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Evidence for biological and chemical isoprene consumption in coastal seawaterThe time course of isoprene concentration in coastal seawater samples incubated in closed glass bottles at the in situ temperature and in the dark demonstrated sustained loss for at least 45 h (Fig. 1a). Enclosure without headspace prevented isoprene loss by ventilation, and darkness was assumed to arrest all or most of the biological production25 and any photochemical production15 or degradation. Thus, the measured loss was considered the result of microbial degradation and chemical oxidation. In most cases an exponential function fitted better the decay than a linear function (Supplementary Table 1), indicating first-order (concentration-dependent) kinetics for isoprene loss.Fig. 1: Isoprene loss in dark incubations of coastal seawater.a Time course of isoprene concentration in 2 L dark incubations of non-filtered seawater samples from the back-reef lagoon of Mo’orea in April (blue) and the coastal Mediterranean in March (red) and May (green). Filled and open symbols correspond to duplicate incubations. Exponential fits to the data are shown by lines. See Supplementary Table 1 for fit equations and metrics, water temperatures and chlorophyll a concentrations. b Time course of isoprene concentration in series of 30 mL dark incubations of coastal Mediterranean seawater. Dark blue: non-filtered; red: filtered through 0.2 µm; green: filtered + 10 µmol L−1 H2O2; purple: filtered + 0.0025 units mL−1 bromoperoxidase (BrPO); light blue: filtered + H2O2 + BrPO. Exponential fit results in Supplementary Table 2.Full size imageIncubation of microorganism-devoid (filtered through 0.2 µm) coastal seawater sampled next to seaweeds showed an isoprene loss (0.12 d−1) that was half the loss in non-filtered water (0.20 d−1; Fig. 1b and Supplementary Table 2), implying that chemical oxidation accounted for half the total loss. Oxidation by OH·, the fastest amongst isoprene reactions with oxidative transients for which reaction rate data exist19, could account for the observed chemical loss. However, the possibility of oxidation by hitherto overlooked, pervasive oxidants like H2O2 deserved consideration. The addition of unrealistically high concentrations of either H2O2 or the enzyme bromoperoxidase (BrPO), substantially speeded up the chemical loss (0.91 d−1 with 10 µmol H2O2 L−1, 0.31 d−1 with 0.0025 units BrPO mL−1; Fig. 1b and Supplementary Table 2). Isoprene could have reacted with H2O2 in seawater as it does in acidic aerosols26. Besides, should dissolved27 BrPOs from seaweeds or outer-membrane-bound28 BrPOs from phytoplankton occur, they would have reacted with added H2O2 to produce hypobromous acid (HOBr), a strong oxidant29 that would further remove isoprene. Indeed, the addition of BrPO consumed isoprene because it produced HOBr by reaction with the naturally occurring H2O2. Confirming this interpretation, large HOBr production by simultaneous addition of BrPO and H2O2 caused complete isoprene removal in less than 4 h (Fig. 1b). Therefore, the results shown in Fig. 1b indicate that isoprene is reactive to pervasive H2O2 either directly or through the formation of enzymatically derived HOBr. All in all, first-order total isoprene loss (Fig. 1a) is expected to depend on photochemically-produced oxidants30 like H2O2, OH· and 1O2 as well as on microbiota through (a) microbial uptake and catabolism11 and (b) reaction with biologically produced oxidants26,31,32 like HOBr, H2O2 or superoxide.Variability of isoprene loss rate constants in the open oceanTen of the eleven offshore experimental sites were located in the open ocean, and one was located on the Southwestern Atlantic Shelf. Altogether they covered wide ranges of latitude (40°N–61°S), sea surface temperature (−0.8–28.6 °C), daily-averaged wind speed (3–12 m s−1), fluorometric chlorophyll-a (chla) concentration (0.1–5.8 mg m−3), and isoprene concentration (4–104 nmol m−3) (Fig. 2, Table 1 and Supplementary Table 3). Unfiltered seawater samples from the surface ocean were incubated in glass bottles for 24 h, at the in situ temperature and in the dark, and first-order loss rate constants were determined from initial and final isoprene concentrations (see Methods). Note that loss was determined under the assumption that isoprene production was arrested in the dark25. There is published evidence that residual isoprene production may occur in the dark33, but in our incubations, it was insufficient to counteract loss. Thus, isoprene losses caused by processes other than ventilation may have been underestimated.Fig. 2: Geographical distribution of the offshore experiments.Location of the sampling and incubation sites are shown by circles, coloured for isoprene concentration.Full size imageTable 1 Measured biological variables and isoprene process rate constants.Full size tableLoss rate constants (kloss = kbio + kchem) varied over an order of magnitude, ranging 0.03–0.64 d−1 with a median of 0.08 d−1 (Table 1). They did not show any significant relationship to sea surface temperature (SST) (Supplementary Fig. 1) but showed proportionality to the chla concentration (Fig. 3a) that was best described by the following linear regression equation:$${k}_{{{{{{rm{loss}}}}}}}=0.10; (pm 0.01),{{{{{rm{x}}}}}}, [{{{{{rm{chl}}}}}}a]+0.05; (pm 0.01)$$
(1)
Fig. 3: Isoprene processes and their main drivers.a Rate constant of isoprene loss in dark incubations (kloss, considered to be microbial and chemical consumption) vs. chlorophyll-a concentration. The linear regression equation is kloss = 0.10 × [chla] + 0.05 (R2 = 0.96, p = 10−7, n = 11). The standard error of the slope is 0.01 L mg−1 d−1, and the standard error of the intercept is 0.01 d−1. Error bars represent the experimentally determined standard error of kloss. The colour scale of the circles indicates bacterial abundances. b Specific (chla-normalised) rate of isoprene production vs seawater temperature (SST) across the sample series. The dashed line is the general smoothed trend. The blue line is the exponential adjustment at SST , 1000)$$
(2)
Substitution in Eq. (1) results in:$${k}_{{{{{{rm{loss}}}}}}}=0.14,{{{{{rm{x}}}}}}, {[{{{{{rm{chl}}}}}}{a}_{{{{{{rm{sat}}}}}}}]}^{1.28}+0.05$$
(3)
which is our recommended equation for kloss prediction from satellite chla. Note that only the variable term (kbio) changes from Eq. (1), while the intercept (kchem) is maintained at 0.05 d−1.Comparison of isoprene sinks and total turnover timeThe change of isoprene concentration ([iso]) in the surface mixed layer over time can be described as the budget of sources and sinks:$$varDelta [{{{{{rm{iso}}}}}}]/varDelta {{{{{rm{t}}}}}}=[{{{{{rm{iso}}}}}}]cdot ({k}_{{{{{{rm{prod}}}}}}} – {k}_{{{{{{rm{loss}}}}}}} – {k}_{{{{{{rm{vent}}}}}}} – {k}_{{{{{{rm{mix}}}}}}})$$
(4)
where kprod, kvent and kmix are the rate constants of isoprene production, ventilation to the atmosphere and vertical downward mixing by turbulent diffusion, respectively.We calculated kvent from our sampling sites over a period of 24 h (Table 1). Ventilation has been considered the main isoprene sink from the upper mixed layer of the ocean18. In our sampling sites, kloss was 0.4 to 10 times the kvent (median factor: 1.2). That is, loss through microbial + chemical consumption was of the same order as ventilation, sometimes considerably faster. Vertical mixing, kmix, was estimated to be one order of magnitude lower than the other process rates (Table 1), and in all cases but one it was calculated or assumed not to be a loss term but an import term into the mixed layer, because vertical profiles generally show maximum isoprene concentrations below the mixed layer and turbulent diffusion causes upward transport14,17. Altogether, the microbial, chemical, ventilation, and, where relevant, mixing losses resulted in total turnover times (1/(kloss + kvent + kmix)) of isoprene between 1.4 and 16 days, median 5 days (Table 1).Isoprene productionAssuming steady-state for isoprene concentrations over 24 h (Supplementary Fig. 2), i.e. Δ[iso]/Δt = 0 in Eq. (4), the sum of the daily rate constants of all sinks (kloss + kvent) equals the rate constant of isoprene production (kprod), with kmix adding to either side depending on whether it is an import to or an export from the mixed layer (Table 1). Note that kprod was the highest coinciding with higher [chla]. This is consistent with a recent study44 where measurement of the net biological isoprene production (i.e. production — consumption rates) across seasons in the open ocean was attempted; net production rates increased in May, coinciding with a large increase in [chla] and phytoplankton cell abundance.The product of kprod by the isoprene concentration gives the daily isoprene production rate, which can be normalised by dividing it by the chla concentration. In our study, this specific isoprene production rate varied between 1 and 38 nmol (mg chla)−1 d−1 (Table 1), median 8 nmol (mg chla)−1 d−1. These values are within the broad range reported across phytoplankton taxa from laboratory studies with monocultures41,45 (0.3–32, median 3 nmol (mg chla)−1 d−1, n = 124). Five of the eleven sites gave values >13 nmol (mg chla)−1 d−1, i.e. in the higher end of the laboratory data range. This is not unexpected, since measurements in monoculture experiments are typically conducted before reaching nutrient limitation, below light saturation and in the absence of UV radiation, to mention three stressors commonly occurring in the surface open ocean. If isoprene biosynthesis and release is enhanced by any of these stressors, as is the case in vascular plants7,10, then monoculture-derived results will easily render underestimates of isoprene production in the open ocean. Production by heterotrophic bacteria46 could have also contributed to increase apparent specific isoprene production rates, but the occurrence and importance of this process in the marine environment is unknown.When plotted against the SST, which was also the temperature of the incubations, specific isoprene production rates increased exponentially between −0.8 and 23 °C and dropped drastically at higher SST (Fig. 3b). Several studies with phytoplankton monocultures have reported positive dependence of specific isoprene production rates on temperature45,47,48,49,50. One of these studies45 described that the increase with temperature reaches an optimum for production that varies among phytoplankton strains and with light intensity, but falls around 23–26 °C. The most detailed study47 was conducted with a Prochlorococcus strain; remarkably, the shape of the specific production rate vs. temperature curve for this cyanobacterium strain was almost identical to that of Fig. 3b, with an exponential increase until 23 °C and a drop thereafter. This is the canonical curve type of enzymatic activities, but the thermal behaviour of the enzymes for isoprene synthesis in marine unicellular algae has not yet been characterised12.Revising the magnitude and players of the marine isoprene cycleOur results allow redrawing the isoprene cycle in the surface mixed layer of the ocean. Figure 4 sketches the magnitude of the rate constants for production and sinks presented in Table 1, averaged according to a chla concentration threshold: the blue and green arrows correspond to the experiments in waters with [chla] lower and higher than 0.4 mg m−3, respectively. Isoprene production in productive (chla-richer) waters is faster than in oligotrophic (chla-poorer) waters. Vertical mixing is assumed to majorly constitute an input into the mixed layer, yet very small. Photochemical production and emission from surfactants15 in the surface microlayer of productive waters is depicted as uncertain. Among sinks, the microbiota-dependent consumption is much faster in productive waters; actually, the statistical uncertainty of Eq. (1) and the uneven distribution of incubation results along the [chla] axis hamper resolving kbio in phytoplankton-poor waters ( More

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