Abstract
Clarifying the role of precipitation in microbial dissemination is essential for elucidating the processes involved in disease emergence and spread. The ecology of Pseudomonas syringae and its presence throughout the water cycle makes it an excellent model to address this issue. In this study, 90 samples of freshly fallen rain and snow collected from 2005–2011 in France were analyzed for microbiological composition. The conditions favorable for dissemination of P. syringae by this precipitation were investigated by (i) estimating the physical properties and backward trajectories of the air masses associated with each precipitation event and by (ii) characterizing precipitation chemistry, and genetic and phenotypic structures of populations. A parallel study with the fungus Botrytis cinerea was also performed for comparison. Results showed that (i) the relationship of P. syringae to precipitation as a dissemination vector is not the same for snowfall and rainfall, whereas it is the same for B. cinerea and (ii) the occurrence of P. syringae in precipitation can be linked to electrical conductivity and pH of water, the trajectory of the air mass associated with the precipitation and certain physical conditions of the air mass (i.e. temperature, solar radiation exposure, distance traveled), whereas these predictions are different for B. cinerea. These results are pertinent to understanding microbial survival, emission sources and atmospheric processes and how they influence microbial dissemination.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Ajouz S, Nicot PC, Bardin M . (2010). Adaptation to pyrrolnitrin in Botrytis cinerea and cost of resistance. Plant Pathol 59: 556–566.
Amato P, Parazols M, Sancelme M, Laj P, Mailhot G, Delort AM . (2007). Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dome: major groups and growth abilities at low temperatures. FEMS Microbiol Ecol 59: 242–254.
Attard E, Yang H, Delort AM, Amato P, Poeschl U, Glaux C et al. (2012). Effects of atmospheric conditions on ice nucleation activity of Pseudomonas. Atmos Chem Phys 12: 10667–10677.
Aylor DE, Schmale DG, Shields EJ, Newcomb M, Nappo CJ . (2011). Tracking the potato late blight pathogen in the atmosphere using unmanned aerial vehicles and Lagrangian modeling. Agr Forest Meteorol 151: 251–260.
Burrows SM, Elbert W, Lawrence MG, Poschl U . (2009). Bacteria in the global atmosphere - Part 1: review and synthesis of literature data for different ecosystems. Atmos Chem Phys 9: 9263–9280.
Celle-Jeanton H, Travi Y, Loye-Pilot MD, Huneau F, Bertrand G . (2009). Rainwater chemistry at a Mediterranean inland station (Avignon, France): local contribution versus long-range supply. Atmos Res 91: 118–126.
Cunnac S, Lindeberg M, Collmer A . (2009). Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr Opin Microbiol 12: 53–60.
Davis JM . (1987). Modeling the long-range transport of plant pathogens in the atmosphere. Annu Rev Phytopathol 25: 169–188.
Decognet V, Bardin M, Trottin-Caudal Y, Nicot PC . (2009). Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99: 185–193.
Delmas V, Jones HG, Tranter M, Delmas R . (1996). The weathering of aeolian dusts in alpine snows. Atmos Environ 30: 1317–1325.
Delort A-M, Amato P, Sancelme M, Morris CE, Laj P . (2007). Isolation of ice-nucleation active microorganisms from cloud water. In: Earth: Our Changing Planet. Proceedings of the XXIV International Union of Geodesy and Geophysics (IUGG) General Assembly; 2–13 July 2007; Perugia (Italy).
Development Team (2011). Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project http://qgis.osgeo.org/.
Draxler RR, Hess GD . (1998). An overview of the HYSPLIT_4 modelling system for trajectories, dispersion and deposition. Aus Meteorol Mag 47: 295–308.
Draxler RR, Rolph GD . (2011) HYSPLIT (HYbrid Single-Particle Lagrangian Integrated Trajectory) Model access via NOAA ARL READY websitehttp://ready.arl.noaa.gov/HYSPLIT.phpNOAA Air Resources Laboratory: Silver Spring, MD, USA.
Edwards SG, Seddon B . (2001). Selective media for the specific isolation and enumeration of Botrytis cinerea conidia. Lett Appl Microbiol 32: 63–66.
Falush D, Stephens M, Pritchard JK . (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567–1587.
Fitt BDL, McCartney HA, Walklate PJ . (1989). The role of rain in dispersal of pathogen inoculum. Annu Rev Phytopathol 27: 241–270.
Flossmann AI, Hall WD, Pruppacher HR . (1985). A theoritical study of the wet removal of atmospheric pollutants. Part 1: The redistribution of aerosol particles captured through nucleation and impaction scavenging by growing cloud drops. J Atmos Sci 42: 583–606.
Gregory PH . (1961) The Microbiology of the Atmosphere. Interscience Publishers, Inc: New York, NY, USA.
Griffin DW, Kellogg CA, Garrison VH, Shinn EA . (2002). The global transport of dust - An intercontinental river of dust, microorganisms and toxic chemicals flows through the Earth's atmosphere. Am Sci 90: 228–235.
Guillot G, Estoup A, Mortier F, Cosson JF . (2005a). A spatial statistical model for landscape genetics. Genetics 170: 1261–1280.
Guillot G, Mortier F, Estoup A . (2005b). GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5: 712–715.
Guillot G, Renaud S, Ledevin R, Michaux J, Claude J . (2012). A unifying model for the analysis of phenotypic, genetic and geographic data. Syst Biol 61: 897–911.
Hara K, Zhang D . (2012). Bacterial abundance and viability in long-range transported dust. Atmos Environ 47: 20–25.
Harrison RM, Jones AM, Biggins PDE, Pomeroy N, Cox CS, Kidd SP et al. (2005). Climate factors influencing bacterial count in background air samples. Int J Biometeorol 49: 167–178.
Hirano SS, Baker LS, Upper CD . (1996). Raindrop momentum triggers growth of leaf-associated populations of Pseudomonas syringae on field-grown snap bean plants. Appl Env Microbiol 62: 2560–2566.
Holz G, Coertze S, Williamson B . (2004). The Ecology of Botrytis on Plant Surfaces. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds). Botrytis: Biology, Pathology and Control. Kluwer: Dordrecht, The Netherlands, pp 9–24.
Isard SA, Gage SH, Comtois P, Russo JM . (2005). Principles of the atmospheric pathway for invasive species applied to soybean rust. Bioscience 55: 851–861.
Joly M, Attard E, Sancelme M, Deguillaume L, Guilbaud C, Morris CE et al. (2013). Ice nucleation activity of bacteria isolated from cloud water. Atmos Environ 70: 392–400.
Kellogg CA, Griffin DW . (2006). Aerobiology and the global transport of desert dust. Trends Ecol Evol 21: 638–644.
King EO, Ward MK, Raney DE . (1954). Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301–307.
Krupa S, Bowersox V, Claybrooke R, Barnes CW, Szabo L, Harlin K et al. (2006). Introduction of Asian soybean rust urediniospores into the Midwestern United States - A case study. Plant Dis 90: 1254–1259.
Kunkeaw S, Tan S, Coaker G . (2010). Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol Plant Microbe Interact 23: 415–424.
Lee BK, Hong SH, Lee DS . (2000). Chemical composition of precipitation and wet deposition of major ions on the Korean peninsula. Atmos Environ 34: 563–575.
Leyronas C, Nicot PC . (2013). Monitoring viable airborne inoculum of Botrytis cinerea in the South-East of France over 3 years: relation with climatic parameters and the origin of air masses. Aerobiologia 29: 291–299.
Lighthart B . (1997). The ecology of bacteria in the alfresco atmosphere. FEMS Microbiol Ecol 23: 263–274.
Lighthart B . (1999). An hypothesis describing the general temporal and spatial distribution of alfresco bacteria in the earth’s atmospheric surface layer. Atmos Environ 33: 611–615.
Lindemann J, Constantinidou HA, Barchet WR, Upper CD . (1982). Plants as sources of airborne bacteria, including ice nucleation active bacteria. Appl Env Microbiol 44: 1059–1063.
Lindow SE . (1983). The role of bacterial ice nucleation in frost injury to plants. Annu Rev Phytopathol 21: 363–384.
Loye-Pilot MD, Morelli J . (1988). Fluctuations of ionic composition of precipitations collected in Corsica related to changes in the origins of incoming aerosols. J Aerosol Sci 19: 577–585.
Maki T, Susuki S, Kobayashi F, Kakikawa M, Yamada M, Higashi T et al. (2008). Phylogenetic diversity and vertical distribution of a halobacterial community in the atmosphere of an Asian dust (KOSA) source region, Dunhuang City. Air Qual Atmos Health 1: 81–89.
Manteau S, Abouna S, Lambert B, Legendre L . (2003). Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. FEMS Microbiol Ecol 43: 359–366.
Mazzaglia A, Studholme DJ, Taratufolo MC, Cai R, Almeida NF, Goodman T et al. (2012). Pseudomonas syringae pv. actinidiae (PSA) Isolates from Recent Bacterial Canker of Kiwifruit Outbreaks Belong to the Same Genetic Lineage. PLoS One 7: e36518.
Mircea M, Stefan S, Fuzzi S . (2000). Precipitation scavenging coefficient: influence of measured aerosol and raindrop size distributions. Atmos Environ 34: 5169–5174.
Mohan SK, Schaad NW . (1987). An improved agar plating assay for detecting Pseudomonas syringae pv. syringae and P. syringae pv. phaseolicola in contaminated bean seed. Phytopathology 77: 1390–1395.
Möhler O, Georgakopoulos DG, Morris CE, Benz S, Ebert V, Hunsmann S et al. (2008). Heterogeneous ice nucleation activity of bacteria: new laboratory experiments at simulated cloud conditions. Biogeosciences 5: 1425–1435.
Monier JM, Lindow SE . (2003). Pseudomonas syringae responds to the environment on leaves by cell size reduction. Phytopathology 93: 1209–1216.
Monteil CL, Guilbaud C, Glaux C, Lafolie F, Soubeyrand S, Morris CE . (2012). Emigration of the plant pathogen Pseudomonas syringae from leaf litter contributes to its population dynamics in alpine snowpack. Environ Microbiol 14: 2099–2112.
Morris CE, Conen F, Huffman JA, Phillips V, Pöschl U, Sands DC . (2014a). Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere. Glob Chang Biol 20: 341–351.
Morris CE, Leyronas C, Nicot PC . (2014b). Movement of bioaerosols in the atmosphere and the consequences for climate and microbial evolution. In: Colbeck I, Lazaridis M (eds) Aerosol Science: Technology and Applications. John Wiley & Sons, Ltd.: Chichester, UK, pp 393–416.
Morris CE, Sands DC, Vanneste JL, Montarry J, Oakley B, Guilbaud C et al. (2010). Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. mBio 1: 1–10.
Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C, Buffiere A et al. (2008). The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J. 2: 321–334.
Nagarajan S, Singh DV . (1990). Long-distance dispersion of rust pathogens. Annu Rev Phytopathol 28: 139–153.
Oki T, Kanae S . (2006). Global hydrological cycles and world water resources. Science 313: 1068–1072.
Ozsoy T, Saydam AC . (2000). Acidic and alkaline precipitation in the Cilician Basin, north-eastern Mediterranean Sea. Sci Total Environ 253: 93–109.
Pan Z, Yang XB, Pivonia S, Xue L, Pasken R, Roads J . (2006). Long-term prediction of soybean rust entry into the continental United States. Plant Dis 90: 840–846.
Pezet R, Pont V . (1990). Ultrastructural observations of pterostilbene fungotoxicity in dormant conidia of Botrytis cinerea Pers. J Phytopathol 129: 19–30.
Pfender W, Graw R, Bradley W, Carney M, Maxwell L . (2006). Use of a complex air pollution model to estimate dispersal and deposition of grass stem rust urediniospores at landscape scale. Agr Forest Meteorol 139: 138–153.
Pritchard JK, Stephens M, Donnelly P . (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
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: 1–19.
Pruppacher HR, Klett JD . (1997) Microphysics of Clouds and Precipitation. Kluwer Academic Publishers: Dordrecht, The Netherlands.
Purdy LH, Krupa SV, Dean JL . (1985). Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Dis 69: 689–693.
Riffaud CMH, Morris CE . (2002). Detection of Pseudomonas syringae pv. aptata in irrigation water retention basins by immunofluorescence colony-staining. Eur J Plant Pathol 108: 539–545.
Rodhe H, Grandell J . (1972). On the removal time of aerosol particles from the atmosphere by precipitation scavenging. Tellus 24: 442–454.
Rogers RR, Yau MK . (1989). A Short Course in Cloud Physics. Series in Nat Phil. Pergamon Press: Oxford, UK.
Sands DC, Langhans VE, Scharen AL, de Smet G . (1982). The association between bacteria and rain and possible resultant meteorogical implications. J Hungarian Meteorol Ser 86: 148–152.
Sands DC, Schroth MN, Hildebrand DC . (1970). Taxonomy of phytopathogenic pseudomonads. J Bacteriol 101: 9–23.
Sarkar SF, Guttman DS . (2004). Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Env Microbiol 70: 1999–2012.
Smith DJ, Timonen HJ, Jaffe DA, Griffin DW, Birmele MN, Perry KD et al. (2013). Intercontinental dispersal of bacteria and archaea by transpacific winds. Appl Env Microbiol 79: 1134–1139.
Tao Z, Malvick D, Claybrooke R, Floyd C, Bernacchi CJ, Spoden G et al. (2009). Predicting the risk of soybean rust in Minnesota based on an integrated atmospheric model. Int J Biometeorol 53: 509–521.
The R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria, ISBN: 3-900051-07-0.
Tong YY, Lighthart B . (2000). The annual bacterial particle concentration and size distribution in the ambient atmosphere in a rural area of the Willamette valley, Oregon. Aerosol Sci Tech 32: 393–403.
Wang H, Yang XB, Ma Z . (2010). Long-distance spore transport of wheat stripe rust pathogen from Sichuan, Yunnan, and Guizhou in Southwestern China. Plant Dis 94: 873–880.
Webber JF, Parkinson NM, Rose J, Stanford H, Cook RTA, Elphinstone JG . (2008). Isolation and identification of Pseudomonas syringae pv. aesculi causing bleeding canker of horse chestnut in the UK. Plant Pathol 57: 368.
Williamson B, Tudzynsk B, Tudzynski P, van Kan JAL . (2007). Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8: 561–580.
Wolber PK, Deininger CA, Southworth MW, Vandekerckhove J, Vanmontagu M, Warren GJ . (1986). Identification and purification of a bacterial ice nucleation protein. Proc Natl Acad Sci USA 83: 7256–7260.
Zhu M, Radcliffe EB, Ragsdale DW, MacRae IV, Seeley MW . (2006). Low-level jet streams associated with spring aphid migration and current season spread of potato viruses in the US northern Great Plains. Agr Forest Meteorol 138: 192–202.
Acknowledgements
We thank Daniel Granier and his team from the Super Sauze ski resort, for help with collection of samples. We are grateful to Odile Berge (INRA, Avignon) for her help in sampling and for enriching discussions, to Ghislain Géniaux and Michel Mourly (INRA, Avignon) for help with spatial analysis of the trajectories, and to Vaughan Phillips for his insights in cloud physics. We gratefully acknowledge Claire Troulet for excellent technical assistance for the Botrytis cinerea experiments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Monteil, C., Bardin, M. & Morris, C. Features of air masses associated with the deposition of Pseudomonas syringae and Botrytis cinerea by rain and snowfall. ISME J 8, 2290–2304 (2014). https://doi.org/10.1038/ismej.2014.55
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2014.55
Keywords
This article is cited by
-
A Recipe for Success: Three Key Strategies Used by Aphids and Pseudomonas syringae to Colonize the Phyllosphere
Microbial Ecology (2023)
-
Properties relevant to atmospheric dispersal of the ice-nucleation active Pseudomonas syringae strain R10.79 isolated from rain water
Aerobiologia (2021)
-
A comparative evaluation of freezing criteria and molecular characterization of epiphytic ice-nucleating (Ice+) and non-ice-nucleating (Ice−) Pseudomonas syringae and Pseudomonas fluorescens
Journal of Plant Pathology (2020)
-
The overlapping continuum of host range among strains in the Pseudomonas syringae complex
Phytopathology Research (2019)
-
Legal immigrants: invasion of alien microbial communities during winter occurring desert dust storms
Microbiome (2017)
