Isoprene Degradation in the Environment

Exploring the bacterial metabolism of an abundant climate-controlling gas

A short video made in 2015 explaining how we started out on the isoprene project

Isoprene (2-methyl-1,3-butadiene) comprises approximately one third of the total volatile organic compounds emitted to the atmosphere, an amount that is approximately equal to emissions of methane. Although isoprene has a short lifetime in the atmosphere, it has a significant impact on atmospheric chemistry and hence climate. Isoprene in the troposphere leads to the formation of ozone when NOx levels are high. Ozone can act directly as a greenhouse gas and also controls the lifetime of other greenhouse gases, hence, isoprene has a potent effect on global warming. Conversely, isoprene may encourage climate cooling by contributing to the formation of aerosols, which in turn serve as cloud condensation nuclei, resulting in reduced radiative forcing [1, 2].

The vast majority of isoprene emitted to the atmosphere is produced by terrestrial plants (~500 Tg y-1), although isoprene production has also been detected in marine algae, animals (including humans), fungi and bacteria. Isoprene is also produced industrially (~0.8 Tg y-1), where it is used primarily to synthesize polyisoprene rubber (Fig. 1). The exact role of isoprene is unknown in most species, although it appears to be involved in protecting plants from thermal and oxidative stress [1, 2].

Microbes in the environment are a sink for isoprene and constitute a fundamental part of the natural biogeochemical cycle of this important trace gas [3]. Bacterial strains that grow on isoprene as a sole carbon and energy source have been isolated from soil, leaves, and coastal/marine environments [4-7]. However, our knowledge of microbial isoprene cycling is very limited.

Figure 1. The global isoprene cycle, reproduced from McGenity TJ et al [2].

Figure 2. (A) The key isoprene degradation genes and their organisation in Rhodococcus sp. AD45. (B) Schematic of the six proteins that constitute the isoprene monooxygenase protein complex. (C) The proposed pathway for isoprene metabolism in Rhodococcus sp. AD45 (adapted from [8]).

Molecular characterisation of isoprene-degraders have revealed that they contain six genes (isoABCDEF) encoding the isoprene monooxygenase (IsoMO) that catalyses the first step of the isoprene degradation pathway [1, 2]; (Fig.2 A, B). IsoMO is a member of the soluble di-iron monooxygenase (SDIMO) family of proteins and has homology to alkene/aromatic monooxygenases and soluble methane monooxygenase. The role of the later enzyme is also studied by our research group.

Four additional genes, isoGHIJ, are adjacent the IsoMO structural genes and encode enzymes involved in the subsequent steps in isoprene catabolism. A putative pathway for isoprene metabolism has been proposed for Rhodococcus sp. AD45 by van Hylckama Vlieg [8] (Fig. 2 C).

Light microscopy image of Rhodococcus sp. AD45 grown on isoprene

The aim of this ERC funded project (IsoMet) is to obtain a critical, fundamental understanding of the metabolism and ecological importance of biological isoprene degradation and to test the hypothesis that isoprene-degrading bacteria play a crucial role in the biogeochemical isoprene cycle, thus helping to mitigate the effects of this important but neglected climate-active gas. Key objectives are:

To elucidate the biological mechanisms by which isoprene is metabolised.
Develop novel molecular methods to study isoprene biodegradation in the environment.
To understand at the mechanistic level how isoprene cycling by microbes is regulated in the environment.

To learn the latest about our research tune in to the iFAST seminar given by Colin Murrell in June 2021

Video: https://bit.ly/3xwJoEq

This project is funded by the European Research Council

Recent Publications on Isoprene From Our Research Group

Sims, LP; Lockwood, CWJ; Crombie, AT; Bradley, JM; Le Brun, NE; Murrell, JC. (2022) Purification and characterisation of the isoprene monooxygenase from Rhodococcus sp. AD45. Applied and Environmental Microbiology, 88 (7), e00029-22. https://doi.org/10.1128/aem.00029-22
Uttarotai, T.; Sutheeworapong, S.; Crombie, A.T.; Murrell, C.; Mhuantong, W.; Noirungsee, N.; Wangkarn, S.; Bovonsombut, S.; McGenity, T.J.; Chitov, T. (2022) Genome characterisation of an isoprene-degrading Alcaligenes sp. isolated from a tropical restored forest. Biology, 11(4), 519; https://doi.org/10.3390/biology11040519
Dawson, R.A., Rix, G.D., Crombie, A.T and Murrell, J.C. (2022) ‘Omics-guided prediction of the pathway for metabolism of isoprene by Variovorax sp. WS11. Environmental Microbiology 2022 1-14. doi/pdf/10.1111/1462-2920.16149
Dawson, R.A., Crombie, A.T Jansen, R. S., Smith, T.J., Nichol, T. and Murrell, J.C. (2022) Peering down the sink: a review of isoprene metabolism by bacteria. Environmental Microbiology 2022. doi: 10.1111/1462-2920.16325
Carrión, O., Gibson, L., Elias, D.M.O. et al. Diversity of isoprene-degrading bacteria in phyllosphere and soil communities from a high isoprene-emitting environment: a Malaysian oil palm plantation. Microbiome 8, 81 (2020). https://doi.org/10.1186/s40168-020-00860-7
Uttarotai, T., McKew, B.A., Benyahia, F., Murrell, J.C., Mhuantong, W., Wangkarn, S., Chitov, T., Bovonsombut, S., McGenity T.J (2021) Isoprene-degrading bacteria from soils associated with tropical economic crops and framework forest trees. Microorganisms 2021, 9(5), 1024. https://doi.org/10.3390/microorganisms9051024
Dawson, R.A., Crombie, A.T., Pichon, P.R.K., Steinke, M., McGenity, T.J. and Murrell, J.C. (2021) The microbiology of isoprene cycling in aquatic ecosystems. Aquatic Microbial Ecology, 87, 79-98. https://doi.org/10.3354/ame01972
Gibson, L., Crombie, A.T., McNamara, N.P. and Murrell, J.C. (2021). Isoprene-degrading bacteria associated with the phyllosphere of Salix fragilis, a high isoprene-emitting willow of the northern hemisphere. Environmental Microbiome 16 (1), 1-13.

Carrión, O., McGenity, T.J. and Murrell, J.C. (2020) Molecular ecology of isoprene degrading bacteria. Microorganisms, 8(7), 967. https://doi.org/10.3390/microorganisms8070967

Murrell, J.C., McGenity, T. J. and Crombie, A.T (2020) Microbial metabolism of isoprene: a much-neglected climate-active gas. Microbiology, mic.0.000931. https://doi.org/10.1099/mic.0.000931

Gibson, L., Larke-Mejia, N.L. and Murrell, J.C. (2020) Complete genome of isoprene degrading Nocardioides sp. WS12 Microorganisms 2020, 8, 889; https://doi.org/10.3390/microorganisms8060889

Larke-Mejía, N.L., Carrión, O., Crombie, A.T., McGenity, T.J. and Murrell, J.C. (2020) Sphingopyxis sp. strain OPL5, an isoprene-degrading bacterium from the Sphingomonadaceae family isolated from oil palm leaves. Microorganisms, 8, 1557; https://doi.org/10.3390/microorganisms8101557

Uttarotai, T., McKew, B.A., Benyahia, F., Murrell, J.C., Mhuantong, W., Wangkarn, S., Chitov, T., Bovonsombut, S., McGenity T.J (2021) Isoprene-degrading bacteria from soils associated with tropical economic crops and framework forest trees. Microorganisms 2021, 9(5), 1024. https://doi.org/10.3390/microorganisms9051024

Dawson, R.A., Crombie, A.T., Pichon, P.R.K., Steinke, M., McGenity, T.J. and Murrell, J.C. (2021) The microbiology of isoprene cycling in aquatic ecosystems. Aquatic Microbial Ecology (in press)

Dawson, R., Larke-Mejia, N., Crombie, A.T., Farhan Ul-Haque, M. and Murrell, J.C. Isoprene oxidation by the Gram negative model bacterium Variovorax sp. WS11. 2020. Microorganisms, 8(3), 349 https://doi.org/10.3390/microorganisms8030349

Larke-Mejia, N.L., Crombie, A.T., Pratscher, J., McGenity, T.J. and Murrell, J.C. Novel isoprene-degrading Proteobacteria from soil and leaves identified by cultivation and metagenomics analysis of stable isotope probing experiments. Frontiers in Microbiology, 2019; 10, 2700.

Crombie AT, Larke-Mejia NL, Emery H, Dawson R, Pratscher J, Murphy GP, McGenity TJ, and Murrell JC. Poplar phyllosphere harbors disparate isoprene-degrading bacteria. PNAS (USA) 2018; 115, 13081-13086.

McGenity TJ, Crombie AT, Murrell JC. Microbial cycling of isoprene, the most abundantly produced biological volatile organic compound on Earth. ISME J. 2018; 12:931-41.

Crombie AT, Khawand ME, Rhodius VA, Fengler KA, Miller MC, Whited GM et al. Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environ Microbiol. 2015; 17:3314-29.

Crombie AT, Emery H, McGenity TJ, Murrell JC. Draft genome sequences of three terrestrial isoprene-degrading Rhodococcus. Genome Announc. 2017; 5:e01256-17.

El Khawand M, Crombie AT, Johnston A, Vavlline DV, McAuliffe JC, Latone JA et al. Isolation of isoprene degrading bacteria from soils, development of isoA gene probes and identification of the active isoprene-degrading soil community using DNA-stable isotope probing. Environ Microbiol; 2016; 18:2743–53.

Johnston A, Crombie AT, Khawand ME, Sims L, Whited GM, McGenity TJ et al. Identification and characterisation of isoprene-degrading bacteria in an estuarine environment. Environ Microbiol. 2017; 19:3526–37.

Crombie AT, Mejía-Florez NL, McGenity TJ, Murrell JC. Genetics and ecology of isoprene degradation. In: Rojo F, editor. Aerobic utilization of hydrocarbons, oils and lipids. Springer International Publishing; 2018. p. 1-15.

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