Crombie AT, Khawand ME, Rhodius VA, Fengler KA, Miller MC, Whited GM, McGenity TJ, Murrell JC (2015) Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environmental Microbiology doi:10.1111/1462-2920.12793
Crombie et al. (2015) Abstract:
Emissions of biogenic volatile organic compounds (VOCs) form an important part of the global carbon cycle, comprising a significant proportion of net ecosystem productivity. They impact atmospheric chemistry and contribute directly and indirectly to greenhouse gases. Isoprene, emitted largely from plants, comprises one third of total VOCs, yet in contrast to methane, which is released in similar quantities, we know little of its biodegradation. Here, we report the genome of an isoprene degrading isolate, Rhodococcus sp. AD45, and, using mutagenesis shows that a plasmid-encoded soluble di-iron centre isoprene monooxygenase (IsoMO) is essential for isoprene metabolism. Using RNA sequencing (RNAseq) to analyse cells exposed to isoprene or epoxyisoprene in a substrate-switch time-course experiment, we show that transcripts from 22 contiguous genes, including those encoding IsoMO, were highly upregulated, becoming among the most abundant in the cell and comprising over 25% of the entire transcriptome. Analysis of gene transcription in the wild type and an IsoMO-disrupted mutant strain showed that epoxyisoprene, or a subsequent product of isoprene metabolism, rather than isoprene itself, was the inducing molecule. We provide a foundation of molecular data for future research on the environmental biological consumption of this important, climate-active compound.
Exton DA, McGenity TJ, Steinke M, Smith DJ, Suggett DJ (2014) Uncovering the volatile nature of tropical coastal marine ecosystems in a changing world. Global Change Biology 21: 1383-1394. doi: 10.1111/gcb.12764
Exton et al. (2014) Abstract:
Biogenic volatile organic compounds (BVOCs), in particular dimethyl sulphide (DMS) and isoprene, have fundamental ecological, physiological and climatic roles. Our current understanding of these roles is almost exclusively established from terrestrial or oceanic environments but signifies a potentially major, but largely unknown, role for BVOCs in tropical coastal marine ecosystems. The tropical coast is a transition zone between the land and ocean, characterized by highly productive and biodiverse coral reefs, seagrass beds and mangroves, which house primary producers that are amongst the greatest emitters of BVOCs on the planet. Here, we synthesize our existing understanding of BVOC emissions to produce a novel conceptual framework of the tropical marine coast as a continuum from DMS-dominated reef producers to isoprene-dominated mangroves. We use existing and previously unpublished data to consider how current environmental conditions shape BVOC production across the tropical coastal continuum, and in turn how BVOCs can regulate environmental stress tolerance or species interactions via infochemical networks. We use this as a framework to discuss how existing predictions of future tropical coastal BVOC emissions, and the roles they play, are effectively restricted to present day ‘baseline’ trends of BVOC production across species and environmental conditions; as such, there remains a critical need to focus research efforts on BVOC responses to rapidly accelerating anthropogenic impacts at local and regional scales. We highlight the complete lack of current knowledge required to understand the future ecological functioning of these important systems, and to predict whether feedback mechanisms are likely to regulate or exacerbate current climate change scenarios through environmentally and ecologically mediated changes to BVOC budgets at the ecosystem level.
Exton DA, Suggett DJ, McGenity TJ, Steinke M (2013) Chlorophyll-normalized isoprene production in laboratory cultures of marine microalgae and implications for global models. Limnology and Oceanography 58: 1301-1311. doi: 10.4319/lo.2013.58.4.1301
Exton et al. (2013) Abstract:
We used laboratory cultures of marine microalgae to investigate the effects of growth conditions and their taxonomic position on the production of isoprene, a gas that has major effects on atmospheric chemistry and provides stress tolerance to many primary producers. Isoprene was quantified from 21 microalgal strains sampled during exponential growth, using purge-and-trap pre-concentration and gas chromatography with flame-ionization detection. Isoprene production rates varied by two orders of magnitude between strains (0.03–1.34 µmol [g chlorophyll a]−1 h−1), and were positively correlated with temperature (r2 = 0.52, p < 0.001, n = 59). Three distinct sea surface temperature (SST)-dependent relationships were found between isoprene and chlorophyll a (µmol [g chlorophyll a]−1 h−1), an improvement in resolution over the single relationship used in previous models: for three polar strains grown at −1°C (slope = 0.03, R2 = 0.76, p < 0.05, n = 9), nine strains grown at 16°C (slope = 0.24, R2 = 0.43, p < 0.05, n = 27 with Dunaliella tertiolecta excluded), and eight strains grown at 26°C (slope = 0.39, R2 = 0.15, p < 0.05, n = 24). We then used a simple model that applied the SST-dependent nature of isoprene production to three representative bioregions for the growth temperatures used in this study. This approach yielded an estimate of global marine isoprene production that was 51% higher than previous attempts using an SST-independent single relationship. Taking into account the effect of temperature therefore potentially allows more precise modeling of marine isoprene production, and suggests that increasing the SST-based resolution of data beyond the three groups used here could further improve future modeling simulations.
Exton DA, Suggett DJ, Steinke M, McGenity TJ (2012) Spatial and temporal variability of biogenic isoprene emissions from a temperate estuary. Global Biogeochemical Cycles 26: GB2012; doi:10.1029/2011GB004210.
Exton et al. (2012) Abstract:
Isoprene is important for its atmospheric impacts and the ecophysiological benefits it affords to emitting organisms; however, isoprene emissions from marine systems remain vastly understudied compared to terrestrial systems. This study investigates for the first time drivers of isoprene production in a temperate estuary, and the role this production may play in enabling organisms to tolerate the inherently wide range of environmental conditions. Intertidal sediment cores as well as high and low tide water samples were collected from four sites along the Colne Estuary, UK, every six weeks over a year. Isoprene concentrations in the water were significantly higher at low than high tide, and decreased toward the mouth of the estuary; sediment production showed no spatial variability. Diel isoprene concentration increased with light availability and decreased with tidal height; nighttime production was 79% lower than daytime production. Seasonal isoprene production and water concentrations were highest for the warmest months, with production strongly correlated with light (r2 = 0.800) and temperature (r2 = 0.752). Intertidal microphytobenthic communities were found to be the primary source of isoprene, with tidal action acting as a concentrating factor for isoprene entering the water column. Using these data we estimated an annual production rate for this estuary of 681 μmol m−2 y−1. This value falls at the upper end of other marine estimates and highlights the potentially significant role of estuaries as isoprene sources. The control of estuarine isoprene production by environmental processes identified here further suggests that such emissions may be altered by future environmental change.
Exton DA, Smith DJ, McGenity TJ, Hills AJ, Steinke M, Suggett DJ (2010) Application of a Fast Isoprene Sensor (FIS) for measuring isoprene production from marine samples. Limnology and Oceanography: Methods 8: 185-195. doi: 10.4319/lom.2010.8.0185
Exton et al. (2010) Abstract:
Research into isoprene production from marine sources traditionally relies on gas chromatography techniques which are labor intensive, provide a slow sample turnover, and require significant method training. An alternative method is the use of a Fast Isoprene Sensor (FIS), a chemiluminescence-based approach that provides real time isoprene analysis, but is relatively simple to run and also portable. Until now, the FIS has been used in terrestrial but not aquatic isoprene studies. Due to the added difficulties with marine compared with terrestrial sampling, particularly potential interference from dimethyl sulfide (DMS), we have developed a new protocol that allows accurate and reliable data to be obtained from FIS analysis. The detection limit of our modified system to standard gas was 0.02 nM (0.5 ppbv), while minimum isoprene production detected by the FIS was 0.59 nmol h−1 (for Thalassiosira weissflogii). We also compared our FIS-based approach with GC analysis of isoprene emission from marine samples of micro- and macro-algae, and demonstrated a strong similarity (r2 = 0.910, slope = 1.003). The ability to use FIS analysis with marine samples will significantly broaden the scope of isoprene research in marine environments, permitting remote field work, and allow previously unanswered questions to be addressed.
Alvarez LA, Exton DA, Suggett DJ, Timmis KN, McGenity TJ (2009) Characterization of marine isoprene-degrading communities. Environmental Microbiology 11: 3280–3291. doi: 10.1111/j.1462-2920.2009.02069.
Alvarez et al. (2009) Abstract:
Isoprene is a volatile and climate-altering hydrocarbon with an atmospheric concentration similar to that of methane. It is well established that marine algae produce isoprene; however, until now there was no specific information about marine isoprene sinks. Here we demonstrate isoprene consumption in samples from temperate and tropical marine and coastal environments, and furthermore show that the most rapid degradation of isoprene coincides with the highest rates of isoprene production in estuarine sediments. Isoprene-degrading enrichment cultures, analysed by denaturing gradient gel electrophoresis and 454 pyrosequencing of the 16S rRNA gene and by culturing, were generally dominated by Actinobacteria, but included other groups such as Alphaproteobacteria and Bacteroidetes, previously not known to degrade isoprene. In contrast to specialist methane-oxidizing bacteria, cultivated isoprene degraders were nutritionally versatile, and nearly all of them were able to use n-alkanes as a source of carbon and energy. We therefore tested and showed that the ubiquitous marine hydrocarbon-degrader, Alcanivorax borkumensis, could also degrade isoprene. A mixture of the isolates consumed isoprene emitted from algal cultures, confirming that isoprene can be metabolized at low, environmentally relevant concentrations, and suggesting that, in the absence of spilled petroleum hydrocarbons, algal production of isoprene could maintain viable populations of hydrocarbon-degrading microbes. This discovery of a missing marine sink for isoprene is the first step in obtaining more robust predictions of its flux, and suggests that algal-derived isoprene provides an additional source of carbon for diverse microbes in the oceans.