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RESEARCH ARTICLE
Contents Vol 5(6)

Ice nucleation activity of bacteria isolated from snow compared with organic and inorganic substrates

Roya Mortazavi A , Christopher T. Hayes A and Parisa A. Ariya A B
+ Author Affiliations
- Author Affiliations

A Department of Chemistry and Department of Atmospheric and Oceanic Sciences, McGill University, 801 Sherbrooke St W, Montréal, QC, H3A 2K6, Canada.

B Corresponding author. Email: parisa.ariya@mcgill.ca

Environmental Chemistry 5(6) 373-381 https://doi.org/10.1071/EN08055
Submitted: 18 August 2008  Accepted: 19 November 2008   Published: 18 December 2008

Environmental context. Biological ice nucleators have been found to freeze water at very warm temperatures. The potential of bio-aerosols to greatly influence cloud chemistry and microphysics is becoming increasingly apparent, yet detailed knowledge of their actual role in atmospheric processes is lacking. The formation of ice in the atmosphere has significant local, regional and global influence, ranging from precipitation to cloud nucleation and thus climate. Ice nucleation tests on bacteria isolated from snow and laboratory-grown bacteria, in comparison with those of known organic and inorganic aerosols, shed light on this issue.

Abstract. Ice nucleation experiments on bacteria isolated from snow as well as grown in the laboratory, in comparison with those of known organic and inorganic aerosols, examined the importance of bio-aerosols on cloud processes. Snow samples were collected from urban and suburban sites in the greater Montreal region in Canada (45°28′N, 73°45′W). Among many snow bacterial isolates, eight types of bacterial species, none belonging to known effective ice nucleators such as Pseudomonas or Erwinia genera, were identified to show an intermediate range of ice nucleation activity (–12.9 ± 1.3°C to –17.5 ± 2.8°C). Comparable results were also obtained for molten snow samples and inorganic suspensions (kaolin and montmorillonite) of buffered water solutions. The presence of organic molecules (oxalic, malonic and succinic acids) had minimal effect (<2°C) on ice nucleation. Considering experimental limitations, and drawing from observation in snow samples of a variety of bacterial populations with variable ice-nucleation ability, a shift in airborne-species population may significantly alter glaciation processes in clouds.

Additional keywords: bio-aerosols, cloud chemistry.


Acknowledgements

We appreciate the financial support from the Natural Science and Engineering Research Council of Canada (NSERC), Canadian Foundation for Innovation (CFI), and McGill Dawson Chair to P. A. Ariya. We thank Patrick Lulin for growing laboratory cultures of Pseudomonas syringae and Dr Gwyn A. Beattie of Iowa State University for donating viable samples of P. syringae.


References


[1]   Forster P., Ramaswamy V., Artaxo P., Berntsen T., Betts R., Fahey D. W., Haywood J., Lean J., Lowe D. C., Myhre G., Nganga J., Prinn R., Raga G., Schulz M., Van Dorland R., Changes in atmospheric constituents and in radiative forcing, in Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, H. L. Miller) 2007 (Cambridge University Press: Cambridge, UK).

[2]   Heymsfield A., Stith J., Rogers D., Field P., DeMott P., Detwiler A., Knight C., Penner J., Sassen K., Thompson G., Cotton B., Cantrell W., Lewis S., Vali G., Cooper A., Platnick S., Dye J., Isaac G., Lohmann U., Möhler O., Seifert A., Cziczo D., Shaw R., The Ice in Clouds Experiment Research Plan 2005 (National Center for Atmospheric Research: Boulder, CO).

[3]   A. J. Heymsfield , R. M. Sabin , Cirrus crystal nucleation by homogeneous freezing of solution droplets. J. Atmos. Sci. 1989 , 46,  2252.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[4]   H. R. Pruppacher , A new look at homogeneous ice nucleation in supercooled water drops. J. Atmos. Sci. 1995 , 52,  1924.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[5]   Vali G., Ice nucleation – theory: a tutorial, Presented at Ice Formation in the Atmosphere Colloquium, 14–25 June 1999, Boulder, CO 1999 (National Center for Atmospheric Research: Boulder, CO).

[6]   B. Sattler , H. Puxbaum , R. Psenner , Bacterial growth in supercooled cloud droplets. Geophys. Res. Lett. 2001 , 28,  239.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[7]   E. J. Carpenter , S. Lin , D. G. Capone , Bacterial activity in South Pole snow. Appl. Environ. Microbiol. 2000 , 66,  4514.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[8]   R. H. Pierre Amato , O. Magand , M. Sancelme , A.-M. Delort , C. Barbante , C. Boutron , C. Ferrari , Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol. Ecol. 2007 , 59,  255.
        | PubMed |  open url image1

[9]   J. Sun , P. A. Ariya , Atmospheric organic and bio-aerosols as cloud condensation nuclei (CCN): a review. Atmos. Environ. 2006 , 40,  795.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[10]   C. L. Hew , D. S. C. Yang , Protein interaction with ice. Eur. J. Biochem. 1992 , 203,  33.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[11]   H. Obata , Y. Saeki , J. Tanishita , T. Tokuyama , H. Hori , Y. Higashi , Identification of an ice-nucleating bacterium KUIN-1 as Pseudomonas fluorescens and its ice nucleation properties. Agric. Biol. Chem. 1987 , 51,  1761.
        |  CAS |  open url image1

[12]   H. Obata , T. Nakai , J. Tanishita , T. Tokuyama , Identification of an ice-nucleation bacterium and its ice nucleation properties. J. Ferment. Bioeng. 1989 , 67,  143.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[13]   H. Obata , K. Takinami , J. Tanishita , Y. Hasegawa , S. Kawate , T. Tokuyama , T. Ueno , Identification of a new ice-nucleation bacterium and its ice nucleation properties. Agric. Biol. Chem. 1990 , 54,  725.
        |  CAS |  open url image1

[14]   G. J. Warren , Bacterial ice nucleation: molecular biology and applications. Biotechnol. Genet. Eng. Rev. 1987 , 5,  107.
        |  CAS |  open url image1

[15]   A. G. Govindarajan , S. E. Lindow , Phospholipid requirement for expression of ice nuclei in Pseudomonas syringae and in vitro. J. Biol. Chem. 1988 , 263,  9333.
        |  CAS | PubMed |  open url image1

[16]   L. M. Kozloff , M. A. Turner , F. Arellano , Formation of bacterial membrane ice-nucleating lipoglycoprotein complexes. J. Bacteriol. 1991 , 173,  6528.
        |  CAS | PubMed |  open url image1

[17]   L. M. Kozloff , M. A. Turner , F. Arellano , M. Lute , Phosphatidylinositol, a phospholipid of ice-nucleation bacteria. J. Bacteriol. 1991 , 173,  2053.
        |  CAS | PubMed |  open url image1

[18]   P. Wolber , G. Warren , Bacterial ice nucleation proteins. Trends Biochem. Sci. 1989 , 14,  179.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[19]   Y. Kumaki , K. Kawano , K. Hikichi , T. Matsumoto , N. Matsushima , A circular loop of the 16-residue repeating unit in ice nucleation protein. Biochem. Biophys. Res. Commun. 2008 , 371,  5.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[20]   R. L. Green , L. V. Corotto , G. J. Warren , Deletion of mutagenesis of the ice-nucleation gene from Pseudomonas syringae S203. Mol. Gen. Genet. 1988 , 215,  165.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[21]   L. R. Maki , E. L. Galyan , M. Chang-chien , D. R. Caldwell , Ice nucleation induced by Pseudomonas syringae. Appl. Microbiol. 1974 , 28,  456.
        |  CAS | PubMed |  open url image1

[22]   B. Wowk , G. M. Fahy , Inhibition of bacterial ice nucleation by polyglycerol polymers. Cryobiology 2002 , 44,  14.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[23]   W. Szyrmer , I. Zawadzki , Biogenic and anthropogenic sources of ice-forming nuclei: a review. Bull. Am. Meteorol. Soc. 1997 , 78,  209.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[24]   S. S. Hirano , L. S. Baker , C. D. Upper , Ice nucleation temperature of individual leaves in relation to population sizes of ice nucleation-active bacteria and frost injury. Plant Physiol. 1985 , 77,  259.
        | Crossref | PubMed |  open url image1

[25]   A. Blondeaux , J.-F. Hamel , P. Widehem , N. Cochet , Influence of water activity on the ice-nucleating activity of Pseudomonas syringae. J. Ind. Microbiol. Biotechnol. 1999 , 23,  514.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[26]   S. A. Yankofsky , Z. Levin , T. Bertold , N. Sandlerman , Some basic characteristics of bacterial freezing nuclei. J. Appl. Meteorol. 1981 , 20,  1013.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[27]   S. Matthias-Maser , R. Jaenicke , Examination of atmospheric bioaerosol particles with radii >0.2 μm. J. Aerosol Sci. 1994 , 25,  1605.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[28]   O. Mohler , P. J. DeMott , G. Vali , Z. Levin , Microbiology and atmospheric processes: the role of biological particles in cloud physics. Biogeosciences 2007 , 4,  1059.
         open url image1

[29]   P. A. Ariya , M. Amyot , New directions: the role of bioaerosols in atmospheric chemistry and physics. Atmos. Environ. 2004 , 38,  1231.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[30]   P. A. Ariya , O. Nepotchatykh , O. Ignatova , M. Amyot , Microbial degradation of organic compounds. Geophys. Res. Lett. 2002 , 29,  2077.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[31]   B. J. Mason , Ice-nucleating properties of clay minerals and stony meteorites. Q. J. R. Meteorol. Soc. 1960 , 86,  552.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[32]   G. Funke , E. Falsen , C. Barreau , Primary identification of Microbacterium spp. encountered in clinical specimens as CDC coryneform group A-4 and A-5 bacteria. J. Clin. Microbiol. 1995 , 33,  188.
        |  CAS | PubMed |  open url image1

[33]   P. A. Rusin , J. B. Rose , C. N. Haas , C. P. Gerba , Risk assessment of opportunistic bacterial pathogens in drinking water. Rev. Environ. Contam. Toxicol. 1997 , 152,  57.
        |  CAS | PubMed |  open url image1

[34]   G. Warren , P. Wolber , Molecular aspects of microbial ice nucleation. Mol. Microbiol. 1991 , 5,  239.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[35]   J. L. Zhao , C. S. Orser , Conserved repetition in the ice nucleation gene inaX from Xanthomonas campestris pv. Translucens. Mol. Gen. Genet. 1990 , 223,  163.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[36]   M. Kanakidou , J. H. Seinfeld , S. N. Pandis , I. Barnes , F. J. Dentener , M. C. Facchini , R. Van Dingenen , B. Ervens , et al. Organic aerosol and global climate modelling: a review. Atmos. Chem. Phys. 2005 , 5,  1053.
        |  CAS |  open url image1

[37]   Q. Zhang , J. L. Jimenez , M. R. Canagaratna , J. D. Allan , H. Coe , I. Ulbrich , M. R. Alfarra , A. Takami , et al. Ubiquity and dominance of oxygenated species in organic aerosols in anthropogenically-influenced Northern Hemisphere midlatitudes. Geophys. Res. Lett. 2007 , 34,  L13801.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[38]   H. R. Pruppacher , M. Neiburger , The effect of water-soluble substances on the supercooling of water drops. J. Atmos. Sci. 1963 , 20,  376.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[39]   G. Vali , Quantitative evaluation of experimental results on the heterogeneous freezing nucleation of supercooled liquids. J. Atmos. Sci. 1971 , 28,  402.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[40]   Pruppacher H. R., Klett J. D., Microphysics of Clouds and Precipitation 1997 (Kluwer Academic Publishers: Boston, MA).

[41]   L. M. Kozloff , A. M. Schofield , M. Lute , Ice nucleation activity of Pseudomonas syringae and Erwinia herbicola. J. Bacteriol. 1983 , 153,  222.
        |  CAS | PubMed |  open url image1

[42]   M. Dubrovský , V. Petera , B. Sikyta , H. Hegerova , Measurement of the ice nucleation activity of Pseudomonas syringae CCM 4073. Biotechnol. Tech. 1989 , 3,  173.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[43]   L. R. Maki , K. J. Willoughby , Bacteria as biogenic sources of freezing nuclei. J. Appl. Meteorol. 1978 , 17,  1049.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[44]   A. Salam , U. Lohmann , B. Crenna , G. Lesins , P. Klages , D. Rogers , R. Irani , A. MacGillivray , M. Coffin , Ice nucleation studies of mineral dust particles with a new continuous flow diffusion chamber. Aerosol Sci. Technol. 2006 , 40,  134.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[45]   R. C. Schaller , N. Fukuta , Ice nucleation by aerosol particles: experimental studies using a wedge-shaped ice thermal diffusion chamber. J. Atmos. Sci. 1979 , 36,  1788.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[46]   D. C. Rogers , Development of a continuous flow thermal gradient diffusion chamber for ice nucleation studies. Atmos. Res. 1988 , 22,  149.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[47]   S. E. Wood , M. B. Baker , B. D. Swanson , Instrument for studies of homogeneous and heterogeneous ice nucleation in free-falling supercooled water droplets. Rev. Sci. Instrum. 2002 , 73,  3988.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[48]   M. Ettner , S. K. Mitra , S. Borrman , Heterogeneous freezing of single sulfuric acid solution droplets: laboratory experiments utilizing an acoustic levitator. Atmos. Chem. Phys. 2004 , 4,  1925.
        |  CAS |  open url image1

[49]   J. K. Edzwald , C. R. O’Mell , Clay distributions in recent estuarine sediments. Clays Clay Miner. 1975 , 23,  39.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1