Diversity of isoprene-degrading bacteria in phyllosphere and soil communities from a high isoprene-emitting environment: a Malaysian oil palm plantation

Abstract

Background: Isoprene is the most abundantly produced biogenic volatile organic compound (BVOC) on Earth, with annual global emissions almost equal to those of methane. Despite its importance in atmospheric chemistry and climate, little is known about the biological degradation of isoprene in the environment. The largest source of isoprene is terrestrial plants, and oil palms, the cultivation of which is expanding rapidly, are among the highest isoprene-producing trees. Results: DNA stable isotope probing (DNA-SIP) to study the microbial isoprene-degrading community associated with oil palm trees revealed novel genera of isoprene-utilising bacteria including Novosphingobium, Pelomonas, Rhodoblastus, Sphingomonas and Zoogloea in both oil palm soils and on leaves. Amplicon sequencing of isoA genes, which encode the α-subunit of the isoprene monooxygenase (IsoMO), a key enzyme in isoprene metabolism, confirmed that oil palm trees harbour a novel diversity of isoA sequences. In addition, metagenomeassembled genomes (MAGs) were reconstructed from oil palm soil and leaf metagenomes and putative isoprene degradation genes were identified. Analysis of unenriched metagenomes showed that isoA-containing bacteria are more abundant in soils than in the oil palm phyllosphere. Conclusion: This study greatly expands the known diversity of bacteria that can metabolise isoprene and contributes to a better understanding of the biological degradation of this important but neglected climate-active gas.

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

“…Gordonia -like isoA sequences were found in poplar leaf samples, in oil palm leaves from this study (40% of sequences affiliated with Gordonia ) and Malaysian oil palm leaves (over 98%) [ 29 ]. In a similar DNA-SIP experiment, enriching leaves and soil from a Malaysian oil palm tree, Carrión et al showed the presence of Gordonia and members of the Sphingomonadaceae family enriched in the soil and phyllosphere communities [ 30 ].…”

“…New understanding of the physiology, biochemistry, and molecular biology of isoprene metabolism has provided the tools for designing functional gene primers and probes based on isoA, encoding a key component of the IsoMO [ 19 , 29 ]. Surveys with samples from the terrestrial environment, mainly soils and the phyllosphere have revealed the presence of isoprene-degrading bacteria, especially in environments containing trees that produce high concentrations of isoprene [ 19 , 25 , 27 , 29 , 30 ]. DNA-stable isotope probing (DNA-SIP) experiments have also revealed the diversity of active isoprene degraders present in these environments, which are often Actinobacteria, especially Rhodococcus species, but also include other Gram-negative isoprene degraders [ 19 , 25 , 27 ].…”

Molecular Ecology of Isoprene-Degrading Bacteria

“…They also demonstrated that isoprene-degrading bacteria isolated from these environments consumed isoprene naturally produced by microalgal cultures. More recently, experiments conducted with phyllosphere samples from high isoprene-emitting trees from temperate and tropical regions (poplar, willow, and oil palm trees) have shown that this environment is likely to be an important source of isoprene-degrading microorganisms [42][43][44][45]. However, despite these findings, the significance of the biological consumption of isoprene is still a key aspect of the global isoprene cycle that needs to be addressed.…”

“…Isoprene enrichments with garden and tyre dump soils, as well as soils in the vicinity of willow trees, have also led to the isolation of several Rhodococcus species and novel Nocardioides, Ramlibacter, and Variovorax strains, which degrade isoprene [51][52][53][54][55][56]. Recent studies exploring the phyllosphere of poplar, willow, and oil palm trees have shown that this environment harbours a considerable variety of isoprene-degrading isolates, including members of the genera Rhodococcus, Gordonia, Sphingopyxis, and Variovorax [42,51,52,55]. Moreover, Acuña Alvarez et al [41] reported the isolation, from marine and estuarine environments, of several Actinobacteria (Leifsonia, Gordonia, Mycobacterium, Rhodococcus) and Alphaproteobacteria (Stappia, Loktanella, Shinella) that could grow on isoprene, with Gordonia and Mycobacterium being the most well characterised [57].…”

“…Several DNA-SIP experiments with 13 C-labelled isoprene have been conducted with samples from terrestrial, phyllosphere, and marine environments [42,43,45,51,56,57]. El Khawand et al [51] and Larke-Mejía et al [56] investigated the composition of the active isoprene-degrading community from soil beneath willow trees using DNA-SIP with high and low concentrations of isoprene (Table 1).…”