Microbial cycling of isoprene, the most abundantly produced biological volatile organic compound on Earth

Abstract

Isoprene (2-methyl-1,3-butadiene), the most abundantly produced biogenic volatile organic compound (BVOC) on Earth, is highly reactive and can have diverse and often detrimental atmospheric effects, which impact on climate and health. Most isoprene is produced by terrestrial plants, but (micro)algal production is important in aquatic environments, and the relative bacterial contribution remains unknown. Soils are a sink for isoprene, and bacteria that can use isoprene as a carbon and energy source have been cultivated and also identified using cultivation-independent methods from soils, leaves and coastal/marine environments. Bacteria belonging to the Actinobacteria are most frequently isolated and identified, and Proteobacteria have also been shown to degrade isoprene. In the freshwater-sediment isolate, Rhodococcus strain AD45, initial oxidation of isoprene to 1,2-epoxy-isoprene is catalyzed by a multicomponent isoprene monooxygenase encoded by the genes isoABCDEF. The resultant epoxide is converted to a glutathione conjugate by a glutathione S-transferase encoded by isoI, and further degraded by enzymes encoded by isoGHJ. Genome sequence analysis of actinobacterial isolates belonging to the genera Rhodococcus, Mycobacterium and Gordonia has revealed that isoABCDEF and isoGHIJ are linked in an operon, either on a plasmid or the chromosome. In Rhodococcus strain AD45 both isoprene and epoxy-isoprene induce a high level of transcription of 22 contiguous genes, including isoABCDEF and isoGHIJ. Sequence analysis of the isoA gene, encoding the large subunit of the oxygenase component of isoprene monooxygenase, from isolates has facilitated the development of PCR primers that are proving valuable in investigating the ecology of uncultivated isoprene-degrading bacteria.

Actinobacterial Degradation of 2-Hydroxyisobutyric Acid Proceeds via Acetone and Formyl-CoA by Employing a Thiamine-Dependent Lyase Reaction

“…In the latter, the MPD dehydrogenase MpdB is replaced by an only distantly related alcohol dehydrogenase of the glucose-methanol-choline oxidoreductase family ( Figure 1B). Nevertheless, this may be indicative of a second bacterial isoprene oxidation pathway, besides the well-established route via a glutathione adduct (van Hylckama Vlieg et al, 1999;McGenity et al, 2018). In the proposed lyase-dependent route, isoprene would be oxidized as shown for isobutene in Figure 1A via the corresponding 1,2-epoxide and 1,2-diol.…”

2038 – When microbes rule the Earth

“…Terpenes and oxygenated volatile organic compounds are just two classes of volatiles that have been largely neglected by microbiologists. Isoprene, for example, which is liberated to the atmosphere (primarily by plants, but also by phototrophic and heterotrophic microbes) to a similar extent as methane, serves as a carbon and energy source for bacteria, and can be consumed at environmentally relevant concentrations (McGenity et al, 2018). We are beginning to understand the ecology, cryptic cycles, functional genomics and physiology of the microbes involved in transforming this very abundant volatile compound, as well as its role as a signalling molecule (see Fall and Copley, 2000;McGenity et al, 2018).…”

“…Isoprene, for example, which is liberated to the atmosphere (primarily by plants, but also by phototrophic and heterotrophic microbes) to a similar extent as methane, serves as a carbon and energy source for bacteria, and can be consumed at environmentally relevant concentrations (McGenity et al, 2018). We are beginning to understand the ecology, cryptic cycles, functional genomics and physiology of the microbes involved in transforming this very abundant volatile compound, as well as its role as a signalling molecule (see Fall and Copley, 2000;McGenity et al, 2018). One important detrimental effect of isoprene is its reaction with nitrogen oxides (NOx) to create ground-level ozone, with ensuing damage to crop and animal health (Ashworth et al, 2013), which is likely to be exacerbated by increased planting of isoprene-producing crops such as poplar, willow and oil palm, especially near urban areas where NOx concentrations are high (Ashworth et al, 2013).…”

Sphingopyxis sp. Strain OPL5, an Isoprene-Degrading Bacterium from the Sphingomonadaceae Family Isolated from Oil Palm Leaves

“…It has been known for a number of years that soils can be a sink for isoprene [ 14 , 15 ] and this has stimulated research on the microbiology of isoprene metabolism. The biological consumption of isoprene by bacteria and their role in the isoprene cycle has been reviewed in detail recently ([ 16 , 17 , 18 ]). In brief, a number of Gram-positive bacteria, mainly Actinobacteria of the genera Rhodococcus [ 19 , 20 ], Gordonia , Mycobacterium [ 21 ], and Nocardioides [ 22 ] have been isolated and characterized.…”

“…All isoprene degraders characterized to date contain a multi-subunit isoprene monooxygenase, encoded by the genes isoABCDEF , which catalyzes the oxidation of isoprene to epoxyisoprene, and the gene cluster isoGHIJ encoding a glutathione transferase and enzymes catalyzing further steps in the isoprene oxidation pathway [ 23 ]. The isoprene monooxygenase (IsoMO) can be distinguished from related soluble di-iron monooxygenases (SDIMOs, [ 28 ]) that are involved in metabolism of alkenes, as well as alkanes and aromatic compounds (reviewed in [ 18 ]). In Variovorax strain WS11 and Rhodococcus strain AD45, iso genes are carried on megaplasmids [ 24 , 26 ].…”