Skip to main content
SpringerLink
Log in

Clouds: A Transient and Stressing Habitat for Microorganisms

  • Chapter
  • First Online:
Microbial Ecology of Extreme Environments

Abstract

In this chapter, we synthesized the current knowledge about clouds as ecosystems which have been discovered very recently. First, we briefly described the cloud habitat. Cloud physics chemistry and microphysics are described, showing that this environment is extreme. Microorganisms are exposed to a dynamic medium changing extremely rapidly (evaporation/condensation of the cloud droplets, quick temperature and pressure changes, freeze/thaw cycle) and also to chemical stresses (strong oxidants, acidic pHs and toxics). Then the life cycle of microorganisms in the atmosphere is detailed showing that cloud is a transient habitat: microorganisms are aerosolized, transported in the air, integrated in cloud droplets and deposited back to the ground with precipitation. Finally the cloud microbiome is described; it appears that it remains largely unknown and based mainly on culture techniques. In the second part of the chapter, the abilities of these microorganisms to survive in this stressing environment are described in details. Microbes can adapt their metabolism as it was shown that the majority of the community is metabolically active and that they metabolize organic compounds in cloud water. They have also developed general strategies that help resisting to atmospheric constraints, such as the production of extracellular polymeric substances and pigments, or the formation of spores. Finally they can respond to specific stresses such as oxidative, osmotic and temperature stresses thanks to protecting metabolites such as osmo- and thermo-protectants, anti-oxidants or by using specific enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahern HE, Walsh KA, Hill TCJ, Moffett BF (2007) Fluorescent pseudomonads isolated from Hebridean cloud and rain water produce biosurfactants but do not cause ice nucleation. Biogeosciences 4(1):115–124

    Article  CAS  Google Scholar 

  • Aleksic N, Roy K, Sistla G, Dukett J, Houck N, Casson P (2009) Analysis of cloud and precipitation chemistry at whiteface mountain, NY. Atmos Environ 43(17):2709–2716. doi:10.1016/j.atmosenv.2009.02.053

    Article  CAS  Google Scholar 

  • Aller JY, Kuznetsova MR, Jahns CJ, Kemp PF (2005) The sea surface microlayer as a source of viral and bacterial enrichment in marine aerosols. J Aerosol Sci 36(5–6):801–812. doi:10.1016/j.jaerosci.2004.10.012

    Article  CAS  Google Scholar 

  • Amato P, Ménager M, Sancelme M, Laj P, Mailhot G, Delort A-M (2005) Microbial population in cloud water at the Puy de Dôme: implications for the chemistry of clouds. Atmos Environ 39(22):4143–4153

    Article  CAS  Google Scholar 

  • Amato P, Demeer F, Melaouhi A, Fontanella S, Martin-Biesse AS, Sancelme M, Laj P, Delort AM (2007a) A fate for organic acids, formaldehyde and methanol in cloud water: their biotransformation by micro-organisms. Atmos Chem Phys 7:4159–4169

    Article  CAS  Google Scholar 

  • Amato P, Hennebelle R, Magand O, Sancelme M, Delort AM, Barbante C, Boutron C, Ferrari C (2007b) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59(2):255–264

    Article  CAS  PubMed  Google Scholar 

  • Amato P, Parazols M, Sancelme M, Laj P, Mailhot G, Delort A-M (2007c) Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. FEMS Microbiol Ecol 59(2):242–254

    Article  CAS  PubMed  Google Scholar 

  • Amato P, Parazols M, Sancelme M, Mailhot G, Laj P, Delort AM (2007d) An important oceanic source of micro-organisms for cloud water at the Puy de Dôme (France). Atmos Environ 41(37):8253–8263

    Article  CAS  Google Scholar 

  • Amato P, Doyle S, Christner BC (2009) Macromolecular synthesis by yeasts under frozen conditions. Environ Microbiol 11(3):589–596. doi:10.1111/j.1462-2920.2008.01829.x

    Article  CAS  PubMed  Google Scholar 

  • Amato P, Joly M, Schaupp C, Attard E, Möhler O, Morris CE, Brunet Y, Delort A-M (2015) Survival and ice nucleation activity of bacteria as aerosols in a cloud simulation chamber. Atmos Chem Phys 15(11):6455–6465. doi:10.5194/acp-15-6455-2015

    Article  CAS  Google Scholar 

  • Anastasio C, Faust BC, Allen JM (1994) Aqueous phase photochemical formation of hydrogen peroxide in authentic cloud waters. J Geophys Res Atmos 99(D4):8231–8248. doi:10.1029/94JD00085

    Article  CAS  Google Scholar 

  • Ariya PA, Nepotchatykh O, Ignatova O, Amyot M (2002) Microbiological degradation of atmospheric organic compounds. Geophys Res Lett 29(22):2077–2081

    Article  CAS  Google Scholar 

  • Ariya PA, Sun J, Eltouny NA, Hudson ED, Hayes CT, Kos G (2009) Physical and chemical characterization of bioaerosols—implications for nucleation processes. Int Rev Phys Chem 28(1):1–32. doi:10.1080/01442350802597438

    Article  CAS  Google Scholar 

  • Bauer H, Kasper-Giebl A, Löflund M, Giebl H, Hitzenberger R, Zibuschka F, Puxbaum H (2002) The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmos Res 64(1–4):109–119

    Article  CAS  Google Scholar 

  • Bauer H, Schueller E, Weinke G, Berger A, Hitzenberger R, Marr IL, Puxbaum H (2008) Significant contributions of fungal spores to the organic carbon and to the aerosol mass balance of the urban atmospheric aerosol. Atmos Environ 42(22):5542–5549. doi:10.1016/j.atmosenv.2008.03.019

    Article  CAS  Google Scholar 

  • Bianco A, Passananti M, Perroux H, Voyard G, Mouchel-Vallon C, Chaumerliac N, Mailhot G, Deguillaume L, Brigante M (2015) A better understanding of hydroxyl radical photochemical sources in cloud waters collected at the Puy de Dôme station—experimental versus modelled formation rates. Atmos Chem Phys 15(16):9191–9202. doi:10.5194/acp-15-9191-2015

    Article  CAS  Google Scholar 

  • Blanchard DC (1989) The ejection of drops from the sea and their enrichment with bacteria and other materials: a review. Estuaries Coasts 12(3):127–137

    Article  CAS  Google Scholar 

  • Bottos EM, Woo AC, Zawar-Reza P, Pointing SB, Cary SC (2014) Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microb Ecol 67(1):120–128. doi:10.1007/s00248-013-0296-y

    Article  PubMed  Google Scholar 

  • Bowers RM, Lauber CL, Wiedinmyer C, Hamady M, Hallar AG, Fall R, Knight R, Fierer N (2009) Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Appl Environ Microbiol 75(15):5121–5130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodie EL, DeSantis TZ, Parker JPM, Zubietta IX, Piceno YM, Andersen GL (2007) Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci 104(1):299–304

    Article  CAS  PubMed  Google Scholar 

  • Burrows SM, Butler T, Jöckel P, Tost H, Kerkweg A, Pöschl U, Lawrence MG (2009a) Bacteria in the global atmosphere—part 2: modelling of emissions and transport between different ecosystems. Atmos Chem Phys 9(3):10829–10881

    Article  Google Scholar 

  • Burrows SM, Elbert W, Lawrence MG, Pöschl U (2009b) Bacteria in the global atmosphere—part 1: review and synthesis of literature data for different ecosystems. Atmos Chem Phys 9(3):10777–10827

    Article  Google Scholar 

  • Carpenter EJ, Lin S, Capone DG (2000) Bacterial activity in South Pole snow. Appl Environ Microbiol 66(10):4514–4517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol 3(9):570–577

    Article  CAS  PubMed  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5(5):433–436. doi:10.1046/j.1462-2920.2003.00422.x

    Article  CAS  PubMed  Google Scholar 

  • Christner BC, Morris CE, Foreman CM, Cai R, Sands DC (2008a) Ubiquity of biological ice nucleators in snowfall. Science 319(5867):1214

    Article  CAS  PubMed  Google Scholar 

  • Christner BC, Cai R, Morris CE, McCarter KS, Foreman CM, Skidmore ML, Montross SN, Sands DC (2008b) Geographic, seasonal, and precipitation chemistry influence on the abundance and activity of biological ice nucleators in rain and snow. Proc Natl Acad Sci 105(48):18854–18859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collett JL Jr, Aaron Bator D, Sherman E, Moore KF, Hoag KJ, Demoz BB, Rao X, Reilly JE (2002) The chemical composition of fogs and intercepted clouds in the United States. Atmos Res 64(1–4):29–40

    Article  CAS  Google Scholar 

  • Côté V, Kos G, Mortazavi R, Ariya PA (2008) Microbial and ‘de Novo’ transformation of dicarboxylic acids by three airborne fungi. Sci Total Environ 390(2–3):530–537

    Article  PubMed  CAS  Google Scholar 

  • Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64(4):847–67. doi:10.1128/MMBR.64.4.847-867.2000

  • Davies KJ (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50(4–5):279–289. doi:10.1080/713803728

    Article  CAS  PubMed  Google Scholar 

  • De Antoni GL, Pérez P, Abraham A, Añón MC (1989) Trehalose, a cryoprotectant for Lactobacillus bulgaricus. Cryobiology 26(2):149–153. doi:10.1016/0011-2240(89)90045-X

    Article  Google Scholar 

  • Decesari S, Facchini MC, Matta E, Lettini F, Mircea M, Fuzzi S, Tagliavini E, Putaud JP (2001) Chemical features and seasonal variation of fine aerosol water-soluble organic compounds in the Po Valley, Italy. Atmos Environ 35(21):3691–3699

    Article  CAS  Google Scholar 

  • Deguillaume L, Charbouillot T, Joly M, Vaïtilingom M, Parazols M, Marinoni A, Amato P et al (2014) Classification of clouds sampled at the Puy de Dôme (France) based on 10 Yr of monitoring of their physicochemical properties. Atmos Chem Phys 14(3):1485–1506. doi:10.5194/acp-14-1485-2014

    Article  CAS  Google Scholar 

  • DeLeon-Rodriguez N, Lathem TL, Rodriguez-R LM, Barazesh JM, Anderson BE, Beyersdorf AJ, Ziemba LD, Bergin M, Nenes A, Konstantinidis KT (2013) Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc Natl Acad Sci 110(7):2575–2580. doi:10.1073/pnas.1212089110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeMott PJ, Prenni AJ (2010) New directions: need for defining the numbers and sources of biological aerosols acting as ice nuclei. Atmos Environ 44(15):1944–1945

    Article  CAS  Google Scholar 

  • Després VR, Nowoisky JF, Klose M, Conrad R, Andreae MO, Pöschl U (2007) Characterization of primary biogenic aerosol particles in urban, rural, and high-alpine air by DNA sequence and restriction fragment analysis of ribosomal RNA genes. Biogeosciences 4(6):1127–1141

    Article  Google Scholar 

  • Deutsch F, Hoffmann P, Ortner HM (2001) Field experimental investigations on the Fe(II)- and Fe(III)-content in cloudwater samples. J Atmos Chem 40(1):87–105

    Article  CAS  Google Scholar 

  • Dieser M, Greenwood M, Foreman CM (2010) Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct Antarct Alp Res 42(4):396–405. doi:10.1657/1938-4246-42.4.396

    Article  Google Scholar 

  • Duman JG, Olsen TM (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30(3):322–328. doi:10.1006/cryo.1993.1031

    Article  Google Scholar 

  • Ekström S, Nozière B, Hultberg M, Alsberg T, Magnér J, Nilsson ED, Artaxo P (2010) A possible role of ground-based microorganisms on cloud formation in the atmosphere. Biogeosciences 7(1):387–394. doi:10.5194/bg-7-387-2010

    Article  Google Scholar 

  • Elbert W, Taylor PE, Andreae MO, Pöschl U (2007) Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions. Atmos Chem Phys 7(17):4569–4588

    Article  CAS  Google Scholar 

  • Erel Y, Pehkonen SO, Hoffmann MR (1993) Redox chemistry of iron in fog and stratus clouds. J Geophys Res 98(D10):18423–18434

    Article  CAS  Google Scholar 

  • Ervens B, George C, Williams JE, Buxton GV, Salmon GA, Bydder M, Wilkinson F et al (2003) CAPRAM 2.4 (MODAC mechanism): an extended and condensed tropospheric aqueous phase mechanism and its application. J Geophys Res 108(D14):4426. doi:10.1029/2002jd002202

    Article  CAS  Google Scholar 

  • Ervens B, Wang Y, Eagar J, Leaitch WR, Macdonald AM, Valsaraj KT, Herckes P (2013) Dissolved Organic Carbon (DOC) and select aldehydes in cloud and fog water: the role of the aqueous phase in impacting trace gas budgets. Atmos Chem Phys 13(10):5117–5135. doi:10.5194/acp-13-5117-2013

    Article  CAS  Google Scholar 

  • Ervens B, Renard P, Tlili S, Ravier S, Clément J-L, Monod A (2015) Aqueous-phase oligomerization of methyl vinyl ketone through photooxidation—part 2: development of the chemical mechanism and atmospheric implications. Atmos Chem Phys 15(16):9109–9127. doi:10.5194/acp-15-9109-2015

    Article  CAS  Google Scholar 

  • Fahlgren C, Hagström Å, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability, and origin of airborne bacteria. Appl Environ Microbiol 76(9):3015–3025. doi:10.1128/AEM.02092-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Liu Z, Rodriguez-Hernandez M, Knight R, Henn M, Hernandez MT (2008) Short-term temporal variability in airborne bacterial and fungal populations. Appl Environ Microbiol 74(1):200–207

    Article  CAS  PubMed  Google Scholar 

  • Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. doi:10.1038/nrmicro2415

    CAS  PubMed  Google Scholar 

  • Foght J, Aislabie J, Turner S, Brown CE, Ryburn J, Saul DJ, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two southern hemisphere glaciers. Microb Ecol 47(4):329–340

    Article  CAS  PubMed  Google Scholar 

  • Fong N, Burgess M, Barrow K, Glenn D (2001) carotenoid accumulation in the psychrotrophic bacterium ‘Arthrobacter Agilis’ in response to thermal and salt stress. Appl Microbiol Biotechnol 56(5–6):750–756. doi:10.1007/s002530100739

    Article  CAS  PubMed  Google Scholar 

  • Fröhlich-Nowoisky J, Pickersgill DA, Després VR, Pöschl U (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci 106(31):12814–12819. doi:10.1073/pnas.0811003106

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuzzi S, Mandrioli P, Perfetto A (1997) Fog droplets—an atmospheric source of secondary biological aerosol particles. Atmos Environ 31(2):287–290

    Article  CAS  Google Scholar 

  • Gabey AM, Vaitilingom M, Freney E, Boulon J, Sellegri K, Gallagher MW, Crawford IP, Robinson NH, Stanley WR, Kaye PH (2013) Observations of fluorescent and biological aerosol at a high-altitude site in Central France. Atmos Chem Phys 13(15):7415–7428. doi:10.5194/acp-13-7415-2013

    Article  CAS  Google Scholar 

  • Gandolfi I, Bertolini V, Ambrosini R, Bestetti G, Franzetti A (2013) Unravelling the bacterial diversity in the atmosphere. Appl Microbiol Biotechnol 97(11):4727–4736. doi:10.1007/s00253-013-4901-2

    Article  CAS  PubMed  Google Scholar 

  • Garcia E, Hill TCJ, Prenni AJ, DeMott PJ, Franc GD, Kreidenweis SM (2012) Biogenic ice nuclei in boundary layer air over two U.S. High Plains agricultural regions. J Geophys Res Atmos 117:D018209. doi:10.1029/2012JD018343

  • Gourmelon M, Cillard J, Pommepuy M (1994) Visible light damage to Escherichia Coli in seawater: oxidative stress hypothesis. J Appl Bacteriol 77(1):105–112

    Article  CAS  PubMed  Google Scholar 

  • Griffin DW (2007) Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 20(3):459–477. doi:10.1128/CMR.00039-06

    Article  PubMed  PubMed Central  Google Scholar 

  • Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H, Antranikian G (2004) Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic Sea Ice, Spitzbergen. Extremophiles Life Under Extreme Conditions 8(6):475–88. doi:10.1007/s00792-004-0409-0

  • Heald, CL, Spracklen DV (2009) Atmospheric budget of primary biological aerosol particles from fungal spores. Geophys Res Lett 36(9). doi:10.1029/2009GL037493

  • Healy DA, Huffman JA, O’Connor DJ, Pöhlker C, Pöschl U, Sodeau JR (2014) Ambient measurements of biological aerosol particles near Killarney, Ireland: a comparison between real-time fluorescence and microscopy techniques. Atmos Chem Phys 14(15):8055–8069. doi:10.5194/acp-14-8055-2014

    Article  CAS  Google Scholar 

  • Herckes P, Valsaraj KT, Collett JL Jr (2013) A review of observations of organic matter in fogs and clouds: origin, processing and fate. Atmos Res 132–133:434–449. doi:10.1016/j.atmosres.2013.06.005

  • Herlihy LJ, Galloway JN, Mills AL (1987) Bacterial utilization of formic and acetic acid in rainwater. Atmos Environ 21(11):2397–2402

    Article  CAS  Google Scholar 

  • Herrmann H, Schaefer T, Tilgner A, Styler SA, Weller C, Teich M, Otto T (2015) Tropospheric aqueous-phase chemistry: kinetics, mechanisms, and its coupling to a changing gas phase. Chem Rev 115(10):4259–4334. doi:10.1021/cr500447k

    Article  CAS  PubMed  Google Scholar 

  • Hill KA, Shepson PB, Galbavy ES, Anastasio C, Kourtev PS, Konopka A, Stirm BH (2007) Processing of atmospheric nitrogen by clouds above a forest environment. J Geophys Res Atmos 112(D11):D11301. doi:10.1029/2006JD008002

    Article  CAS  Google Scholar 

  • Hirano SS, Upper CD (2000) Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte. Microbiol Mol Biol Rev 64(3):624–653. doi:10.1128/MMBR.64.3.624-653.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoose C, Möhler O (2012) Heterogeneous ice nucleation on atmospheric aerosols: a review of results from laboratory experiments. Atmos Chem Phys 12:9817–9854

    Article  CAS  Google Scholar 

  • Hoose C, Kristjánsson JE, Burrows SM (2010) How important is biological ice nucleation in clouds on a global scale? Environ Res Lett 5(2):024009

    Article  CAS  Google Scholar 

  • Houdier S, Barret M, Dominé F, Charbouillot T, Deguillaume L, Voisin D (2011) Sensitive determination of glyoxal, methylglyoxal and hydroxyacetaldehyde in environmental water samples by using dansylacetamidooxyamine derivatization and liquid chromatography/fluorescence. Anal Chim Acta 704(1–2):162–173

    Google Scholar 

  • Husarova S, Vaitilingom M, Deguillaume L, Traikia M, Vinatier V, Sancelme M, Amato P, Matulova M, Delort A-M (2011) Biotransformation of methanol and formaldehyde by bacteria isolated from clouds. Comparison with radical chemistry. Atmos Environ 45(33):6093–6102. doi:10.1016/j.atmosenv.2011.06.035

    Article  CAS  Google Scholar 

  • Hutchings JW, Robinson MS, McIlwraith H, Kingston JT, Herckes P (2009) The chemistry of intercepted clouds in Northern Arizona during the North American Monsoon Season. Water Air Soil Pollut 199(1–4):191–202. doi:10.1007/s11270-008-9871-0

  • Igawa M, William Munger J, Hoffmann MR (1989) Analysis of aldehydes in cloud- and fogwater samples by HPLC with a postcolumn reaction detector. Environ Sci Technol 23(5):556–561

    Article  CAS  Google Scholar 

  • Imshenetsky AA, Lysenko SV, Kazakov GA (1978) Upper boundary of the biosphere. Appl Environ Microbiol 35(1):1–5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacob DJ, Waldman JM, William Munger J, Hoffmann MR (1984) A field investigation of physical and chemical mechanisms affecting pollutant concentrations in fog droplets. Tellus B 36B(4):272–285

    Article  CAS  Google Scholar 

  • Jeon EM, Kim HJ, Jung K, Kim JH, Kim MY, Kim YP, Ka J-O (2011) Impact of Asian dust events on airborne bacterial community assessed by molecular analyses. Atmos Environ 45(25):4313–4321. doi:10.1016/j.atmosenv.2010.11.054

    Article  CAS  Google Scholar 

  • Joly M, Attard E, Sancelme M, Deguillaume L, Guilbaud C, Morris CE, Amato P, Delort A-M (2013) Ice nucleation activity of bacteria isolated from cloud water. Atmos Environ 70:392–400

    Article  CAS  Google Scholar 

  • Joly M, Amato P, Deguillaume L, Monier M, Hoose C, Delort AM (2014) Quantification of ice nuclei active at near 0 °C temperatures in low-altitude clouds at the Puy de Dôme atmospheric station. Atmos Chem Phys 14(15):8185–8195. doi:10.5194/acp-14-8185-2014

    Article  CAS  Google Scholar 

  • Joly M, Amato P, Sancelme M, Vinatier V, Abrantes M, Deguillaume L, Delort A-M (2015) Survival of microbial isolates from clouds toward simulated atmospheric stress factors. Atmos Environ 117:92–98. doi:10.1016/j.atmosenv.2015.07.009 (September)

    Article  CAS  Google Scholar 

  • Jones AM, Harrison RM (2004) The effects of meteorological factors on atmospheric bioaerosol concentrations: a review. Sci Total Environ 326(1–3):151–180

    Article  CAS  PubMed  Google Scholar 

  • Jr C, Jeffrey L, Daube BC, Jr DG, Hoffmann MR (1990) Intensive studies of Sierra Nevada cloudwater chemistry and its relationship to precursor aerosol and gas concentrations. Atmos Environ Part A Gen Top 24(7):1741–1757

    Article  Google Scholar 

  • Junge K, Eicken H, Swanson BD, Deming JW (2006) Bacterial incorporation of leucine into protein down to −20 °C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology 52(3):417–429

    Article  CAS  PubMed  Google Scholar 

  • Kellogg CA, Griffin DW (2006) Aerobiology and the global transport of desert dust. Trends Ecol Evol 21(11):638–644

    Article  PubMed  Google Scholar 

  • Köhler H (1936) The nucleus in and the growth of hygroscopic droplets. Trans Faraday Soc 32:1152–1161. doi:10.1039/TF9363201152

    Article  Google Scholar 

  • Kourtev PS, Hill KA, Shepson PB, Konopka A (2011) Atmospheric cloud water contains a diverse bacterial community. Atmos Environ 45(30):5399–5405

    Article  CAS  Google Scholar 

  • Kurz M, Burch AY, Seip B, Lindow SE, Gross H (2010) Genome-driven investigation of compatible solute biosynthesis pathways of pseudomonas syringae pv. syringae and their contribution to water stress tolerance. Appl Environ Microbiol 76(16):5452–5462. doi:10.1128/AEM.00686-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeClair JP, Collett JL, Mazzoleni LR (2012) Fragmentation analysis of water-soluble atmospheric organic matter using ultrahigh-resolution FT-ICR mass spectrometry. Environ Sci Technol 46(8):4312–4322. doi:10.1021/es203509b

    Article  CAS  PubMed  Google Scholar 

  • Lighthart B (1997) The ecology of bacteria in the alfresco atmosphere. FEMS Microbiol Ecol 23(4):263–274

    Article  CAS  Google Scholar 

  • Lindemann J, Constantinidou HA, Barchet WR, Upper CD (1982) Plants as sources of airborne bacteria, including ice nucleation-active bacteria. Appl Environ Microbiol 44(5):1059–1063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lindow SE, Arny DC, Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. Appl Environ Microbiol 36(6):831–838

    CAS  PubMed  PubMed Central  Google Scholar 

  • Löflund M, Kasper-Giebl A, Schuster B, Giebl H, Hitzenberger R, Puxbaum H (2002) Formic, acetic, oxalic, malonic and succinic acid concentrations and their contribution to organic carbon in cloud water. Atmos Environ 36(9):1553–1558

    Article  Google Scholar 

  • Mader HM, Pettitt ME, Wadham JL, Wolff EW, John Parkes R (2006) Subsurface ice as a microbial habitat. Geology 34(3):169–172. doi:10.1130/G22096.1

    Article  CAS  Google Scholar 

  • Maki T, Susuki S, Kobayashi F, Kakikawa M, Tobo Y, Yamada M, Higashi T et al (2010) Phylogenetic analysis of atmospheric halotolerant bacterial communities at high altitude in an Asian Dust (KOSA) arrival region, Suzu City. Sci Total Environ 408(20):4556–4562. doi:10.1016/j.scitotenv.2010.04.002

    Article  CAS  PubMed  Google Scholar 

  • Maki T, Kakikawa M, Kobayashi F, Yamada M, Matsuki A, Hasegawa H, Iwasaka Y (2013) Assessment of composition and origin of airborne bacteria in the free troposphere over Japan. Atmos Environ 74:73–82. doi:10.1016/j.atmosenv.2013.03.029

    Article  CAS  Google Scholar 

  • Marinoni A, Laj P, Sellegri K, Mailhot G (2004) Cloud chemistry at the Puy de Dôme: variability and relationships with environmental factors. Atmos Chem Phys 4(3):715–728

    Article  CAS  Google Scholar 

  • Marinoni A, Parazols M, Brigante M, Deguillaume L, Amato P, Delort A-M, Laj P, Mailhot G (2011) Hydrogen peroxide in natural cloud water: sources and photoreactivity. Atmos Res (In Press), Corrected Proof. http://www.sciencedirect.com/science/article/B6V95-528YX2G-1/2/b7d2b89d5b5564997e0d6a96a1c84635

  • Marks R, Kruczalak K, Jankowska K, Michalska M (2001) Bacteria and fungi in air over the Gulf of Gdansk and Baltic sea. J Aerosol Sci 32(2):237–250

    Article  CAS  Google Scholar 

  • Maron P-A, Lejon David PH, Carvalho E, Bizet K, Lemanceau P, Ranjard L, Mougel C (2005) Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16S rDNA clone library. Atmos Environ 39(20):3687–3695. doi:10.1016/j.atmosenv.2005.03.002

    Article  CAS  Google Scholar 

  • Matsumoto K, Kawai S, Igawa M (2005) Dominant factors controlling concentrations of aldehydes in rain, fog, dew water, and in the gas phase. Atmos Environ 39(38):7321–7329. doi:10.1016/j.atmosenv.2005.09.009

    Article  CAS  Google Scholar 

  • Matulová M, Husárová S, Capek P, Sancelme M, Delort A-M (2014) Biotransformation of various saccharides and production of exopolymeric substances by cloud-borne Bacillus sp. 3B6. Environ Sci Technol 48(24):14238–14247. doi:10.1021/es501350s

    Article  PubMed  CAS  Google Scholar 

  • Mayol E, Jiménez MA, Herndl GJ, Duarte CM, Arrieta JM (2014) Resolving the abundance and air-sea fluxes of airborne microorganisms in the North Atlantic Ocean. Front Microbiol 5. doi:10.3389/fmicb.2014.00557

  • Mikami K, Kanesaki Yu, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46(4):905–915

    Article  CAS  PubMed  Google Scholar 

  • Möhler O, DeMott PJ, Vali G, Levin Z (2007) Microbiology and atmospheric processes: The role of biological particles in cloud physics. Biogeosciences 4(6):1059–1071

    Article  Google Scholar 

  • Monier J-M, Lindow SE (2003) Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc Natl Acad Sci 100(26):15977–15982. doi:10.1073/pnas.2436560100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris CE, Georgakopoulos DG, Sands DC (2004) Ice nucleation active bacteria and their potential role in precipitation. J Phys IV France 121:87–103

    Article  Google Scholar 

  • Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C, Buffière A, Yan S, Dominguez H, Thompson BM (2008) The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2(3):321–334

    Article  CAS  PubMed  Google Scholar 

  • Mueller DR, Vincent WF, Bonilla S, Laurion I (2005) Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic ice shelf ecosystem. FEMS Microbiol Ecol 53(1):73–87. doi:10.1016/j.femsec.2004.11.001

    Article  CAS  PubMed  Google Scholar 

  • Olszyna KJ, Meagher JF, Bailey EM (1988) Gas-phase, cloud and rain-water measurements of hydrogen peroxide at a high-elevation site. Atmos Environ (1967) 22(8):1699–1706

    Google Scholar 

  • Padan E, Bibi E, Ito M, Krulwich TA (2005) Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta (BBA) Biomembr 1717(2):67–88. doi:10.1016/j.bbamem.2005.09.010

  • Pan Y-L (2015) Detection and characterization of biological and other organic-carbon aerosol particles in atmosphere using fluorescence. J Quant Spectrosc Radiat Transfer Topical Issue Opt Part Charact Remote Sens Atmos Part I 150:12–35. doi:10.1016/j.jqsrt.2014.06.007 (January)

    CAS  Google Scholar 

  • Panoff J-M, Thammavongs B, Guéguen M (2000) Cryoprotectants lead to phenotypic adaptation to freeze–thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40(3):264–269. doi:10.1006/cryo.2000.2240

    Article  CAS  PubMed  Google Scholar 

  • Parazols M, Marinoni A, Amato P, Abida O, Laj P, Mailhot G, Delort A-M, Sergio Z (2007) Speciation and role of iron in cloud droplets at the Puy de Dôme Station. J Atmos Chem 57(3):299–300

    Article  CAS  Google Scholar 

  • Pehkonen SO, Erel Y, Hoffmann MR (1992) Simultaneous spectrophotometric measurement of iron(II) and iron(III) in atmospheric water. Environ Sci Technol 26(9):1731–1736

    Article  CAS  Google Scholar 

  • Poli A, Anzelmo G, Nicolaus B (2010) Bacterial exopolysaccharides from extreme marine habitats: production, characterization and biological activities. Mar Drugs 8(6):1779–1802. doi:10.3390/md8061779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price P Buford (2000) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci 97(3):1247–1251. doi:10.1073/pnas.97.3.1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prospero JM, Blades E, Mathison G, Naidu R (2005) Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21(1):1–19. doi:10.1007/s10453-004-5872-7

    Article  Google Scholar 

  • Pruppacher HR, Jaenicke R (1995) The processing of water vapor and aerosols by atmospheric clouds, a global estimate. Atmos Res 38(1–4):283–295

    Article  Google Scholar 

  • Renoux A, Boulaud D (1998) Les Aérosols: Physique et Métrologie. Lavoisier Technique & Documentation

    Google Scholar 

  • Richards LW (1995) Airborne chemical measurements in nighttime stratus clouds in the Los Angeles Basin. Atmos Environ 29(1):27–46

    Article  CAS  Google Scholar 

  • Šantl-Temkiv T, Finster K, Hansen BM, Nielsen NW, Karlson UG (2012) The microbial diversity of a storm cloud as assessed by hailstones. FEMS Microbiol Ecol 81(3):684–695. doi:10.1111/j.1574-6941.2012.01402.x

    Article  CAS  Google Scholar 

  • Šantl-Temkiv T, Finster K, Dittmar T, Hansen BM, Thyrhaug R, Nielsen NW, Karlson UG (2013a) Hailstones: a window into the microbial and chemical inventory of a storm cloud. PLoS ONE 8(1):e53550. doi:10.1371/journal.pone.0053550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Šantl-Temkiv T, Finster K, Hansen BM, Pašić L, Karlson UG (2013b) Viable methanotrophic bacteria enriched from air and rain can oxidize methane at cloud-like conditions. Aerobiologia 29(3):373–384. doi:10.1007/s10453-013-9287-1

    Article  Google Scholar 

  • Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophys Res Lett 28(2):239–242

    Article  Google Scholar 

  • Sauer F, Schuster G, Schäfer C, Moortgat GK (1996) Determination of H2O2 and organic peroxides in cloud and rain water on the Kleiner Feldberg during FELDEX. Geophys Res Lett 23(19):2605–2608

    Article  CAS  Google Scholar 

  • Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W (1995) Picrophilus Gen. Nov., Fam. Nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177(24):7050–7059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaji S, Prakash Jogadhenu S S (2010) How do bacteria sense and respond to low temperature? Arch Microbiol 192(2):85–95. doi:10.1007/s00203-009-0539-y

    Article  CAS  PubMed  Google Scholar 

  • Smith DJ, Griffin DW, McPeters RD, Ward PD, Schuerger AC (2011) Microbial survival in the stratosphere and implications for global dispersal. Aerobiologia 27(4):319–332. doi:10.1007/s10453-011-9203-5

    Article  Google Scholar 

  • Smith DJ, Timonen HJ, Jaffe DA, Griffin DW, Birmele MN, Perry KD, Ward PD, Roberts MS (2013) Intercontinental dispersal of bacteria and archaea by transpacific winds. Appl Environ Microbiol 79(4):1134–1139. doi:10.1128/AEM.03029-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stead D, Park SF (2000) Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter Coli to freeze-thaw stress. Appl Environ Microbiol 66(7):3110–3112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephanie, Waturangi DE (2011) Distribution of Ice Nucleation-Active (INA) bacteria from rain-water and air. HAYATI J Biosci 18(3):108–112

    Google Scholar 

  • Storz G, Tartaglia LA, Farr SB, Ames BN (1990) Bacterial defenses against oxidative stress. Trends Genet 6:363–368. doi:10.1016/0168-9525(90)90278-E

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Ariya PA (2006) Atmospheric organic and bio-aerosols as Cloud Condensation Nuclei (CCN): a review. Atmos Environ 40(5):795–820

    Article  CAS  Google Scholar 

  • Suzuki I, Kanesaki Yu, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40(1):235–244. doi:10.1046/j.1365-2958.2001.02379.x

    Article  CAS  PubMed  Google Scholar 

  • Tanghe A, Van Dijck P, Thevelein JM (2003) Determinants of freeze tolerance in microorganisms, physiological importance, and biotechnological applications. Adv Appl Microbiol 53:129–176

    Article  CAS  PubMed  Google Scholar 

  • Tanghe A, Van Dijck P, Thevelein JM (2006) Why do microorganisms have aquaporins? Trends Microbiol 14(2):78–85. doi:10.1016/j.tim.2005.12.001

    Article  PubMed  CAS  Google Scholar 

  • Tilgner A, Herrmann H (2010) Radical-driven carbonyl-to-acid conversion and acid degradation in tropospheric aqueous systems studied by CAPRAM. Atmos Environ 44:5415–5422. doi:10.1016/j.atmosenv.2010.07.050

    Article  CAS  Google Scholar 

  • Tong Y, Lighthart B (1998) Effect of simulated solar radiation on mixed outdoor atmospheric bacterial populations. FEMS Microbiol Ecol 26(4):311–316. doi:10.1111/j.1574-6941.1998.tb00515.x

    Article  CAS  Google Scholar 

  • Vaïtilingom M (2011) Rôle Des Microorganismes Des Nuages Dans La Chimie Atmosphérique. Comparaison Avec La Chimie Radicalaire. Blaise Pascal, Clermont-Ferrand, France. http://tel.archives-ouvertes.fr/tel-00783928

  • Vaïtilingom M, Amato P, Sancelme M, Laj P, Leriche M, Delort A-M (2010) Contribution of microbial activity to carbon chemistry in clouds. Appl Environ Microbiol 76(1):23–29

    Article  PubMed  CAS  Google Scholar 

  • Vaïtilingom M, Charbouillot T, Deguillaume L, Maisonobe R, Parazols M, Amato P, Sancelme M, Delort A-M (2011) Atmospheric chemistry of carboxylic acids: microbial implication versus photochemistry. Atmos Chem Phys 11:8721–8733

    Article  CAS  Google Scholar 

  • Vaïtilingom M, Attard E, Gaiani N, Sancelme M, Deguillaume L, Flossmann AI, Amato P, Delort A-M (2012) Long-term features of cloud microbiology at the Puy de Dôme (France). Atmos Environ 56:88–100. doi:10.1016/j.atmosenv.2012.03.072

    Article  CAS  Google Scholar 

  • Vaïtilingom M, Deguillaume L, Vinatier V, Sancelme M, Amato P, Chaumerliac N, Delort A-M (2013) Potential impact of microbial activity on the oxidant capacity and organic carbon budget in clouds. Proc Natl Acad Sci 110(2):559–564. doi:10.1073/pnas.1205743110

    Article  PubMed  Google Scholar 

  • Valverde-Canossa J, Wieprecht W, Acker K, Moortgat GK (2005) H2O2 and organic peroxide measurements in an orographic cloud: the FEBUKO experiment. Atmos Environ 39(23–24):4279–4290

    Article  CAS  Google Scholar 

  • van Pinxteren D, Plewka A, Hofmann D, Müller K, Kramberger H, Svrcina B, Bächmann K et al (2005) Schmücke hill cap cloud and valley stations aerosol characterisation during FEBUKO (II): organic compounds. Atmos Environ 39(23–24):4305–4320

    Article  CAS  Google Scholar 

  • Vorob’eva LI (2004) Stressors, stress reactions, and survival of bacteria: a review. Appl Biochem Microbiol 40(3):217–224. doi:10.1023/B:ABIM.0000025941.11643.19

  • Wang Y, Guo J, Wang T, Ding A, Gao J, Zhou Y, Collett JL Jr, Wang W (2011) Influence of regional pollution and sandstorms on the chemical composition of cloud/fog at the summit of Mt. Taishan in Northern China. Atmos Res 99(3–4):434–442. doi:10.1016/j.atmosres.2010.11.010

  • Wang Y, Chiu C-A, Westerhoff P, Valsaraj KT, Herckes P (2013) Characterization of atmospheric organic matter using size-exclusion chromatography with inline organic carbon detection. Atmos Environ 68:326–332. doi:10.1016/j.atmosenv.2012.11.049

    Article  CAS  Google Scholar 

  • Watanabe K, Ishizaka Y, Takenaka C (2001) Chemical characteristics of cloud water over the Japan Sea and the Northwestern Pacific Ocean near the central part of Japan: airborne measurements. Atmos Environ 35(4):645–655

    Article  CAS  Google Scholar 

  • Weller C, Tilgner A, Bräuer P, Herrmann H (2014) Modeling the impact of iron-carboxylate photochemistry on radical budget and carboxylate degradation in cloud droplets and particles. Environ Sci Technol 48(10):5652–5659. doi:10.1021/es4056643

    Article  CAS  PubMed  Google Scholar 

  • Witkin EM (1976) Ultraviolet mutagenesis and inducible DNA repair in Escherichia Coli. Bacteriol Rev 40(4):869–907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Womack AM, Bohannan Brendan J M, Green JL (2010) Biodiversity and biogeography of the atmosphere. Philos Trans R Soc B Biol Sci 365(1558):3645–3653. doi:10.1098/rstb.2010.0283

    Article  Google Scholar 

  • Zhang J, Li Y, Chen W, Guo-Cheng D, Chen J (2012) Glutathione improves the cold resistance of Lactobacillus Sanfranciscensis by physiological regulation. Food Microbiol 31(2):285–292. doi:10.1016/j.fm.2012.04.006

    Article  PubMed  CAS  Google Scholar 

  • Zweifel UL, Hagström Å, Holmfeldt K, Thyrhaug R, Geels C, Frohn LM, Skjøth CA, Karlson UG (2012) High bacterial 16S rRNA gene diversity above the atmospheric boundary layer. Aerobiologia 28(4):481–498. doi:10.1007/s10453-012-9250-6

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Chimie de Clermont-Ferrand, Unviersité Clermont-Auvergne, BP 10448, 63000, Clermont-Ferrand, France

    Anne Marie Delort, Muriel Joly, Pierre Amato, Nolwenn Wirgot, Audrey Lallement & Martine Sancelme

  2. Laboratoire de Météorologie Physique, Institut de Chimie de Clermont-Ferrand and Observatoire de Physique du Globe de Clermont-Ferrand, Université Clermont-Auvergne, BP 10448, 63000, Clermont-Ferrand, France

    Mickael Vaïtilingom

  3. Institute of Chemistry, Slovak Academy of Sciences, Bratislava, Slovakia

    Maria Matulova

  4. Laboratoire de Météorologie Physique, Observatoire de Physique du Globe de Clermont-Ferrand, Université Clermont-Auvergne, BP 10448, 63000, Clermont-Ferrand, France

    Laurent Deguillaume

Authors
  1. Anne Marie Delort
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mickael Vaïtilingom
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muriel Joly
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Amato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nolwenn Wirgot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Audrey Lallement
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Martine Sancelme
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Matulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Laurent Deguillaume
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne Marie Delort .

Editor information

Editors and Affiliations

  1. Singapore Center Envmtl. Life Sc. Engineer., Nanyang Technological Univ., Singapore, Singapore

    Caroline Chénard

  2. Singapore Center Envmtl. Life Sc. Engineer., Nanyang Technological Univ., Singapore, Singapore

    Federico M. Lauro

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Delort, A.M. et al. (2017). Clouds: A Transient and Stressing Habitat for Microorganisms. In: Chénard, C., Lauro, F. (eds) Microbial Ecology of Extreme Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-51686-8_10

Download citation

Publish with us

Policies and ethics

Search

Navigation