Article pubs.acs.org/est
Transition Metal Associations with Primary Biological Particles in Sea Spray Aerosol Generated in a Wave Channel Timothy L. Guasco,†,∥ Luis A. Cuadra-Rodriguez,† Byron E. Pedler,‡ Andrew P. Ault,§,⊥ Douglas B. Collins,† Defeng Zhao,†,# Michelle J. Kim,‡ Matthew J. Ruppel,† Scott C. Wilson,† Robert S. Pomeroy,† Vicki H. Grassian,§ Farooq Azam,‡ Timothy H. Bertram,† and Kimberly A. Prather†,‡,* †
Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California, 92093 Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California, 92093 § Department of Chemistry, University of Iowa, Iowa City, Iowa, 52242 ‡
S Supporting Information *
ABSTRACT: In the ocean, breaking waves generate air bubbles which burst at the surface and eject sea spray aerosol (SSA), consisting of sea salt, biogenic organic species, and primary biological aerosol particles (PBAP). Our overall understanding of atmospheric biological particles of marine origin remains poor. Here, we perform a control experiment, using an aerosol time-of-flight mass spectrometer to measure the mass spectral signatures of individual particles generated by bubbling a salt solution before and after addition of heterotrophic marine bacteria. Upon addition of bacteria, an immediate increase occurs in the fraction of individual particle mass spectra containing magnesium, organic nitrogen, and phosphate marker ions. These biological signatures are consistent with 21% of the supermicrometer SSA particles generated in a previous study using breaking waves in an oceanatmosphere wave channel. Interestingly, the wave flume mass spectral signatures also contain metal ions including silver, iron, and chromium. The nascent SSA bioparticles produced in the wave channel are hypothesized to be as follows: (1) whole or fragmented bacterial cells which bioaccumulated metals and/or (2) bacteria-derived colloids or biofilms which adhered to the metals. This study highlights the potential for transition metals, in combination with specific biomarkers, to serve as unique indicators for the presence of marine PBAP, especially in metal-impacted coastal regions. serving as IN and CCN.15−19 In particular, bacteria, a common PBAP, have been shown to be the most efficient IN, initiating ice formation at temperatures as warm as −2 °C.14,20 In addition to climate effects, PBAP are believed to impact the cytotoxicity of airborne particulate matter.14,21 While the health and climate impacts of PBAP have recently led to increased attention, there remain many questions and different opinions regarding the extent of control that PBAP exert on atmospheric processes, in part due to conflicting reports on the atmospheric flux and concentrations of PBAP.18,22−32 Although numerous field studies have highlighted the possibility that PBAP can serve as an important source of IN on regional scales during different seasons,16,17,33,34 local and global simulations have reported wide-ranging results with regard to the role of PBAP in atmospheric ice formation.30,35−38 In order to develop a
1. INTRODUCTION Atmospheric aerosol particles impact human health, air quality, and the Earth’s climate in important, yet poorly understood, ways.1,2 The parameters that play a role in determining the effects of aerosols are chemical composition,3−8 particle size,8−11 and morphology. With regard to climate, aerosols impact the radiative balance by scattering and absorbing radiation as well as by acting as cloud condensation (CCN) and ice nuclei (IN) in processes referred to as the direct and indirect effects, respectively.11,12 Due to the wide array of aerosol sources and the multitude of transformations particles can undergo in the atmosphere, there are numerous particle types which are composed of heterogeneous mixtures of many chemical components.13 Primary biological aerosol particles (PBAP) are a particularly interesting class of particles of which there is an extreme paucity of knowledge.14 PBAP refers to solid airborne particles derived from biological organisms (e.g., microorganisms, fragments of biological materials, and cellular exudates) that can profoundly influence climate and the hydrological cycle by © 2013 American Chemical Society
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2. EXPERIMENTAL SECTION 2.1. Single-Particle Analysis with ATOFMS and TEMEDX. The chemical composition of individual sea spray particles was obtained with both on- and off-line instrumentation. Dual-polarity mass spectra of particles in the 0.5−3.0 μm size range were recorded in real-time using an ATOFMS.68 Particle phase water has been shown to inhibit the detection of negative ion spectra,69 therefore, the sampling inlet of the ATOFMS was preceded by a silica gel diffusion dryer. The operating principles of the ATOFMS have been described previously,68 so only a brief discussion will be provided here. A vacuum continuously draws particles from atmospheric pressure into a differentially pumped vacuum chamber, accelerating particles to their terminal velocity, which inherently depends on particle size. The particles then pass through the output of two continuous wave visible lasers, which are separated by a known, fixed distance. The time required for each particle to traverse through the two laser beams, measured by monitoring light scattering signals, is used to determine the size-dependent velocity of individual particles. The calculated particle velocity is used to trigger a frequency quadrupled (266 nm) Q-switched Nd:YAG laser which is aligned through the ion source region of the time-of-flight mass spectrometer perpendicular to the aerosol path. This ultraviolet laser pulse desorbs and ionizes the chemical constituents from individual particles, providing both positive and negative ions for simultaneous analysis by a dual-polarity time-of-flight mass spectrometer. For the wave channel experiments, samples were collected with a micro-orifice uniform deposit impactor (MOUDI; MSP Corp. Model 100) for offline analysis by transmission electron microscopy with energy dispersive X-ray spectroscopy (TEMEDX). Samples were collected on each stage of the MOUDI with Carbon Type B 400 mesh TEM grids (Ted Pella Inc., Part number 01814-F). TEM analysis was conducted on a JEOL 2100f field emission TEM with an accelerating voltage of 200 keV and a Gatan high angle annular dark field (HAADF) detector. EDX analysis was performed using a Thermo Noran Nano EDX detector (Nanotrace, Thermo Inc.) and analyzed using the NSS software package. 2.2. Bubbling Apparatus Experiments. A control salt solution consisting of NaCl and MgCl2 was prepared to simulate oceanic salinity (∼32 ‰) and the ratio of Na+/Mg2+ (∼8.4:1, by mass) by dissolving 56.9 g NaCl (Sigma-Aldrich, 99.999%) and 10.2 g MgCl2 (Sigma-Aldrich, > 98% purity) in 2 L of ultrapure Milli-Q (18.2 MΩ) water. While seawater consists of a more complex ionic mixture than Na+, Mg2+, and Cl−, this NaCl/MgCl2 solution, containing the two most abundant salts, was chosen based upon a recent shipboard field study in the Indian Ocean which showed that the fraction of marine particles in which 24Mg+ was the dominant positive ion and was positively correlated with oceanic biological productivity.70 Additionally, a recent study showed that under certain seawater conditions, heterotrophic bacteria contain 5−7 times more Mg2+ than Na+.71 Before dissolution, the salts were combusted at 450 °C for 6 h to remove organic impurities. A culture of heterotrophic bacteria (Alteromonas sp. AltSIO)72 was grown in ZoBell 2216E media (5 g peptone and 1 g yeast extract per liter of 0.7 μm filtered autoclave-sterilized seawater). To remove any possible contamination due to the presence of the organic-rich growth media, the liquid bacterial culture was pelleted by centrifugation at 5000g for 5 min, washed, and
more definitive understanding of the role PBAP play in affecting global and regional climate, additional studies which identify and study their impact are required. Oceans cover 71% of the Earth’s surface and represent a significant source of naturally occurring gases and particles, with sea spray aerosol (SSA) representing one of the most abundant aerosol types in the atmosphere.39,40 In addition to a variety of inorganic salts, seawater is comprised of a complex mixture of dissolved organic species including lipids,41 amino acids,42 and proteins,43 as well as particulate organic matter, such as colloids,44,45 bacteria, and phytoplankton.46 SSA is ejected into the atmosphere when entrained air bubbles, produced by breaking waves, burst at the surface of the ocean.40,47 As bubbles rise through the water column, they scavenge surface active organic matter and marine microorganisms, forming particles that are enriched in these materials relative to their respective mean seawater concentrations.48−56 As such, the ocean represents a potentially large and chemically complex source of atmospheric PBAP.23,57 The majority of marine aerosol studies that investigate the enrichment of organic species do so as a function of the ratio of absolute mass of salt to organic species for an ensemble of collected particles.53,56 While these studies have provided valuable information on the sensitivity of SSA to oceanic biological conditions, they have not provided insight into the chemical mixing state (i.e., the associations between chemical species) of individual SSA particles, a critical factor in determining cloud properties in marine environments.58−61 Field-deployable single-particle mass spectrometers (SPMS) are powerful tools that measure the size-resolved chemical composition of individual particles in real-time.62 The real-time detection capability of SPMS make them ideally suited for in situ studies which constrain the factors controlling marine PBAP emissions and their climate-relevant properties (e.g., analyzing the composition of ice crystal residues).63,64 To fully establish links between ocean biology and marine PBAP emissions, the mass spectral signatures for marine biogenic species need to be fully characterized under more controlled conditions. Although SPMS have previously been used to analyze terrestrial PBAP,16,65,66 the inherent complexity of the seawater biochemical matrix can preclude detection of previously identified mass spectral markers of biological particles in investigations of marine aerosols. Identification of marine PBAP sources requires comparison of the mass spectral signatures of ambient particles to laboratory measured standards of known origin.67 In this study, we investigate the SPMS signatures of PBAP by comparing particles generated using two separate methods: (1) a sintered glass bubbler submerged in a synthetic NaCl and MgCl2 solution to which heterotrophic bacteria were added and (2) a 33 m long, linear glass-walled hydraulic wave channel filled with seawater drawn from the coastal Pacific Ocean which was amended with multiple additions of biogenic material. The bubbler experiment represents “pristine” seawater without dissolved organic interferences, whereas the wave channel corresponds to coastal seawater which contains biogenic organic species and transition metals associated with residual rust in the flume. For each aerosol generation technique, the chemical compositions of individual SSA particles were measured using an aerosol time-of-flight mass spectrometer (ATOFMS). Additionally, for the wave channel study, particles were collected for complementary off-line electron microscopy analysis. 1325
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resuspended a total of three times; once in 0.1 μm filtered seawater and then twice more in the NaCl/MgCl2/Milli-Q water solution. SSA was generated using a 500 mL bubble bursting apparatus, which consisted of a glass container and a sintered glass frit with porosity “C” rated at 25−50 μm (Ace Glass 7164−26, Vineland, NJ) submerged approximately 25 cm below the surface of the seawater control solution. To facilitate comparison, >4500 particles were sampled before and after addition of heterotrophic bacteria. Bubbles were generated by flowing approximately 0.4 L/min of clean, dry filtered air through the glass filter. A schematic diagram of the bubbling apparatus is provided in the Supporting Information, SI (Figure S2). Prior to use, all glassware was rinsed with Milli-Q water, 10% hydrochloric acid, hexanes, acetone, methanol, and finally with Milli-Q again. The glassware was then combusted with the same procedure as that used for purifying the salts. 2.3. CAICE Fall Intensive Overview. Sea spray aerosol measurements were made as part of the Center for Aerosol Impacts on Climate and the Environment (CAICE) Fall Intensive Campaign from October 31st to November 16th, 2011. Complete details of this campaign are provided elsewhere,61 so only a brief discussion will be given here. Nascent SSA was generated by breaking waves in a well characterized 33 m long, 0.5 m wide, sealed, glass-walled wave channel, which was retrofitted with a clean air handling system.61 While previous sea spray studies have traditionally employed artificial aerosol generation techniques,55,73,74 the wave flume accurately reproduces the sea spray production process of plunging breakers,75 in order to produce particles which are more representative of natural SSA in both size and chemical composition.61 The wave tank was filled to a depth of 0.6 m with seawater drawn from the coastal Pacific Ocean at the Scripps Pier (32° 52.02′ N, 117° 15.43′ W), passed through sand filters designed to remove large debris, and delivered directly into the wave channel. Here, we compare control signatures with results from a five day “mesocosm” experiment, in which the seawater composition was modulated through four separate additions of heterotrophic bacteria cultures, bacterial growth media (ZoBell 2216E), a phytoplankton culture, and f/ 2 growth media.76,61 A detailed description of each addition is provided in SI Table S1. As part of the mesocosm experiment, a variety of methods were used to characterize the seawater in the wave flume, including measurements of the concentrations of chlorophyll-a (chl-a), total organic carbon (TOC), and a variety of transition metals, as well as cell abundances of photosynthetic eukaryotes, heterotrophic bacteria, and cyanobacteria.61 Descriptions of collection and analysis techniques for each of these are presented in the SI. Additionally, SI Figure S1 displays the time-resolved values of chl-a, TOC, and cell abundances.
these three types in Figure 1. An example mass spectrum of the bioparticle type, which accounted for up to 21% of the
Figure 1. Representative mass spectra of individual particles defined as (A) Bio, (B) SS-OC, and (C) SS. Each spectrum is divided into negative (left) and positive (right) spectra.
supermicrometer particles during the CAICE Fall Intensive Campaign, is displayed in Figure 1A. In addition to the enhanced abundance of Mg+, the negative ion spectra of these particles contain markers of organic nitrogen (ON; 26CN−, 42 CNO−, 120,122MgCl2CN−, 72C3H6NO+) and phosphate (P; 63 PO2−, 79PO3−, and 97H2PO4−), constituents which have also been observed in SPMS analyses of terrestrial PBAP.16,65,66 It is important to note the initial ATOFMS source apportionment of bioparticles uses both the positive ions with an intense Mg+, and often Ca+ or K+, in combination with negative ion spectra which show far higher sensitivity to the ON and P biomarker ions than the positive ion spectra. The use of both positive and negative ion spectra for apportionment is a critical distinction from other SPMS studies which can use only one polarity at a time, usually positive ions, for apportioning particles.77 It should be noted that while bioparticles shown in Figure 1A include both negative and positive ion spectra, some of the bubbler bioparticles lacked negative ion spectra. The positive ion spectra of these bioarticles matched the spectra of particles also producing negative ion spectra, and contained a characteristic peak at m/z 19 (H3O+), suggesting the particles retained water which has been shown to suppress negative ion formation.69 The other two particle types in the size range relevant to this current study are SS and SS-OC.61,78,79 The SS particle types
3. RESULTS AND DISCUSSION 3.1. Bubbling Apparatus Experiments. As described in Prather et al.,61 sea spray aerosol produced by breaking waves is composed of four common particle types with characteristic single particle chemical signatures and size distributions. These classes are identified as sea salt (SS), sea salt with organic carbon (SS-OC), bioparticles (Bio), and organic carbon (OC). OC type particles are smaller than the lower-limit operating range of the ATOFMS used in the bubbler control study. Therefore, only the three former particle types were detected. Representative dual-polarity mass spectra are shown for each of 1326
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6.8 × 106 cells mL−1; Figure 3, orange circles) under low chl-a conditions, while a final addition of a phytoplankton culture significantly increased the chl-a concentrations (0.06 to 6.38 mg m−3, red line).
show distinct differences in the negative ion signatures. The mass spectrum of a SS-OC particle displayed in Figure 1B is characterized by ON and P markers and intense cluster ion peaks comprising inorganic and organic species (e.g., 81,83 Na2Cl+, 120,122MgCl2CN−, 129,131,133MgCl3−). The mass spectrum of the other SS particle type (Figure 1C) contains intense sodium and chloride peaks (23Na+, 35,37Cl−), as well as less intense magnesium (24Mg+) and sodium chloride ionic clusters (46Na2+, 81,83Na2Cl+, 58,60NaCl−, 93,95NaCl2), a pattern which can be attributed to freshly produced sea salt particles.61,70,79 As described previously, we infer that differences in the mass spectra of these two types are related to differences in the relative amounts of organic carbon mixed with the salt-rich particles.61 In order to determine which SPMS signatures are related to marine PBAP, we investigated which particle types showed an increase upon addition of heterotrophic bacteria to the NaCl/ MgCl2 control solution. Figure 2 displays the relative
Figure 3. ATOFMS fraction of Bio (blue line) and SS-OC (green line) particles and the seawater concentrations of heterotrophic bacteria (orange circles) and chlorophyll a (red line) measured over the course of the mesocosm experiment. Times of the four additions of biogenic material are indicated with black arrows. The orange arrow indicates the time period when the concentration of heterotrophic bacteria began to rise after the addition of the ZoBell growth media. Descriptions of each addition are provided in SI Table S1.
The bubbling experiments show the Bio and SS-OC particle types as being the main SSA signatures related to the presence of bacteria, and thus one would expect their abundances to show some correlation with heterotrophic bacteria cell concentrations in the wave flume. It would also be expected that these markers may also serve as more general indicators of elevated organic content in seawater during periods with higher biological activity. Figure 3 shows temporal variations in the ATOFMS fractions of Bio (blue line) and SS-OC (green line) particles, as well as seawater heterotrophic bacteria and chl-a concentrations. The black arrows at the top indicate the times of the four additions of biological material (SI Table S1). Most notably, the first addition at day 0.61 consisted of heterotrophic bacteria and ZoBell growth media, which was followed by an increase in heterotrophic bacterial abundance beginning on day 1.24 (Figure 3, orange arrow). This delay is likely due to the time required for the heterotrophic bacteria processing of the organic-rich ZoBell growth media. Additionally, it should be noted that the biological material was added ∼2 m ahead of the wave breaking region, while the seawater samples were collected ∼20 m beyond the wave breaking region. Thus for the wave flume experiments, in contrast to the bubbling experiments, there was an offset in the temporal behavior of seawater bacteria concentrations and the associated SSA signatures produced. As shown in Figure 3, approximately one day after the heterotrophic bacteria were added and concentrations began to increase, the ATOFMS fractions of Bio and SS-OC particles also increased. The smaller relative increase in SSA biosignatures in the wave channel experiment compared to the bubbling experiment could be due to the fact that bacteria and biogenic species were already present in the natural seawater in the wave channel study. Previous bubbling studies have demonstrated that bubble surfaces can become saturated with hydrophobic species as they rise to the top of the water column and thus can only eject a limited amount of material under high biological activity conditions.80,81 The fractions of Bio and SS-OC particles increased under elevated bacteria and chl-a concentrations, confirming that
Figure 2. Relative contributions of the different particle types measured by the ATOFMS for no bacteria (left) and bacteria added (right) for particles generated by bubbling a seawater control solution (SW Proxy) composed of NaCl and MgCl2. Blue represents Bio particles, green represents SS-OC particles, and red indicates SS particles.
abundance of the three major particle types for the unamended inorganic (left) and bacteria-enriched solutions (right). Before addition of bacteria (Figure 2, left), SS particles accounted for 90% of the sampled particles (red), while only ∼10% of the sampled particles were classified as Bio (blue) or SS-OC (green), respectively. Upon addition of bacteria (Figure 2, right), the fraction of Bio and SS-OC particles dramatically increased from 9.5% to 40% and 0.15% to 34%, respectively. The increase in these particle types upon addition of bacteria confirms that the Bio particle type and the corresponding organic nitrogen and phosphate signatures are indeed indicative of the presence of marine bacteria. This mass spectral signature combination represents: (1) intact heterotrophic bacteria cells, (2) fragments of cells, or (3) bacterial exudates. 3.2. CAICE Mesocosm Experiment. To investigate the applicability of these signatures to marine-derived PBAP, we compared the particles produced during the bubbling study to those generated using breaking waves in a sealed glass wave channel. Throughout a mescocom study, in which the biological conditions of the seawater were modulated by controlled additions of biogenic material, ATOFMS measurements were made concurrently with the suite of seawater analyses listed in 2.3. In the mesocosm experiment, initial additions of bacteria cultures and organic-rich growth media led to elevated heterotrophic bacteria concentrations (6.4 × 105 to 1327
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Figure 4. (A) ATOFMS fraction of silver containing particles (black line) and the seawater concentrations of heterotrophic bacteria (orange circles) measured over the mesocosm experiment. (B) Scatterplot of the ATOFMS fraction of silver containing particles and seawater concentration heterotrophic bacteria.
Figure 5. (A) Negative (left) and positive (right) mass spectra of a representative individual silver containing particle. (B) Relative contributions of the different particle types as measured by the ATOFMS for nonsilver containing particles (left) and silver containing particles (right).
increase in concentration occurs until it peaks at 16% ∼20 h later. This trend is also shown in the scatter plot in Figure 4B. A strong, positive correlation (R2 = 0.90) is found for the concentration of heterotrophic bacteria in seawater and the fraction of SSA particles associated with silver. In order to better understand the association between silver ions and bacteria, it is necessary to further examine the mass spectra of these silver-containing particles to determine if silver can be used as a tracer for the presence of marine bacteriaassociated aerosol. A representative mass spectrum of a particle containing silver ions is provided in Figure 5A. As was the case with the particles previously identified as Bio and SS-OC, ON and P biomarker ions at m/z = −26, −42, and −79 are present. Additional transition metals (52Cr+ and 56Fe+), are also observed. In fact, over 94% of Ag-containing particles were
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