A marine biogenic source of atmospheric ice-nucleating particles

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The amount of ice present in clouds can affect cloud lifetime, precipitation and radiative properties1,2. The formation of ice in clouds is facilitated by the presence of airborne ice-nucleating particles1,2. Sea spray is one of the major global sources of atmospheric particles, but it is unclear to what extent these particles are capable of nucleating ice3,4,5,6,7,8,9,10,11. Sea-spray aerosol contains large amounts of organic material that is ejected into the atmosphere during bubble bursting at the organically enriched sea–air interface or sea surface microlayer12,13,14,15,16,17,18,19. Here we show that organic material in the sea surface microlayer nucleates ice under conditions relevant for mixed-phase cloud and high-altitude ice cloud formation. The ice-nucleating material is probably biogenic and less than approximately 0.2 micrometres in size. We find that exudates separated from cells of the marine diatom Thalassiosira pseudonana nucleate ice, and propose that organic material associated with phytoplankton cell exudates is a likely candidate for the observed ice-nucleating ability of the microlayer samples. Global model simulations of marine organic aerosol, in combination with our measurements, suggest that marine organic material may be an important source of ice-nucleating particles in remote marine environments such as the Southern Ocean, North Pacific Ocean and North Atlantic Ocean.

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Figure 1: Sea-spray aerosol particles enriched in organic material are generated when bubbles burst at the air–sea interface.
Figure 2: Ice nucleation by material in the SML.
Figure 3: Spectroscopic analysis of Arctic SML samples and freezing experiments with diatom exudate.
Figure 4: Global distribution of atmospheric marine biogenic INPs.


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T.W.W., B.J.M. and T.F.W. acknowledge the assistance provided by the crew and other scientists onboard the R/V Knorr and the RRS James Clark Ross, the British Antarctic Survey, K. Baustian, J. McQuaid, A. Windross, J. Knulst, J. F. Wilson, A. M. Booth, R. Chance, L. J. Carpenter, S. Peppe, D. O’Sullivan, N. Umo, I. Cotton, H. Pearce, H. Price and M. J. Callaghan. The STXM/NEXAFS analysis was performed at the Advanced Light Source (ALS), Lawrence Berkeley National Laboratory supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under contract no. DE-AC02-05CH11231 (user award to D.A.K./J.Y.A. ALS-05955). STXM analyses were facilitated by A. L. D. Kilcoyne and M. K. Gilles. L.A.L. acknowledges assistance from R. Leaitch, E. Mungall, R. Christensen and J. Li, and the Pacific region Department of Fisheries and Oceans staff. The Marine Boundary Layer sampling site in Ucluelet is jointly supported and maintained by Environment Canada, the British Columbia Ministry of the Environment and Metro Vancouver. We acknowledge funding from the Natural Environment Research Council (NE/K004417/1, NE/I020059/1, NE/I013466/1, NE/I028696/1, NE/I019057/1, NE/H009485/1), the European Research Council (FP7, 240449 ICE, BACCHUS 603445), the UK Aerosol Society, National Science Foundation (AGS-1232203), German Research Foundation (WU585/6-1), the Climate Change and Atmospheric Research Program of the Natural Sciences and Engineering Research Council of Canada (for NETCARE), Fisheries and Oceans Canada, Environment Canada, NOAA’s Climate Program Office (for WACS II), and the DOE Office of Science (BER) Earth System Modeling Program.

Author information

T.W.W. organized the ICE-ACCACIA campaign, designed experiments, collected and analysed samples during and after the campaign, managed collaborations and co-wrote this manuscript. L.A.L. designed experiments and analysed samples during the NETCARE campaign and co-wrote this manuscript. P.A.A. collected and analysed STXM/NEXAFS spectra and diatom exudate freezing data and contributed to manuscript writing. M.N.B. collected flow cytometry data for SML samples during ACCACIA. I.M.B. sought funding for ACCACIA and helped design the microlayer sampling procedure. S.M.B., J.V.T., J.B. and K.S.C. performed and analysed the model simulations. C.J. performed heating tests on ICE-ACCACIA samples. W.P.K. assisted with collection of material during the WACS II cruise, provided exudate material for experiments, and participated in STXM/NEXAFS data collection. G.M., J.J.N. and S.R. conducted total organic carbon measurements on Arctic samples. L.A.M., O.W. and E.P. collected the Ucluelet, Line P and open ocean samples, and conducted the NETCARE biogeochemical analysis. C.L.S. helped organize the measurements at the Ucluelet site and facilitated the use of the sampling site. T.F.W. collected and analysed samples during and after the ICE-ACCACIA campaign and assisted with design of experiments. J.D.Y.-H., J.A.H., R.H.M., M.S. and J.P.S.W. collected the Ucluelet samples and helped with the NETCARE experiments. A.K.B. and J.P.D.A. oversaw and organized the NETCARE field campaign and provided financial support for it. D.A.K. and J.Y.A. initiated and designed the STXM/NEXAFS and diatom exudate freezing experiments, contributed to the writing of this manuscript and provided financial support for WACS II cruise participation, exudate freezing experiments, and STXM/NEXAFS analyses. B.J.M. established the collaborations necessary for this paper, helped to write the paper and oversaw the ICE-ACCACIA campaign and sought funding for it.

Correspondence to Theodore W. Wilson or Luis A. Ladino.

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Extended data figures and tables

Extended Data Figure 1 Sampling locations.

SML and SSW samples were collected during the ACCACIA campaign (July–August 2013) at Arctic sampling stations at the locations marked with solid red circles. Also shown are sampling locations during the WACS II campaign (May–June 2014) in the North Atlantic Ocean. NETCARE samples were collected at locations in the Northeast Pacific (yellow star and green square, CCGS John P. Tully, 14–19 June 2013). The red diamond and blue asterisk correspond to the sampling locations for the NETCARE British Columbia (BC) coastal samples (12–15 August 2013). The inset is a zoom of the BC coast sampling locations.

Extended Data Figure 2 Effects of heating and filtering on the ice nucleation activity of microlayer samples.

a, The effect of filtering through different pore-sized filters on the temperature at which 50% of droplets had frozen (T50) of Arctic and Atlantic SML samples tested using the μl-NIPI. Error bars represent ± the standard deviation calculated from the freezing temperatures in each experiment, which consisted of between 30 and 53 individual events. Shaded grey area is the range of T50 found for fresh unfiltered SSW during the campaign. b, Comparison of the UT-CFDC onset RHice of unfiltered, filtered (0.2 µm) and heated (to 100 °C for 10 min) North Pacific and BC coast SML and SSW samples. The blue lines, and the red and dark blue symbols are as shown in Fig. 2d. The green symbols represent the filtered onsets, whereas the black symbols represent the heated results. Ice-nucleation-onset error bars represent one standard deviation based on three to four replicates. c, Results of heating tests using Arctic and Atlantic SML samples on T50 tested using the μl-NIPI. Error bars represent ± the standard deviation calculated from the freezing temperatures in each experiment, which consisted of between 28 and 46 individual events. Shaded grey area is the range of T50 found for fresh untreated Arctic SSW.

Extended Data Figure 3 Ice surface site densities for the Pacific microlayer samples.

Comparison of the ice surface densities (ns) calculated from UT-CFDC data for the NETCARE SML samples with literature data. The ns values were obtained at −40 °C assuming that the particles were spherical. The SML ns values are indicated by the coloured symbols, whereas the mineral dust ns values are indicated by the grey symbols. The dark grey and light grey symbols are from refs 21 and 22, respectively.

Extended Data Figure 4 Bacterial cell counts for Arctic samples.

a, Bacterial cell counts from flow cytometry performed on Arctic SSW (black squares), fresh Arctic SML (red circles). b, The SML sample cell counts plotted against T50 (temperature at which 50% of droplets frozen) and line of best fit, R2 = 0.29.

Extended Data Figure 5 Correlation of TEP and DOC with the UT-CFDC RHice onsets.

a, b, Ice nucleation RHice onsets for Northeast Pacific (see Extended Data Table 1) samples plotted against measured DOC concentration (a) and TEP enrichment factor (b). Error bars represent the experimental uncertainty in relative humidity with respect to ice in the UT-CFDC.

Extended Data Figure 6 Ice-nucleating activity of diatoms cells and their exudates.

WACIFE frozen fraction curves derived from 60–129-μm-sized droplets (0.4 nl volume) as a function of temperature. Green symbols indicate diatom exudates in 0.1-μm-filtered sea water. Blue and red symbols represent 0.1-μm-filtered sea water devoid of exudates with and without the addition of growth media, respectively. All temperatures have been corrected for freezing point depression to pure water conditions from their initial aqueous solution water activity, aw = 0.985 (open circles), 0.97 (open squares), 0.96 (filled diamonds), 0.95 (open diamonds), 0.94 (filled circles), 0.925 (open triangle), 0.90 (asterisks). Shaded areas illustrate ranges of observed heterogeneous ice nucleation of intact and fragmented diatom cells (green) and homogeneous ice nucleation of aqueous NaCl droplets (grey) for similar aw values6,32. Error bars represent the instrumental uncertainty in temperature measurement. Predicted homogeneous freezing temperatures for similar sized water droplets are indicated by the grey bar31,40.

Extended Data Figure 7 TOC and DOC measurements for Arctic samples.

Arctic SML TOC and DOC measurements and Arctic SSW DOC measurements. TOC error bars represent the measured 2% coefficient of variance. DOC sample error was calculated as the coefficient of variation from the mean and standard deviation of three sample replicates. For comparison here we provide the Atlantic TOC measurements; Atlantic SML1 = 5.954 ± 0.185 mg l−1, Atlantic SML2 = 4.643 ± 0.135 mg l−1.

Extended Data Figure 8 μl-NIPI freezing curves for Arctic and Atlantic samples uncorrected for freezing depression caused by salts.

Fraction frozen curves for 1 µl droplet freezing experiments using Arctic and Atlantic ocean samples, uncorrected for freezing point depression. SML, SSW and boat flushing water (grey points; symbols correspond to those for SML sampled at the same locations) to check for the absence of contaminant INPs before sampling.

Extended Data Figure 9 Summary of ice nucleation experimental setups.

a, Pipetting 1 µl droplets onto a hydrophobic glass slide. b, Schematic of the µl-NIPI cold stage used for immersion mode droplet freezing experiments. c, Schematic of the experimental setup for cirrus cloud relevant experiments. CPC, condensation particle counter; DMA, differential mobility analyser; OPC, optical particle counter. d, Schematic of the water-activity-controlled immersion freezing experiment (WACIFE) for freezing of micrometre-sized droplets containing diatom exudates as a function of water activity, aw, and relative humidity, RH. Images are not to scale. The procedure for preparing and freezing droplets of filtered and autoclaved natural sea water with and without added f/2 nutrients droplets is similar except 0.1 μm filtration is not required.

Extended Data Table 1 Details of the sampled SMLs and SSWs

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Wilson, T., Ladino, L., Alpert, P. et al. A marine biogenic source of atmospheric ice-nucleating particles. Nature 525, 234–238 (2015) doi:10.1038/nature14986

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