybe an important lifestyle for MOB before O2 was present on Earth. Therefore, clarifying the source of the oxygen atom is helpful in revealing the mechanisms of adaptation to hypoxic and anoxic environments and in understanding the metabolic strategies of MOB in ancient atmospheric circumstances. Additionally, with more MOB strains isolated from anoxic aquatic environments, the corresponding genomic information is needed to construct their synergistic evolutionary history with Earth, especially during the Great Oxygenation Event (GOE) (Lyons et al., 2014). Thirdly, although recent case studies have shown that CH4 oxidation mediated by MOB under anoxia significantly reduces CH4 emission in freshwater lakes (Li et al., 2023; Milucka et al., 2015), it is urgent to re‐evaluate the contribution of MOB to CH4 mitigation on a larger anoxic scale in aquatic ecosystems, which account for half of the global CH4 emission (Rosentreter et al., 2021). Lastly, if NOX − are the terminal electron acceptors, Gammaproteobacterial‐MOB may lead to a net production of the far more potent greenhouse gas N2O (Griffis et al., 2017; Stein & Lidstrom, 2024), resulting in further climate change even though CH4 is consumed (Kits et al., 2015). Therefore, it is necessary to consider the net greenhouse effect of CH4 oxidation by MOB under O2‐limited conditions. Given the positive feedback between greenhouse CH4 emission and ubiquitous aquatic deoxygenation (Bonaglia et al., 2022), the role of MOB in anoxic environments needs to be thoroughly understood.

AUTHOR CONTRIBUTIONS

Biao Li: Conceptualization; data curation; visualization; writing – original draft; writing – review and editing; funding acquisition. Zhendu Mao: Methodology; software; visualization. Jingya Xue: Methodology; visualization; software; funding acquisition. Peng Xing: Writing – review and editing; funding acquisition; supervision. Qinglong L. Wu: Supervision; conceptualization; writing – review and editing; funding acquisition.

CONFLICT OF INTEREST STATEMENT

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Supporting information

Data S1. Supporting information

EMI4-16-e70002-s001.docx (232.2KB, docx)

ACKNOWLEDGEMENTS

This study was jointly supported by National Natural Science Foundation of China (32201334, 42293264, 92251304 and 42207256), Special Funds of Scientific and Technological Innovation for Carbon Peak and Neutrality in Jiangsu Province (BK20220015), Project of National Key Basic Research and Development (2023YFF1304501), Project of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou, GML20220017), Chinese Postdoctoral Science Foundation (2022M721661), Outstanding Postdoctoral Project in Jiangsu Province (2022ZB455), and Project of State Key Laboratory of Lake Science and Environment (2022SKL019).

Li, B. , Mao, Z. , Xue, J. , Xing, P. & Wu, Q.L. (2024) Metabolic versatility of aerobic methane‐oxidizing bacteria under anoxia in aquatic ecosystems. Environmental Microbiology Reports, 16(5), e70002. Available from: 10.1111/1758-2229.70002

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions. Supporting Materials can be accessed at Figshare and the link is http://doi.org/10.6084/m9.figshare.26755312.

REFERENCES

  1. Ahmadi, F. & Lackner, M. (2024) Recent findings in methanotrophs: genetics, molecular ecology, and biopotential. Applied Microbiology and Biotechnology, 108, 60. [DOI] [PubMed] [Google Scholar]
  2. Apel, K. & Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399. [DOI] [PubMed] [Google Scholar]
  3. Awala, S.I. , Gwak, J.H. , Kim, Y. , Jung, M.Y. , Dunfield, P.F. , Wagner, M. et al. (2024) Nitrous oxide respiration in acidophilic methanotrophs. Nature Communications, 15, 4226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bar‐Or, I. , Elvert, M. , Eckert, W. , Kushmaro, A. , Vigderovich, H. , Zhu, Q.Z. et al. (2017) Iron‐coupled anaerobic oxidation of methane performed by a mixed bacterial‐archaeal community based on poorly reactive minerals. Environmental Science & Technology, 51, 12293–12301. [DOI] [PubMed] [Google Scholar]
  5. Beal, E.J. , House, C.H. & Orphan, V.J. (2009) Manganese‐ and iron‐dependent marine methane oxidation. Science, 325, 184–187. [DOI] [PubMed] [Google Scholar]
  6. Berg, J.S. , Ahmerkamp, S. , Pjevac, P. , Hausmann, B. , Milucka, J. & Kuypers, M.M.M. (2022) How low can they go? Aerobic respiration by microorganisms under apparent anoxia. FEMS Microbiology Reviews, 46, fuac006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Biderre‐Petit, C. , Jezequel, D. , Dugat‐Bony, E. , Lopes, F. , Kuever, J. , Borrel, G. et al. (2011) Identification of microbial communities involved in the methane cycle of a freshwater meromictic lake. FEMS Microbiology Ecology, 77, 533–545. [DOI] [PubMed] [Google Scholar]
  8. Blees, J. , Niemann, H. , Wenk, C. , Zopfi, J. , Schubert, C. , Kirf, M. et al. (2014) Micro‐aerobic bacterial methane oxidation in the chemocline and anoxic water column of deep south‐alpine Lake Lugano (Switzerland). Limnology and Oceanography, 59, 311–324. [Google Scholar]
  9. Boetius, A. , Ravenschlag, K. , Schubert, C. , Rickert, D. , Widdel, F. , Gieseke, A. et al. (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407, 623–626. [DOI] [PubMed] [Google Scholar]
  10. Bonaglia, S. , Rütting, T. , Kononets, M. , Stigebrandt, A. , Santos, I.R. & Hall, P.O.J. (2022) High methane emissions from an anoxic fjord driven by mixing and oxygenation. Limnology and Oceanography Letters, 7, 392–400. [Google Scholar]
  11. Breitburg, D. , Levin, L.A. , Oschlies, A. , Gregoire, M. , Chavez, F.P. , Conley, D.J. et al. (2018) Declining oxygen in the global ocean and coastal waters. Science, 359, eaam7240. [DOI] [PubMed] [Google Scholar]
  12. Bristow, L.A. , Dalsgaard, T. , Tiano, L. , Mills, D.B. , Bertagnolli, A.D. , Wright, J.J. et al. (2016) Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters. Proceedings of the National Academy of Sciences of the United States of America, 113, 10601–10606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cabrol, L. , Thalasso, F. , Gandois, L. , Sepulveda‐Jauregui, A. , Martinez‐Cruz, K. , Teisserenc, R. et al. (2020) Anaerobic oxidation of methane and associated microbiome in anoxic water of northwestern Siberian lakes. Science of the Total Environment, 736, 139588. [DOI] [PubMed] [Google Scholar]
  14. Cai, C. , Zhang, X. , Wu, M. , Liu, T. , Lai, C.‐Y. , Frank, J. et al. (2021) Roles and opportunities for microbial anaerobic oxidation of methane in natural and engineered systems. Energy & Environmental Science, 14, 4803–4830. [Google Scholar]
  15. Canfield, D.E. & Kraft, B. (2022) The ‘oxygen’ in oxygen minimum zones. Environmental Microbiology, 24, 5332–5344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chai, F.G. , Li, L. , Xue, S. & Liu, J.X. (2020) Auxiliary voltage enhanced microbial methane oxidation co‐driven by nitrite and sulfate reduction. Chemosphere, 250, 126259. [DOI] [PubMed] [Google Scholar]
  17. Chang, J. , Wu, Q. , Yan, X.X. , Wang, H. , Lee, L.W. , Liu, Y.C. et al. (2021) Enhancement of nitrite reduction and enrichment of Methylomonas via conductive materials in a nitrite‐dependent anaerobic methane oxidation system. Environmental Research, 193, 110565. [DOI] [PubMed] [Google Scholar]
  18. Chen, K.H. , Wu, H.H. , Ke, S.F. , Rao, Y.T. , Tu, C.M. , Chen, Y.P. et al. (2012) Bacteriohemerythrin bolsters the activity of the particulate methane monooxygenase (pMMO) in Methylococcus capsulatus (Bath). Journal of Inorganic Biochemistry, 111, 10–17. [DOI] [PubMed] [Google Scholar]
  19. Chistoserdova, L. (2016) Lanthanides: new life metals? World Journal of Microbiology and Biotechnology, 32, 138. [DOI] [PubMed] [Google Scholar]
  20. Chistoserdova, L. , Vorholt, J.A. & Lidstrom, M.E. (2005) A genomic view of methane oxidation by aerobic bacteria and anaerobic archaea. Genome Biology, 2005(6), 208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Choi, D.W. , Bandow, N.L. , McEllistrem, M.T. , Semrau, J.D. , Antholine, W.E. , Hartsel, S.C. et al. (2010) Spectral and thermodynamic properties of methanobactin from gamma‐proteobacterial methane oxidizing bacteria: a case for copper competition on a molecular level. Journal of Inorganic Biochemistry, 104, 1240–1247. [DOI] [PubMed] [Google Scholar]
  22. Choi, D.W. , Do, Y.S. , Zea, C.J. , McEllistrem, M.T. , Lee, S.W. , Semrau, J.D. et al. (2006) Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn (II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b. Journal of Inorganic Biochemistry, 100, 2150–2161. [DOI] [PubMed] [Google Scholar]
  23. Chronopoulou, P. , Shelley, F. , Pritchard, W. , Maanoja, S. & Trimmer, M. (2017) Origin and fate of methane in the eastern tropical North Pacific oxygen minimum zone. The ISME Journal, 11, 1386–1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dershwitz, P. , Bandow, N.L. , Yang, J. , Semrau, J.D. , McEllistrem, M.T. , Heinze, R.A. et al. (2021) Oxygen generation via water splitting by a novel biogenic metal ion‐binding compound. Applied and Environmental Microbiology, 87, e0028621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Diaz, J.M. , Hansel, C.M. , Voelker, B.M. , Mendes, C.M. , Andeer, P.F. & Zhang, T. (2013) Widespread production of extracellular superoxide by heterotrophic bacteria. Science, 340, 1223–1226. [DOI] [PubMed] [Google Scholar]
  26. Dismukes, G.C. , Klimov, V.V. , Baranov, S.V. , Kozlov, Y.N. , DusGupta, J. & Tyryshkin, A. (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 98, 2170–2175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. DiSpirito, A.A. , Semrau, J.D. , Murrell, J.C. , Gallagher, W.H. , Dennison, C. & Vuilleumier, S. (2016) Methanobactin and the link between copper and bacterial methane oxidation. Microbiology and Molecular Biology Reviews, 80, 387–409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Elbon, C.E. , Stewart, F.J. & Glass, J.B. (2024) Novel Alphaproteobacteria transcribe genes for nitric oxide transformation at high levels in a marine oxygen‐deficient zone. Applied and Environmental Microbiology, 90, e02099‐23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ettwig, K. , Butler, M. , Le Paslier, D. , Pelletier, E. , Mangenot, S. , Kuypers, M. et al. (2010) Nitrite‐driven anaerobic methane oxidation by oxygenic bacteria. Nature, 464, 543–548. [DOI] [PubMed] [Google Scholar]
  30. Ettwig, K.F. , Speth, D.R. , Reimann, J. , Wu, M.L. , Jetten, M.S.M. & Keltjens, J.T. (2012) Bacterial oxygen production in the dark. Frontiers in Microbiology, 3, 273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gilman, A. , Fu, Y.F. , Hendershott, M. , Chu, F. , Puri, A.W. , Smith, A.L. et al. (2017) Oxygen‐limited metabolism in the methanotroph Methylomicrobium buryatense 5GB1C. PeerJ, 5, e3945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Griffis, T.J. , Chen, Z. , Baker, J.M. , Wood, J.D. , Millet, D.B. , Lee, X. et al. (2017) Nitrous oxide emissions are enhanced in a warmer and wetter world. Proceedings of the National Academy of Sciences of the United States of America, 114, 12081–12085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Gwak, J.H. , Awala, S.I. , Nguyen, N.L. , Yu, W.J. , Yang, H.Y. , von Bergen, M. et al. (2022) Sulfur and methane oxidation by a single microorganism. Proceedings of the National Academy of Sciences of the United States of America, 119, e2114799119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hanson, R. & Hanson, T. (1996) Methanotrophic bacteria. Microbiological Reviews, 60, 439–471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Haroon, M. , Hu, S. , Shi, Y. , Imelfort, M. , Keller, J. , Hugenholtz, P. et al. (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature, 500, 567–570. [DOI] [PubMed] [Google Scholar]
  36. He, R. , Wang, J. , Pohlman, J.W. , Jia, Z. , Chu, Y.X. , Wooller, M.J. et al. (2022) Metabolic flexibility of aerobic methanotrophs under anoxic conditions in Arctic lake sediments. The ISME Journal, 16, 78–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. He, R. , Wooller, M.J. , Pohlman, J.W. , Tiedje, J.M. & Leigh, M.B. (2015) Methane‐derived carbon flow through microbial communities in arctic lake sediments. Environmental Microbiology, 17, 3233–3250. [DOI] [PubMed] [Google Scholar]
  38. He, Z.F. , Zhang, Q.Y. , Feng, Y.D. , Luo, H.W. , Pan, X.L. & Gadd, G.M. (2018) Microbiological and environmental significance of metal‐dependent anaerobic oxidation of methane. Science of the Total Environment, 610–611, 759–768. [DOI] [PubMed] [Google Scholar]
  39. Helm, K.P. , Bindoff, N.L. & Church, J.A. (2011) Observed decreases in oxygen content of the global ocean. Geophysical Research Letters, 38, L23602. [Google Scholar]
  40. Jane, S.F. , Hansen, G.J.A. , Kraemer, B.M. , Leavitt, P.R. , Mincer, J.L. , North, R.L. et al. (2021) Widespread deoxygenation of temperate lakes. Nature, 594, 66–70. [DOI] [PubMed] [Google Scholar]
  41. Jayakumar, A. & Ward, B.B. (2020) Diversity and distribution of nitrogen fixation genes in the oxygen minimum zones of the world oceans. Biogeosciences, 17, 5953–5966. [Google Scholar]
  42. Kalvelage, T. , Lavik, G. , Jensen, M.M. , Revsbech, N.P. , Löscher, C. , Schunck, H. et al. (2015) Aerobic microbial respiration in oceanic oxygen minimum zones. PLoS One, 10, e0133526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kalyuzhnaya, M. , Gomez, O. & Murrell, J. (2019) The methane‐oxidizing bacteria (Methanotrophs). In: Taxonomy, genomics and ecophysiology of hydrocarbon‐degrading microbes, Gewerbestrasse: Springer Nature Switzerland AG; pp. 245–278. [Google Scholar]
  44. Kalyuzhnaya, M. , Yang, S. , Rozova, O. , Smalley, N. , Clubb, J. , Lamb, A. et al. (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nature Communications, 4, 2785. [DOI] [PubMed] [Google Scholar]
  45. Kanonenberg, K. , Schwarz, C.K.W. & Schmitt, L. (2013) Type I secretion systems—a story of appendices. Research in Microbiology, 164, 596–604. [DOI] [PubMed] [Google Scholar]
  46. Kasting, J.F. (1993) Earth's early atmosphere. Science, 259, 920–926. [DOI] [PubMed] [Google Scholar]
  47. Keeling, R.F. , Körtzinger, A. & Gruber, N. (2010) Ocean deoxygenation in a warming world. Annual Review of Marine Science, 2, 199–299. [DOI] [PubMed] [Google Scholar]
  48. Khanongnuch, R. , Mangayil, R. & Rissanen, A.J. (2023) Conversion of methane to organic acids is a widely found trait among gammaproteobacterial methanotrophs of freshwater lake and pond ecosystems. Microbiology Spectrum, 11, e01742‐23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Khanongnuch, R. , Mangayil, R. , Svenning, M.M. & Rissanen, A.J. (2022) Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems. ISME Communications, 2, 85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Kits, K.D. , Klotz, M.G. & Stein, L.Y. (2015) Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1. Environmental Microbiology, 17, 3219–3232. [DOI] [PubMed] [Google Scholar]
  51. Knittel, K. & Boetius, A. (2009) Anaerobic oxidation of methane: Progress with an unknown process. Annual Review of Microbiology, 63, 311–334. [DOI] [PubMed] [Google Scholar]
  52. Kraft, B. , Jehmlich, N. , Larsen, M. , Bristow, L. , Könneke, M. , Thamdrup, B. et al. (2022) Oxygen and nitrogen production by an ammonia‐oxidizing archaeon. Science, 375, 97–100. [DOI] [PubMed] [Google Scholar]
  53. Labasque, T. , Chaumery, C. , Aminot, A. & Kergoat, G. (2004) Spectrophotometric Winkler determination of dissolved oxygen: re‐examination of critical factors and reliability. Marine Chemistry, 88, 53–60. [Google Scholar]
  54. Li, B. , Tao, Y. , Mao, Z. , Gu, Q. , Han, Y. , Hu, B. et al. (2023) Iron oxides act as an alternative electron acceptor for aerobic methanotrophs in anoxic lake sediments. Water Research, 234, 119833. [DOI] [PubMed] [Google Scholar]
  55. Lu, X. , Gu, W.Y. , Zhao, L.D. , Farhan, M.F.U. , DiSpirito, A.A. , Semrau, J.D. et al. (2017) Methylmercury uptake and degradation by methanotrophs. Science Advances, 3, e1700041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Lu, Z. & Imlay, J.A. (2021) When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence. Nature Reviews. Microbiology, 19, 774–785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Lv, P.L. , Shi, L.D. , Wang, Z. , Rittmann, B. & Zhao, H.P. (2019) Methane oxidation coupled to perchlorate reduction in a membrane biofilm batch reactor. Science of the Total Environment, 667, 9–15. [DOI] [PubMed] [Google Scholar]
  58. Lyons, T.W. , Reinhard, C.T. & Planavsky, N.J. (2014) The rise of oxygen in Earth's early ocean and atmosphere. Nature, 506, 307–315. [DOI] [PubMed] [Google Scholar]
  59. Mao, S.H. , Zhang, H.H. , Zhuang, G.C. , Li, X.J. , Liu, Q. , Zhou, Z. et al. (2022) Aerobic oxidation of methane significantly reduces global diffusive methane emissions from shallow marine waters. Nature Communications, 13, 7309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Martinez‐Cruz, K. , Leewis, M.C. , Herriott, I.C. , Sepulveda‐Jauregui, A. , Anthony, K.W. , Thalasso, F. et al. (2017) Anaerobic oxidation of methane by aerobic methanotrophs in sub‐Arctic lake sediments. Science of the Total Environment, 607–608, 23–31. [DOI] [PubMed] [Google Scholar]
  61. McDonald, I.R. & Murrell, J.C. (1997) The methanol dehydrogenase structural gene mxaf and its use as a functional gene probe for methanotrophs and methylotrophs. Applied and Environmental Microbiology, 63, 3218–3224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Miller, L.G. , Baesman, S.M. , Carlstrom, C.I. , Coates, J.D. & Oremland, R.S. (2014) Methane oxidation linked to chlorite dismutation. Frontiers in Microbiology, 5, 275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Milucka, J. , Kirf, M. , Lu, L. , Krupke, A. , Lam, P. , Littmann, S. et al. (2015) Methane oxidation coupled to oxygenic photosynthesis in anoxic waters. The ISME Journal, 9, 1991–2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Murrell, J.C. & Dalton, H. (1983) Nitrogen fixation in obligate methanotrophs. Microbiology, 129, 3481–3486. [Google Scholar]
  65. Murrell, J.C. , Gilbert, B. & McDonald, I.R. (2000) Molecular biology and regulation of methane monooxygenase. Archives of Microbiology, 173, 325–332. [DOI] [PubMed] [Google Scholar]
  66. Murrell, J.C. , McDonald, I.R. & Gilbert, B. (2000) Regulation of expression of methane monooxygenases by copper ions. Trends in Microbiology, 8, 221–225. [DOI] [PubMed] [Google Scholar]
  67. Myllykangas, J. , Rissanen, A.J. , Hietanen, S. & Jilbert, T. (2020) Influence of electron acceptor availability and microbial community structure on sedimentary methane oxidation in a boreal estuary. Biogeochemistry, 148, 291–309. [Google Scholar]
  68. Naqvi, S.W.A. , Lam, P. , Narvenkar, G. , Sarkar, A. , Naik, H. , Pratihary, A. et al. (2018) Methane stimulates massive nitrogen loss from freshwater reservoirs in India. Nature Communications, 9, 1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Oni, O. & Friedrich, M. (2017) Metal oxide reduction linked to anaerobic methane oxidation. Trends in Microbiology, 25, 88–90. [DOI] [PubMed] [Google Scholar]
  70. Oswald, K. , Milucka, J. , Brand, A. , Hach, P. , Littmann, S. , Wehrli, B. et al. (2016) Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters. Limnology and Oceanography, 61, S101–S118. [Google Scholar]
  71. Oswald, K. , Milucka, J. , Brand, A. , Littmann, S. , Wehrli, B. , Kuypers, M.M.M. et al. (2015) Light‐dependent aerobic methane oxidation reduces methane emissions from seasonally stratified lakes. PLoS One, 10, e0132574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Pienkowska, A. , Glodowska, M. , Mansor, M. , Buchner, D. , Straub, D. , Kleindienst, S. et al. (2021) Isotopic labeling reveals microbial methane oxidation coupled to Fe(III) mineral reduction in sediments from an as‐contaminated aquifer. Environmental Science & Technology Letters, 8, 832–837. [Google Scholar]
  73. Raghoebarsing, A.A. , Pol, A. , van de Pas‐Schoonen, K.T. , Smolders, A.J. , Ettwig, K.F. , Rijpstra, W.I. et al. (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature, 440, 918–921. [DOI] [PubMed] [Google Scholar]
  74. Rahalkar, M. , Deutzmann, J. , Schink, B. & Bussmann, I. (2009) Abundance and activity of methanotrophic bacteria in littoral and profundal sediments of Lake Constance (Germany). Applied and Environmental Microbiology, 75, 119–126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Reim, A. , Luke, C. , Krause, S. , Pratscher, J. & Frenzel, P. (2012) One millimetre makes the difference: high‐resolution analysis of methane‐oxidizing bacteria and their specific activity at the oxic‐anoxic interface in a flooded paddy soil. The ISME Journal, 6, 2128–2139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Reis, P.C.J. , Tsuji, J.M. , Weiblen, C. , Schiff, S.L. , Scott, M. , Stein, L.Y. et al. (2024) Enigmatic persistence of aerobic methanotrophs in oxygen‐limiting freshwater habitats. The ISME Journal, 18, wrae041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Revsbech, N.P. , Larsen, L.H. , Gundersen, J. , Dalsgaard, T. , Ulloa, O. & Thamdrup, B. (2009) Determination of ultra‐low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnology and Oceanography: Methods, 7, 371–381. [Google Scholar]
  78. Rissanen, A.J. , Saarela, T. , Jäntti, H. , Buck, M. , Peura, S. , Aalto, S.L. et al. (2021) Vertical stratification patterns of methanotrophs and their genetic controllers in water columns of oxygen‐stratified boreal lakes. FEMS Microbiology Ecology, 97, fiaa252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Rosentreter, J. , Borges, A. , Deemer, B. , Holgerson, M. , Liu, S. , Song, C. et al. (2021) Half of global methane emissions come from highly variable aquatic ecosystem sources. Nature Geoscience, 14, 225–230. [Google Scholar]
  80. Roslev, P. & King, G.M. (1995) Aerobic and anaerobic starvation metabolism in methanotrophic bacteria. Applied and Environmental Microbiology, 61, 1563–1570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Saxton, M.A. , Samarkin, V.A. , Schutte, C.A. , Bowles, M.W. , Madigan, M.T. , Cadieux, S.B. et al. (2016) Biogeochemical and 16S rRNA gene sequence evidence supports a novel mode of anaerobic methanotrophy in permanently ice‐covered Lake Fryxell, Antarctica. Limnology and Oceanography, 61, S119–S130. [Google Scholar]
  82. Schmidtko, S. , Stramma, L. & Visbeck, M. (2017) Decline in global oceanic oxygen content during the past five decades. Nature, 542, 335–339. [DOI] [PubMed] [Google Scholar]
  83. Schmitz, R.A. , Peeters, S.H. , Versantvoort, W. , Picone, N. , Pol, A. , Jetten, M.S.M. et al. (2021) Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles. FEMS Microbiology Reviews, 45, fuab007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Schorn, S. , Graf, J.S. , Littmann, S. , Hach, P.F. , Lavik, G. , Speth, D.R. et al. (2024) Persistent activity of aerobic methane‐oxidizing bacteria in anoxic lake waters due to metabolic versatility. Nature Communications, 15, 5293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Semrau, J.D. , DiSpirito, A.A. , Obulisamy, P.K. & Kang‐Yun, C.S. (2020) Methanobactin from methanotrophs: genetics, structure, function and potential applications. FEMS Microbiology Letters, 367, fnaa045. [DOI] [PubMed] [Google Scholar]
  86. Shi, L. , Dong, H. , Reguera, G. , Beyenal, H. , Lu, A. , Liu, J. et al. (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Reviews. Microbiology, 14, 651–662. [DOI] [PubMed] [Google Scholar]
  87. Shi, L.D. , Lv, P.L. , McIlroy, S.J. , Wang, Z. , Dong, X.L. , Kouris, A. et al. (2021) Methane‐dependent selenate reduction by a bacterial consortium. The ISME Journal, 15, 3683–3692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Skennerton, C.T. , Ward, L.M. , Michel, A. , Metcalfe, K. , Valiente, C. , Mullin, S. et al. (2015) Genomic reconstruction of an uncultured hydrothermal vent Gammaproteobacterial methanotroph (family Methylothermaceae) indicates multiple adaptations to oxygen limitation. Frontiers in Microbiology, 6, 1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Stein, L.Y. & Lidstrom, M.E. (2024) Greenhouse gas mitigation requires caution. Science, 384, 1068–1069. [DOI] [PubMed] [Google Scholar]
  90. Stolper, D.A. , Revsbech, N.P. & Canfield, D.E. (2010) Aerobic growth at nanomolar oxygen concentrations. Proceedings of the National Academy of Sciences of the United States of America, 107, 18755–18760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Su, G. , Zopfi, J. , Niemann, H. & Lehmann, M.F. (2022) Multiple groups of methanotrophic bacteria mediate methane oxidation in anoxic lake sediments. Frontiers in Microbiology, 13, 864630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Thamdrup, B. , Steinsdóttir, H. , Bertagnolli, A. , Padilla, C. , Patin, N. , Garcia‐Robledo, E. et al. (2019) Anaerobic methane oxidation is an important sink for methane in the ocean's largest oxygen minimum zone. Limnology and Oceanography, 64, 2569–2585. [Google Scholar]
  93. Thomas, S. , Holland, I.B. & Schmitt, L. (2014) The type 1 secretion pathway—the haemolysin system and beyond. Biochimica et Biophysica Acta (BBA) ‐ Molecular Cell Research, 1843, 1629–1641. [DOI] [PubMed] [Google Scholar]
  94. Tollefson, J. (2022) Scientists raise alarm over ‘dangerously fast’ growth in atmospheric methane. Nature. Available from: 10.1038/d41586-022-00312-2 [DOI] [PubMed] [Google Scholar]
  95. Trojan, D. , Garcia‐Robledo, E. , Meier, D.V. , Hausmann, B. , Revsbech, N.P. , Eichorst, S.A. et al. (2021) Microaerobic lifestyle at nanomolar O2 concentrations mediated by low‐affinity terminal oxidases in abundant soil bacteria. mSystems, 6, e00250‐21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. van Ginkel, C.G. , Rikken, G.B. , Kroon, A.G.M. & Kengen, S.W.M. (1996) Purification and characterization of chlorite dismutase: a novel oxygen‐generating enzyme. Archives of Microbiology, 166, 321–326. [DOI] [PubMed] [Google Scholar]
  97. van Grinsven, S. , Sinninghe Damste, J.S. , Abdala Asbun, A. , Engelmann, J.C. , Harrison, J. & Villanueva, L. (2020) Methane oxidation in anoxic lake water stimulated by nitrate and sulfate addition. Environmental Microbiology, 22, 766–782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. van Grinsven, S. , Sinninghe Damsté, J.S. , Harrison, J. , Polerecky, L. & Villanueva, L. (2021) Nitrate promotes the transfer of methane‐derived carbon from the methanotroph Methylobacter sp. to the methylotroph Methylotenera sp. in eutrophic lake water. Limnology and Oceanography, 66, 878–891. [Google Scholar]
  99. Xu, X. , Zhu, J. , Thies, J. & Wu, W. (2020) Methanol‐linked synergy between aerobic methanotrophs and denitrifiers enhanced nitrate removal efficiency in a membrane biofilm reactor under a low O2:CH4 ratio. Water Research, 174, 115595. [DOI] [PubMed] [Google Scholar]
  100. Zheng, Y. , Wang, H. , Liu, Y. , Zhu, B. , Li, J. , Yang, Y. et al. (2020) Methane‐dependent mineral reduction by aerobic methanotrophs under hypoxia. Environmental Science & Technology Letters, 7, 606–612. [Google Scholar]
  101. Zhi, W. , Klingler, C. , Liu, J.T. & Li, L. (2023) Widespread deoxygenation in warming rivers. Nature Climate Change, 13, 1105–1113. [Google Scholar]
  102. Zhu, B. , Bradford, L. , Huang, S. , Szalay, A. , Leix, C. , Weissbach, M. et al. (2017) Unexpected diversity and high abundance of putative nitric oxide dismutase (Nod) genes in contaminated aquifers and wastewater treatment systems. Applied and Environmental Microbiology, 83, e02750‐16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Zhu, Y. , Purdy, K. , Eyice, Ö. , Shen, L. , Harpenslager, S. , Yvon‐Durocher, G. et al. (2020) Disproportionate increase in freshwater methane emissions induced by experimental warming. Nature Climate Change, 10, 685–690. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Data S1. Supporting information

EMI4-16-e70002-s001.docx (232.2KB, docx)

Data Availability Statement

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions. Supporting Materials can be accessed at Figshare and the link is http://doi.org/10.6084/m9.figshare.26755312.

Articles from Environmental Microbiology Reports are provided here courtesy of Wiley

RESOURCES