Biogeosciences
www.biogeosciences.net
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4
1
2007
10.5194/bg-4-115-2007
http://www.biogeosciences.net/4/115/2007/
http://www.biogeosciences.net/4/115/2007/bg-4-115-2007.html
http://www.biogeosciences.net/4/115/2007/bg-4-115-2007.pdf
115
124
2007-02-12
Fluorescent pseudomonads isolated from Hebridean cloud and rain water produce biosurfactants but do not cause ice nucleation
H. E. Ahern
K. A. Walsh
T. C. J. Hill
t.c.j.hill@uel.ac.uk
B. F. Moffett
University of East London, Romford Road, Stratford, London, UK
Environment Agency, Wallingford, UK
Microorganisms were discovered in clouds over 100 years ago but information
on bacterial community structure and function is limited. Clouds may not
only be a niche within which bacteria could thrive but they might also
influence dynamic processes using ice nucleating and cloud condensing
abilities. Cloud and rain samples were collected from two mountains in the
Outer Hebrides, NW Scotland, UK. Community composition was determined using
a combination of amplified 16S ribosomal DNA restriction analysis and
sequencing. 256 clones yielded 100 operational taxonomic units (OTUs) of
which half were related to bacteria from terrestrial psychrophilic
environments. Cloud samples were dominated by a mixture of fluorescent
<i>Pseudomonas</i> spp., some of which have been reported to be ice nucleators. It was
therefore possible that these bacteria were using the ice nucleation (IN)
gene to trigger the Bergeron-Findeisen process of raindrop formation as a
mechanism for dispersal. In this study the IN gene was not detected in any
of the isolates using both polymerase chain reaction (PCR) and differential
scanning calorimetry (DSC). Instead 55% of the total isolates from both
cloud and rain samples displayed significant biosurfactant activity when
analyzed using the drop-collapse technique. All isolates were characterised
as fluorescent pseudomonads. Surfactants have been found to be very
important in lowering atmospheric critical supersaturations required for the
activation of aerosols into cloud condensation nuclei (CCN). It is also
known that surfactants influence cloud droplet size and increase cloud
lifetime and albedo. Some bacteria are known to act as CCN and so it is
conceivable that these fluorescent pseudomonads are using surfactants to
facilitate their activation from aerosols into CCN. This would allow water
scavenging,~countering desiccation, and assist in their widespread
dispersal.
Abdul-Razzak, H. and Ghan, S.: Parameterization of the influence of organic surfactants on aerosol activation, J. Geophys. Res., 109(D3), D03205, doi:10.1029/2003JD004043, 2004.
Amato, P., Menager, M., Sancelme, M., Laj, P., Mailhot, G. D., and Delort, A.: Microbial population in cloud water at the Puy de Dome: Implications for the chemistry of clouds, Atmos. Env., 39, 4143–4153, 2005.
Bauer, H., Giebl, R., Kasper-Giebl, A., Loflund, H., Giebl, H., Hitzenberger, H, Zibuschka, F., and Puxbaum, H.: The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmos. Res., 64, 109–-119, 2002.
Bauer, H., Giebl, H., Hitzenberger, R., Kasper-Giebl, A., Reischl, G., Zibuschka, F., and Puxbaum, H.: Airborne bacteria as cloud condensation nuclei, J. Geophys. Res., 108(D21), AAC 2–1, 2003.
Blas, M., Sobik, M., and Twarowski, R.: Changes of cloud water chemical composition in the Western Sudety Mts., Poland, in: Proceedings of the third International Conference on Fog, Fog Collection and Dew, NetSys International, 2004.
Bodour, A. and Miller-Maier, R.: Application of a modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms, J. Microbiol. Methods, 32, 273–280. 1998.
Bossis, E., Lemanceau, P., Latour, X., and Gardan, L.: The taxonomy of \textitPseudomonas fluorescens and \textitPseudomonas putida: current status and need for revision, Agronomie, 20, 51–63, 2000.
Brimblecombe, P. and Latif, M.: Rediscovering atmospheric surfactants, Env. Chem., 1, 11–12, 2004.
Brown, M., Larson, D., and Bold, H.: Airborne algae: Their abundance and heterogeneity, Science, 143, 583–585, 1964.
Bullrich, K. and Hänel, G.: Effects of organic aerosol constituents on extinction and absorption coefficients and liquid water contents of fog and clouds, Pure Appl. Geophys., 116, 293–301, 1978.
Casareto, B., Suzuki, Y. Okado, K., and Morita, M.:Biological micro particles in rain water, Geophys. Res Lett. 23, 173–176, 1996.
Castrillo, L., Lee, R., Wyman, J., Lee, M., and Rutherford, S.: Field persistence of ice-nucleating active \textitPseudomonas fluorescens strains for biological control of overwintering Colorado potato beetles (Coleoptera: Chrysomelidae), J. Econ. Entomol. 93, 226–233, 2000.
Edwards, A., Van Den Bussche, R., Winchman, H., and Orser, C.: Unusual pattern of bacterial ice nucleation gene evolution, Mol. Biol. Evol., 11(6), 911–920, 1994.
Facchini, M., Mircea, M., Fuzzi, S., and Charlson, R.: Cloud albedo enhancement by surface-active organic solutes in growing droplets. Nature, 401, 257–259, 1999.
Facchini, M., Decasari, S., Mircea, S., Fuzzi, S., and Loglio, G.: Surface tension of atmospheric wet aerosol and cloud/fog droplets in relation to their organic carbon content and chemical composition, Atmos. Environ., 34, 4853–4857, 2000.
Facchini, M., Mircea, M., Fuzzi, S., and Charlson, R.: Influence of soluble surfactant properties on the activation of aerosol particles containing inorganic solute, J. Atmos. Sci. 58, 1465–1467, 2001.
Ferek, R., Garrett, T., Hobbs, P., Strader, S., Johnson, D., Taylor, J., Ackerman, K., Kogan, Y., Liu, Q., Albrecht, B., and Babb, D.: Drizzle suppression in ship tracks, J Atmos. Sci., 57, 2707–2728, 2000.
Franc, G. and DeMott, P.: Cloud activation characteristics of airborne \textitErwinia carotovora cells, J. Appl. Meteorol., 37, 1293–1300, 1998.
Fuzi, S., Mandrioli, P., and Perfetto, A.: Fog droplets – an atmospheric source of secondary biological aerosol particles, Atmos. Env., 31, 287–290, 1997.
Gioda, A., Mayol-Bracero, O., Rodriguez, A., Morales-Garcia, F., and Morales R.: Chemical characterization of cloud water at the East Peak, Puerto Rico, during the rain in cumulus over the ocean experiment (RICO), in: Proceedings of 12th Conference on Cloud Physics, American Meteorological Society, 2003.
Hallet, J. and Mossop, S.: Production of secondary ice particles during the riming process, Nature, 249, 23–28, 1974.
Hirano, S. and Upper, C.: Ecology of ice nucleation-active bacteria, in: Biological Ice Nucleation and Its Applications, edited by: Lee Jr., R., Warren, G., and Gusta, L., APS Press, St. Paul, Minnesota, 41–62, 1995.
Jain, D., Collins-Thompson, D., Lee, H., and Trevors, J.: A drop-collapsing test for screening surfactant producing microorganisms, J. Microbiol. Methods, 13, 271–279, 1991.
Kieft, T.: Ice nucleating activity in Lichens, Appl. Env. Micro., 54, 1678–1681, 1988.
Köhler, H.: The nucleus in the growth of hygroscopic droplets, Trans. Far. Soc., 32, 1152–1161, 1936.
Lindow, S.: The role of Bacterial ice nucleation in frost injury to plants, Ann. Rev. Phytopathol., 21, 363–384, 1983.
Mandrioli, P., Puppi, G., Bagni, N., and Prodi, F.: Distribution of microorganisms in Hailstones, Nature, 246, 416–417, 1973.
Maron, P., Lejon, D., Carvalho, E., Bizet, K., Lemanceau, P. Ranjard, L., and Mougel, C.: Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16S rDNA clone library, Atmos. Env., 39, 3687–3695, 2005.
Moffett B., Walsh, K., Harris J., and Hill T.: Analysis of bacterial community structure using 16S rDNA analysis, Anaerobe 6, 129–131, 2000.
Morris, C., Georgakpoulos, D., and Sands, D.: Ice nucleation active bacteria and their potential role in precipitation, J. Phys. IV France, 121, 87–103, 2005.
Page, R.: TREEVIEW: An application to display phylogenetic trees on personal computers, CABIOS 12, 357–358, 1996.
Pruppacher, H. and Klett, J.: Microphysics of Clouds and Precipitation. 2d ed, Kluwer Academic Publishers, 974, 1997.
Radosevich, J., Wilson, W., Shinn, J., DeSantis, T., and Anderse, G.: Development of a high-volume aerosol collection system for the identification of air-borne micro-organisms, Lett. Appl. Microbiol., 34, 162–167, 2002.
Sattler, B., Puxbaum, H., and Psenner, R.: Bacterial growth in supercooled cloud droplets, Geophys. Res. Lett., 28, 239–242, 2001.
Shulman, M., Jacobson, M., Carlson, R., Synovec, R., and Young, T.: Dissolution behaviour and surface tension effects of organic compounds in nucleating cloud droplets, Geophys. Res. Lett. 23, 277–280, 1996.
Snider, J., Layton, R., Caple, G., and Chapman, D.: Bacteria as condensation nuclei, J. Rech. Atmos., 19, 139–145, 1985.
Sun, J. and Ariya, P.: Atmospheric organic and bio-aerosols as cloud condensation nuclei (CCN): A review, Atmos. Env., 40, 795–820, 2006.
Szyrmer, W. and Zawadski, I.: Biogenic and anthropogenic sources of ice-forming nuclei: A review, BAMS, 78, 209–228, 1997.
Vali, G.: Principles of ice nucleation, in: Biological Ice Nucleation and Its Applications, editied by: Lee Jr., R., Warren, G., and Gusta, L., APS Press, St. Paul, Minnesota, 1–28, 1995.
Vali, G.: Ice Nucleation a review, in: Nucleation and Atmospheric Aerosols, Proc. 14th Int. Conf. Nucleation and Atmospheric Aerosols, edited by: Kulmala, M. and Wagner, P., Elsevier Science, Ltd. Oxford, UK, 89–92, 1996.
Warren, G., Corotto, L., and Wolber, P.: Conserved repeats in diverged ice nucleation structural genes from two species of \textitPseudomonas, Nucleic Acids Res., 14, 8047–8060, 1986.
Wolber, P. and Warren, G.: Bacterial ice-nucleation proteins, Trends Biochem. Sci., 14, 179–182, 1989.
Yamamoto, S., Kasai, H., Arnold, D., Jackson, R., Vivian, A., and Harayama, S.: Phylogeny of the genus \textitPseudomonas: intrageneric structure reconstructed from the nucleotide sequences of \textitgyrB and \textitrpoD genes, Microbiology, 146, 2385–2394, 2000.