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Geographic, Seasonal, and Precipitation Chemistry Influence on the Abundance and Activity of Biological Ice Nucleators in Rain and Snow

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Geographic, Seasonal, and Precipitation Chemistry Influence on the Abundance and Activity of Biological Ice Nucleators in Rain and Snow Geographic, seasonal, and precipitation chemistry influence on the abundance and activity of biological ice nucleators in rain and snow Brent C. Christnera,1, Rongman Caib,2, Cindy E. Morrisc, Kevin S. McCarterb, Christine M. Foremand,e, Mark L. Skidmoref, Scott N. Montrossf, and David C. Sandsg Departments of aBiological Sciences and bExperimental Statistics, Louisiana State University, Baton Rouge, LA 70803; cUnite´de Pathologie Ve´ge´ tale UR407, Institut National de la Recherche Agronomique, F-84140 Montfavet, France; and dCenter for Biofilm Engineering and Departments of eLand Resources and Environmental Sciences, fEarth Sciences, and gPlant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717 Communicated by P. Buford Price, Jr., University of California, Berkeley, CA, October 7, 2008 (received for review August 14, 2008) Biological ice nucleators (IN) function as catalysts for freezing at diflava, Pseudomonas fluorescens, Pantoea agglomerans, and -relatively warm temperatures (warmer than ؊10 °C). We examined Xanthomonas campestris), but also fungi (e.g., Fusarium ave the concentration (per volume of liquid) and nature of IN in naceum), algae such as Chlorella minutissima, and birch pollen precipitation collected from Montana and Louisiana, the Alps and (5). P. syringae (6–8) and F. avenaceum (7) in particular have Pyrenees (France), Ross Island (Antarctica), and Yukon (Canada). been detected in atmospheric aerosols and clouds. Ice- The temperature of detectable ice-nucleating activity for more nucleating strains of P. syringae possess a 120- to 180-kDa ice than half of the samples was > ؊5 °C based on immersion freezing nucleation active protein in their outer membrane comprised testing. Digestion of the samples with lysozyme (i.e., to hydrolyze of contiguous repeats of a consensus octapeptide; the protein bacterial cell walls) led to reductions in the frequency of freezing binds water molecules in an ordered arrangement, providing a (0–100%); heat treatment greatly reduced (95% average) or com- nucleating template that enhances ice crystal formation (9). pletely eliminated ice nucleation at the measured conditions in Based on reports of ice-nucleating bacteria at altitudes of every sample. These behaviors were consistent with the activity several kilometers (6, 10) and the warm temperatures at which being bacterial and/or proteinaceous in origin. Statistical analysis they function as ice nuclei (Ϫ2°CtoϪ7 °C; ref. 5), biological IN revealed seasonal similarities between warm-temperature ice- may play a role in the precipitation cycle. Very large numbers of nucleating activities in snow samples collected over 7 months in microorganisms inhabit leaf surfaces globally (1024 to 1026 cells; Montana. Multiple regression was used to construct models with ref. 11), deciduous plants harbor large populations of ice- biogeochemical data [major ions, total organic carbon (TOC), par- nucleating bacteria on their leaves (Ϸ105 ice-nucleating bacteria Ϫ ticle, and cell concentration] that were accurate in predicting the cm 2; ref. 12), and various species of ice-nucleating bacteria or concentration of microbial cells and biological IN in precipitation biological IN in general have been detected in phytoplankton- 2؉ ؉ based on the concentration of TOC, Ca , and NH4 , or TOC, cells, rich marine waters (13), snow (14, 15), and rain (15, 16). 2؉ ؉ ؉ 3؊ 2؊ ؊ ؊ Ca ,NH4 ,K ,PO4 ,SO4 ,Cl , and HCO3 . Our results indicate that Although biological particles represent a significant component biological IN are ubiquitous in precipitation and that for some of atmospheric aerosols (17), few data have been available on the geographic locations the activity and concentration of these par- concentration of airborne biological ice nuclei. Therefore, the ticles is related to the season and precipitation chemistry. Thus, our abundance and distribution of the most active IN in the atmo- research suggests that biological IN are widespread in the atmo- sphere (i.e., biological IN) are described in only a very limited sphere and may affect meteorological processes that lead to way and their meteorological role is unknown. precipitation. Our previous work on snowfall collected from a variety of mid- and high-latitude locations indicated that biological IN are atmosphere ͉ climate ͉ microbial dissemination ͉ biological ice nuclei ubiquitous in precipitation from a range of global locations and represent the most active IN at temperatures warmer than Ϫ t subzero temperatures warmer than Ϫ40 °C, aerosol 10 °C (14). Here, we present results from a comprehensive Aparticles in clouds initiate freezing through the hetero- analysis of biological IN in snow and rain and use statistical geneous nucleation of ice directly from water vapor or by methods to examine correlations between the microbiological freezing droplets via several mechanisms: deposition, conden- and biogeochemical data. A primary objective of this study was sation, contact, and immersion freezing (1). These processes to elucidate biogeochemical markers of the presence of biolog- lead to ice formation in clouds that can trigger precipitation. ical IN to provide information on conditions that favor their A diverse range of natural and anthropogenic particles, re- distribution in the atmosphere and predict other contexts where ferred to as ice-forming nuclei or ice nucleators (IN), are they would be abundant. We show that for some geographical capable of initiating the ice phase (2). The maximum temper- locations the concentration (i.e., per rain or snow water equiv- ature at which an IN can initiate freezing is specific to that alent volume) and activity of biological IN is correlated with the nucleator, but they function similarly by providing templates biogeochemistry of the precipitation and season of deposition. for the aggregation of individual water molecules in the configuration of an ice embryo, resulting in a subsequent phase Author contributions: B.C.C., C.E.M., and D.C.S. designed research; B.C.C., R.C., and C.E.M. change and the cascade of crystal formation (3). Consequently, performed research; C.M.F., M.L.S., and S.N.M. contributed new reagents/analytic tools; knowledge of the nature and sources of IN in the atmosphere B.C.C., R.C., and K.S.M. analyzed data; and B.C.C. wrote the paper. is important for understanding the meteorological processes The authors declare no conflict of interest. responsible for precipitation. The most active naturally occur- 1To whom correspondence should be addressed. E-mail: [email protected]. ring IN are biological in origin and have the capacity to 2Present address: Department of Plant Pathology, Virginia Polytechnic Institute and State catalyze freezing at temperatures near Ϫ2 °C (4). The most University, Blacksburg, VA 24061. widespread and well-studied biological aerosols with ice- This article contains supporting information online at www.pnas.org/cgi/content/full/ nucleating activity are comprised of certain species of plant- 0809816105/DCSupplemental. associated bacteria (Pseudomonas syringae, Pseudomonas viri- © 2008 by The National Academy of Sciences of the USA 18854–18859 ͉ PNAS ͉ December 2, 2008 ͉ vol. 105 ͉ no. 48 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0809816105 Downloaded by guest on September 26, 2021 Ϫ1 A 160 ice nuclei L ). Calculation of the ice nuclei concentration at a BB - 4 Oct given temperature using immersion freezing testing requires that BB - 4 Nov at least one aliquot tested remains unfrozen. For this reason, it 140 BS - 2 Dec BB - 29 Dec was not possible to determine the ice nuclei concentration over 1 - 120 YC - 29 Dec the entire experimental temperature range tested for all samples. L BB - 15 Jan i Given that the cumulative concentration of ice nuclei typically e l BB - 24 Feb c 100 u n u YC - 24 Feb increases with decreasing temperature, samples where all ali- MB - 15 Mar e quots were frozen at the warmer temperatures assayed probably c i 80 BS - 6 Apr contained much higher ice nuclei concentrations at Ϫ9 °C than e VdL - 29 Dec v i t SAT - 26 Jan the upper limit values we report. In general, snow samples from a l 60 u CL - 16 Feb France contained higher concentrations of ice nuclei that were m VdL - 18 Feb u active at warmer temperatures relative to those in samples from C 40 FR - 20 Feb Montana and higher latitudes. FR - 22 Feb LC - 10 Mar In rain samples from Louisiana, the lowest and highest ice 20 WG - 6 Jun nuclei concentrations at temperatures warmer than Ϫ10 °C (41 MCM - 29 Jan and 510 ice nuclei LϪ1, respectively) were observed in samples 0 -9 -8 -7 -6 -5 -4 -3 collected in August and October, respectively (Fig. 1B). Com- o parison of the cumulative ice nuclei concentration spectra in rain Temperature ( C) collected from July through October 2007 revealed variation B 700 among the samples, with differences ranging by a factor of 12 to 180 at temperatures between Ϫ5 °C and Ϫ9 °C. There were 3 Jul 600 clearly 2 outlying samples (August 17 and October 4) that 19 Jul contained significantly higher ice nuclei concentrations at Ϫ9°C 27 Jul Ϫ 1- (480 and 510 ice nuclei L 1, respectively) than the other rainfalls L 31 Jul 500 ielcun 17 Aug analyzed. However, the highest measurable ice nuclei concen- 28 Aug tration was observed at Ϫ11 °C (660 ice nuclei LϪ1) from a 400 29 Aug 7 Sep sample collected on August 28 in which the ice nuclei concen- SCIENCES Ϫ Ϫ e ice 12 Sep tration increased nearly 10-fold between 10 °C and 11 °C ENVIRONMENTAL vitalu 300 22 Sep (Fig. 1B). When the cumulative ice nuclei concentration at 25 Sep temperatures warmer than Ϫ7 °C in snow from various locations muC 4 Oct 200 5 Oct (Fig. 1A) is compared with that in rain from Louisiana (Fig. 1B), 8 Oct the range of ice nuclei concentrations observed was similar 17 Oct Ϫ1 Ϫ1 100 (1–150 ice nuclei L in snow; 8–230 ice nuclei L in rain).
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