Abstract
Climate change due to the continuous increase in the release of green-house gasses associated with anthropogenic activity has made a significant impact on the sustainability of life on our planet. Methane (CH4) is a green-house gas whose concentrations in the atmosphere are on the rise. CH4 measurement is important for both the environment and the safety at the industrial and household level. Methanotrophs are distinguished for their unique characteristic of using CH4 as the sole source of carbon and energy, due to the presence of the methane monooxygenases that oxidize CH4 under ambient temperature conditions. This has attracted interest in the use of methanotrophs in biotechnological applications as well as in the development of biosensing systems for CH4 quantification and monitoring. Biosensing systems using methanotrophs rely on the use of whole microbial cells that oxidize CH4 in presence of O2, so that the CH4 concentration is determined in an indirect manner by measuring the decrease of O2 level in the system. Although several biological properties of methanotrophic microorganisms still need to be characterized, different studies have demonstrated the feasibility of the use of methanotrophs in CH4 measurement. This review summarizes the contributions in methane biosensing systems and presents a prospective of the valid use of methanotrophs in this field.
Key points
• Methanotroph environmental relevance in methane oxidation
• Methanotroph biotechnological application in the field of biosensing
• Methane monooxygenase as a feasible biorecognition element in biosensors
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Introduction
Methane (CH4) is an odorless and colorless gas widely used in the generation of electricity and as a heating fuel. It is an important green-house gas (GHG) being the second biggest contributor to global warming, with a global warming potential 28 times higher than carbon dioxide (CO2) over a 100-year period since it is a stronger absorber of the infrared radiation with a thermal effect (wavelength 2.5-15 µm) that is emitted by the Earth when exposed to temperatures above 0 °C (Myhre et al. 2013). CH4 concentration in the atmosphere has shown a continuous increase, from an estimated value of around 700 ppb prior to the industrial revolution up to 1895.7 ppb in 2021 (Etheridge et al. 1998; NOAA 2022). Such increase is mostly attributed to anthropogenic activities, as it is estimated that more than 50% of CH4 emissions in the atmosphere are related to industrial activities, livestock farming, agriculture, the use of fossil fuels, biomass burning, rice paddies, among others (Saunois et al. 2020; IPCC 2021; EEA 2022; Zhang et al. 2022).
CH4 sinks are determinant since they contribute to the decrease CH4 levels in the atmosphere. Hydroxyl (OH) and chlorine (Cl) radicals constitute the primary sink, followed by microbial oxidation in soils by methanotrophic microorganisms (Saunois et al. 2020; Jackson et al. 2021). Methanotrophs are prokaryotes recognized for their unique capacity to utilize CH4 as a sole source of carbon and energy and are known to play a crucial role in the Earth’s biogeochemical carbon cycle (Hanson and Hanson 1996). They are widely distributed in the environment and have an important role in the consumption of atmospheric CH4, as well as in the capture of CH4 generated biologically or geothermally before it is released in the environment, acting as biofilters (Kalyuzhnaya et al. 2019). It is estimated that aerobic methanotrophs in upland soils consume up to 30 Tg CH4 per year, which corresponds to 6% of the global methane sinking capability (Shukla et al. 2013). The ability of methanotrophs to oxidize CH4 at ambient temperature has attracted increasing attention because of their potential use in bioremediation strategies, biotechnological applications, and the development of biosensing systems (Strong et al. 2015; Kwon et al. 2019; Gęsicka et al. 2021; Guerrero-Cruz et al. 2021). Particularly, CH4 detection and monitoring is important for both the environmental health and the human safety in domestic and industrial settings (Lawrence 2006; Aldhafeeri et al. 2020). Leaking of natural gas, which is comprised of 95% of CH4, is an important issue, since it is estimated that each year, just in the United States, around 9 million of tons of natural gas leak in the atmosphere during extraction transport and storage, directly contributing to the increase of CH4 concentration. Moreover, CH4 is highly flammable and forms explosive mixtures in the range of 5–15% v/v in air; indeed, accidental leaks have led to the occurrence of important explosions. Besides the risk associated to its flammability, inhalation of CH4 can cause suffocation and can be fatal if the levels of oxygen (O2) are lower that 12% (Lawrence 2006; Patel 2017).
Different analytical methods to detect CH4 are available; among them are gas chromatography (GC), select ion flow tube-mass spectrometry (SIFT-MS), infrared (IR) spectroscopy, and electrochemistry. Each of these techniques has its own advantages and disadvantages. For example, GC is widely used in gas detection, and it has a low LOD being suitable to detect small leaks of CH4; however, it needs cumbersome and costly instrumentation, making it very difficult to perform measurements outside of a laboratory. SIFT-MS is instead a portable system with the potential to be used in different environments; it has been recently used for the breath analysis; however, the sensitivity and specificity are issues that still need to be optimized (Langford 2023). IR spectroscopy allows a selective and specific detection of gases; however, it is a laboratory-based technique, requires qualified personnel, and has high running costs (Kamieniak et al. 2015). Due to the constraints of the classical methods, new reliable and cost-effective techniques should be developed. In this context, sensors have achieved great notoriety and have proven to be useful from environmental to clinical applications (Bonini et al. 2020, 2021; Vivaldi et al. 2020; Poma et al. 2021). Sensing systems for CH4 measurement using optical, calorimetric, pyroelectric, and electrochemical transduction methods have been described in literature. A comparison of the different detection methods in CH4 sensing has been provided by Aldhafeeri and colleagues (Aldhafeeri et al. 2020), where the advantages and disadvantages have been clearly presented. For example, optical detection sensing methods are non-destructive and able to operate without oxygen, but these are costly, have a high-power consumption, and have some selectivity issues. Instead, devices using calorimetry as transduction method have good selectivity and simplistic design and are easy to manufacture; however, these require harsh operating conditions and have a short life span and low detection accuracy. The characteristics of electrochemical sensors like their low-cost, high sensitivity, ease of use, portability, ease of miniaturization and the possibility to perform a remote monitoring made them a valid alternative in the control of generated greenhouse gasses at their source (Lawrence 2006; Kamieniak et al. 2015). Electrochemical CH4 detection can be achieved through its direct oxidation on the electrode surface; however, this approach needs aprotic solvents and specific electrolytes. Alternatively, the direct adsorption of CH4 onto a noble metal (e.g., platinum) electrode surface can be employed. Semi-conductive metals oxides like tin oxide are also used to produce solid state sensors, but these systems mostly operate at high temperatures (above 400 °C) to oxidize CH4 and suffer from poor selectivity, even though the use of filters containing noble metals catalysts and dopants can reduce this problem (Lawrence 2006; Sekhar et al. 2016). In this scenario, methanotrophs able to oxidize CH4 at ambient temperature and pressure may represent a valid alternative for the development of innovative CH4 biosensing systems using the whole cells or the enzymes participating in CH4 oxidation. Considering as well the variety of environments where methanotrophs can be isolated, the sensing devices could be suited to different applications. This minireview provides an overview on biosensing systems using methanotrophic bacteria in combination with electrochemical transduction techniques, focusing on the characteristics of methanotrophs as well as on the description of biosensing systems so far developed for CH4 detection, quantification, and monitoring.
Methanotrophic microorganisms
Methanotrophs are microorganisms able to oxidize CH4 under aerobic or anaerobic conditions using different electron acceptors. They are ubiquitous in the environment, as their presence has been demonstrated in a variety of terrestrial and aquatic ecosystems (e.g., soil, mud, rivers, sediments, and sewage water), including extreme environments (e.g., hot springs, alkaline lakes, and permafrost) (Trotsenko and Khmelenina 2002; Semrau and DiSpirito 2019; Houghton et al. 2019; Guerrero-Cruz et al. 2021). Methanotrophs described up to date belong to the phyla Proteobacteria, Verrucomicrobia, and NC10. In addition, members of the Archaea domain have also been found (Kalyuzhnaya et al. 2019; Guerrero-Cruz et al. 2021).
Aerobic methanotrophs use oxygen as the electron acceptor during the oxidation of CH4 to methanol as shown in reaction (1):
On the contrary, in anaerobic methanotrophic archaea sulfate is used as the final electron acceptor (Knittel and Boetius 2009; Bhattarai et al. 2019), according to the reaction (2):
In aerobic methanotrophs, the CH4 oxidation is catalyzed by the metalloenzymes, known as methane monooxygenases (MMOs), able to break the strong C-H bond (∆H = 105 kcal/mol) (Banerjee et al. 2019). The methyl-coenzyme M reductase is thought to be involved in the oxidation of CH4 in anaerobic conditions (Bhattarai et al. 2019; Thauer 2019).
Methane monooxygenases (MMOs)
In aerobic methanotrophs, two types of MMOs are known, i.e., the membrane-bound particulate methane monooxygenase (pMMO) and the cytoplasmatic enzyme soluble methane monooxygenase (sMMO) (Ross and Rosenzweig 2017). Nearly all methanotrophs possess the pMMO enzyme, while sMMO is only present in just a few methanotrophs such as Methylococcus capsulatus strain Bath, and other bacterial species belonging to the genera Methylosinus, Methylocystis, Methylomicrobium, and Methylomonas (Murreil et al. 2000; Khider et al. 2021). Both sMMO and pMMO oxidase CH4, but they are different in structure, active site composition, and substrate selectivity (Sirajuddin and Rosenzweig 2015; Chan et al. 2021). The enzyme pMMO is a copper-dependent protein including only one hydroxylase component, which is a trimer of around 300 kDa containing three subunits PmoA, PmoB, and PmoC (Fig. 1a) (Khider et al. 2021). pMMO can also oxidase n-alkanes and n-alkenes (Sirajuddin and Rosenzweig 2015). The difficulties associated with the isolation and solubilization of the membrane enzyme pMMO have led to a better characterization of the less prevalent enzyme sMMO; these studies have mostly focused on two bacterial species, namely, Methylococcus capsulatus (Bath) and Methylosinus trichosporium OB3b. The catalytic activity of sMMO is achieved by three components, the 245 kDa hydroxylase (MMOH), a 16 kDa regulatory protein (MMOB), and the 40 kDa reductase (MMOR) (Fig. 1b–e) (Banerjee et al. 2019). MMOH is an homodimeric protein composed of three subunits (α, β, and γ), with a diiron active site present in the α subunit. MMOR is a nicotinamide adenine dinucleotide (NADH)-dependent protein containing flavin adenine dinucleotide (FAD) and an iron sulfur [2Fe-2S] domain, which delivers two electrons to the active center of MMOH through the oxidation of NADH (Ross and Rosenzweig 2017; Banerjee et al. 2019). MMOB forms a complex with MMOH, and its presence is known to increase the catalytic activity (Banerjee et al. 2019). sMMO has a wider substrate range including n-alkanes, n-alkenes, aromatic, and heterocyclic compounds, but only CH4 is relevant for the cell metabolism (Banerjee et al. 2019; Khider et al. 2021). sMMO is encoded by an operon composed of six genes, namely mmoXYZBCD, mmoX, mmoY, mmoZ, codifying for the α, β, and γ subunit of MMOH, respectively, while MMOB and MMOR are encoded by mmoB and mmoC, respectively. An additional gene mmoD is predicted to encode for a regulatory protein (Khider et al. 2021).
The use of biosensing systems in methane quantification
The peculiar ability of methanotrophs to oxidize CH4 has attracted the attention toward their use in the development of biosensing systems for its quantification and monitoring. Bacterial cells, known to use CH4 as a carbon source (Table 1), have been mainly used in combination with electrochemical sensors to measure O2 consumption resulting from the oxidation of CH4 (Fig. 2).
The first works, by Okada et al. 1981 (Okada et al. 1981) and Karube et al. 1982 (Karube et al. 1982), depicted a system composed of two reactors, two oxygen electrodes, and a series of valves and tubes allowing the influx of CH4 and air into the reactors and toward the O2 electrodes under the control of a pump (Fig. 3a). In such systems, only one of the reactors contained the methanotrophic bacteria Methylomonas flagellata, so the difference in the current signal between the O2 electrodes was registered and used as the analytical signal. The decrease in the O2 concentration was directly associated to the CH4 oxidation and shown to be dependent on its concentration. Okada and collaborators (Okada et al. 1981) used M. flagellata bacterial cells entrapped on acetylcellulose filters coated with agar. The system showed a linear response below 6.6 mM, with a limit of detection (LOD) of 13.1 μM. Karube and collaborators (Karube et al. 1982) used instead M. flagellata microbial cells in suspension, obtaining a linear response below 6.6 mM and an LOD of 5 μM. The response of both systems was compared with measurements performed by gas chromatography with a thermal conductivity detector, and a significant correlation was established. However, none of these systems was able to provide a continuous measurement, since oxygen had to be introduced for the measurement and then restored. Subsequent studies by Wen et al. (Wen et al. 2008) and Zhao et al. (Zhao et al. 2009) similarly reported the development of measuring systems based on the use of reactors to quantify the CH4 concentration in the aqueous phase by using electrodes measuring dissolved O2 (Fig. 3b). The reactors contained bacterial strains of Pseudomonas aeruginosa (ME16) and Klebsiella sp. (ME17), both capable of oxidizing CH4, which were co-immobilized in polyvinyl alcohol (PVA), alginate, and boric acid beads. This system showed a linear response in the range of 0.4–2.2 mM, with an LOD of 0.1 mM (Wen et al. 2008). Differently, Zhao et al. only used the Klebsiella sp. strain ME17 immobilized in polyvinyl alcohol (PVA)-boric acid beads. In this work, a linear response from 0-7.1 mM CH4, with an LOD of 88 µM was reported (Zhao et al. 2009). Although these early sensing systems did not allow for an in situ monitoring and continuous measurement, they proved it feasible to measure CH4 using whole bacterial cells.
Schematic representation of CH4 biosensing systems. (a) Sensing system based on the use of CH4 oxidizing bacteria: 1, vacuum pump; 2, sample gas bag; 3, gas sample line; 4, cotton filter; 5, control reactor; 6, reactor containing M. flagellata; 7, O2 electrode; 8, amplifier; 9, recorder; 10, vacuum pump; 11–17, glass stopcocks (Okada et al. 1981; Karube et al. 1982) (reprinted from (Karube et al. 1982) with permission from Elsevier). (b) Sensing system for CH4 measurement in solution: 1, pump; 2, gas valve; 3, sample gas; 4, flow-meter; 5, thermostat magnetic stirrer; 6, magnetic bar; 7, oxygen sensor; 8, phosphate buffer solution; 9, bacterial beads; and 10, datalogger and computer (Wen et al. 2008; Zhao et al. 2009) (reprinted from (Wen et al. 2008) with permission from Elsevier). (c) Entire system (left) microsensor tip (right), composed of a gas and a media capillary. An internal O2 electrode is present in the gas capillary which serves as the O2 reservoir (Damgaard and Revsbech 1997) (reprinted from (Damgaard and Revsbech 1997) with permission from ACS)
Systems for the continuous measurement of CH4 have also been described, for example, from Damgaard and colleagues (Damgaard and Revsbech 1997) who developed a microscale sensor composed of an O2 microsensor and two glass capillaries. One gas capillary served as the O2 reservoir and housed the microsensor, whose tip protruded in the reaction space within the media capillary that contained the bacterial cells of M. trichosporium OB3b (Fig. 3c). This system was based on the counter diffusion principle, i.e., in the presence of CH4 the bacterial cells consumed the O2 from the reservoir and the decrease in O2 concentration was registered by the microsensor; a linear response was obtained range from 0–40 mM of CH4 partial pressure, with a response time of 20–100 s. However, O2 diffusing from the environment may act as a major interferent, so this device would be useful only under anoxic conditions. This system was also tested in presence of other compounds such as H2S, CH3COOH, NH3, CO2 and H2, among them only H2S was determined to be an interferent. In 2001, this microsensor was applied to the measurement of CH4 microprofile in a sewage outlet biofilm, a system where both methanogenesis and methane oxidation occur (Damgaard et al. 2001). In another work, the same authors showed a modification of the aforementioned device by the addition of an external capillary where heterotrophic bacteria such as Agrobacterium radiobacter were introduced. Under those conditions, the O2 present in the environment would be first consumed, avoiding its entrance to the gas capillary and consequently the O2 interference to the signal. A linear range of 0–10 mM CH4 partial pressure was obtained, with a response time of 60 s. This system was applied to the measurement of a CH4 microprofile in a rice paddy soil (Damgaard et al. 1998).
So far, only one study described a sensor using the sMMO enzyme as a biorecognition element instead of the whole cell for the detection of CH4 (Chuang and Engineering 2005). In this proof-of-concept study, the MMOH component from M. capsulatus was immobilized onto a gold electrode previously modified with an oligopeptide. Throughout the application of a potential, electrons were transferred from the electrode to the enzyme catalytic site. Cyclic voltammetry was employed as transduction technique, and acetonitrile (CH3CN) was first used as a substrate to validate the system. An increase in the registered current signal was observed in the presence of increased CH3CN concentrations, and most of this signal was attributed to the MMOH on the electrode. In the presence of different CH4 concentrations, a response was recorded and associated to the presence of the enzyme. However, in contrast to CH3CN, when CH4 was used, an inconsistent response was registered, which could be attributed to the kinetics of CH4 partitioning between gas and liquid phase. Besides of these results, this work showed the practicability of this strategy and demonstrated the feasibility of the direct CH4 measurement.
Conclusions
The development of methane sensing systems is relevant to the industrial and household safety and also to the environment protection. The unique characteristic of methanotrophs using CH4 as the sole source of carbon and energy, due to the presence of MMOs in aerobic environments, has inspired the development of CH4 biosensing systems. So far, just a few studies of this type are available; in such works, an indirect determination of CH4 is mainly performed by using whole bacterial cells and sensors measuring the O2 concentration. These pioneering studies proved the use of bioreactors containing methanotrophs feasible, while later studies progressed toward the development of microsensors performing continuous measurements and characterizing the CH4 microprofile in samples such as lake sediments, rice paddies, and biofilms. The use of the enzyme sMMO as a biorecognition element in the construction of a biosensor for CH4 was depicted in a proof-of-concept study. This work demonstrated the possibility of using this enzyme in the CH4 measurement and paves the way for future applications of MMOs in the set-up of methane sensing devices. The increasing interest in the use of methanotrophs in different biotechnological applications has led to a considerable progress in the understanding of methanotrophs biology. Particularly, the acquired knowledge of the structure and function of MMOs, together with the use of new available strategies for their modification and their heterologous expression, may help in their implementation as biorecognition elements in the development of enzymatic biosensors. There is still work to be done, but we believe that such systems soon could be used.
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Open access funding provided by Università di Pisa within the CRUI-CARE Agreement. The study was funded by Metitech s.r.l. and the Programma Operativo Nazionale (PON) Ricerca Innovazione 2014-2020 (DM 1062/2021). AB was supported by the project CRISPRSENSE funded by Tuscany region, Italy (“DECRT. DIRIG. n. 21607 of 29-11-2021”).
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NP surveyed the literature and wrote the manuscript. NP, AB, and FV designed the structure of the mini-review. D Biagini, MDL, D Bottai, FDF, and AT reviewed and edited the manuscript. All authors read and approved the manuscript.
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Poma, N., Bonini, A., Vivaldi, F. et al. Biosensing systems for the detection and quantification of methane gas. Appl Microbiol Biotechnol 107, 5627–5634 (2023). https://doi.org/10.1007/s00253-023-12629-7
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DOI: https://doi.org/10.1007/s00253-023-12629-7