Bacterial composition and survival on Sahara dust particles transported to the European Alps

Frontiers in Microbiology

Volumn 6, Issue DEC, 2015, Pages

  Meola, Marco ^a   Lazzaro, Anna ^a   Zeyer, Josef ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Bioaerosols; Biolog; Desiccation stress; Jungfraujoch; MiSeq Illumina; Saharan dust event; Snow; UV radiation

Indexed keywords

ALPS; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; CONTROLLED STUDY; DUST; ECOPHYSIOLOGY; EUROPE; GEOGRAPHIC AND GEOLOGICAL PHENOMENA; HIGH THROUGHPUT SEQUENCING; METEOROLOGY; MICROBIAL COMMUNITY; NONHUMAN; PHYSICAL CHEMISTRY; REAL TIME POLYMERASE CHAIN REACTION; ROENTGEN SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; SNOW COVER;

EID: 84954568239     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01454     Document Type: Article

References (105)

1. Amato, P., Joly, M., Schaupp, C., Attard, E., Möhler, O., Morris, C. E., et al. (2015). Survival and ice nucleation activity of bacteria as aerosols in a cloud simulation chamber. Atmos. Chem. Phys. 15, 6455-6465. doi: 10.5194/acp-15-6455-2015
2. Amato, P., Menager, M., Sancelme, M., Laj, P., Mailhot, G., and Delort, A. M. (2005). Microbial population in cloud water at the Puy de Dome: implications for the chemistry of clouds. Atmos. Environ. 39, 4143-4153. doi: 10.1016/j.atmosenv.2005.04.002
3. Amato, P., Parazols, M., Sancelme, M., Laj, P., Mailhot, G., and Delort, A. M. (2007a). 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. doi: 10.1111/j.1574-6941.2006.00199.x
4. Amato, P., Parazols, M., Sancelme, M., Mailhot, G., Laj, P., and Delort, A.-M. (2007b). An important oceanic source of micro-organisms for cloud water at the Puy de Dôme (France). Atmos. Environ. 41, 8253-8263. doi: 10.1016/j.atmosenv.2007.06.022
5. Anderson, M. J., Crist, T. O., Chase, J. M., Vellend, M., Inouye, B. D., Freestone, A. L., et al. (2011). Navigating the multiple meanings of beta diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19-28. doi: 10.1111/j.1461-0248.2010.01552.x
6. Bajerski, F., and Wagner, D. (2013). Bacterial succession in Antarctic soils of two glacier forefields on Larsemann Hills, East Antarctica. FEMS Microbiol. Ecol. 85, 128-142. doi: 10.1111/1574-6941.12105
7. Barberán, A., Henley, J., Fierer, N., and Casamayor, E. O. (2014). Structure, inter-annual recurrence, and global-scale connectivity of airborne microbial communities. Sci. Total Environ. 487, 187-195. doi: 10.1016/j.scitotenv.2014.04.030
8. Barton, A. D., Dutkiewicz, S., Flierl, G., Bragg, J., and Follows, M. J. (2010). Patterns of diversity in marine phytoplankton. Science 327, 1509-1511. doi: 10.1126/science.1184961
9. Be, N. A., Thissen, J. B., Fofanov, V. Y., Allen, J. E., Rojas, M., Golovko, G., et al. (2015). Metagenomic analysis of the airborne environment in urban spaces. Microb. Ecol. 69, 346-355. doi: 10.1007/s00248-014-0517-z
10. Behzad, H., Gojobori, T., and Mineta, K. (2015). Challenges and opportunities of airborne metagenomics. Genome Biol. Evol. 7, 1216-1226. doi: 10.1093/gbe/evv064
11. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Methodol. 57, 289-300.
12. Blankinship, J. C., Becerra, C. A., Schaeffer, S. M., and Schimel, J. P. (2014). Separating cellular metabolism from exoenzyme activity in soil organic matter decomposition. Soil Biol. Biochem. 71, 68-75. doi: 10.1016/j.soilbio.2014.01.010
13. Bowers, R. M., Lauber, C. L., Wiedinmyer, C., Hamady, M., Hallar, A. G., Fall, R., et al. (2009). Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Appl. Environ. Microbiol. 75, 5121-5130. doi: 10.1128/AEM.00447-09
14. Brucker, R. M., Harris, R. N., Schwantes, C. R., Gallaher, T. N., Flaherty, D. C., Lam, B. A., et al. (2008). Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 34, 1422-1429. doi: 10.1007/s10886-008-9555-7
15. Callegan, R. P., Nobre, M. F., McTernan, P. M., Battista, J. R., Navarro-González, R., McKay, C. P., et al. (2008). Description of four novel psychrophilic, ionizing radiation-sensitive Deinococcus species from alpine environments. Int. J. Syst. Evol. Microbiol. 58, 1252-1258. doi: 10.1099/ijs.0.65405-0
16. Caporaso, J. G., Bittinger, K., Bushman, F. D., Desantis, T. Z., Andersen, G. L., and Knight, R. (2010). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267. doi: 10.1093/bioinformatics/btp636
17. Caquineau, S., Gaudichet, A., Gomes, L., and Legrand, M. (2002). Mineralogy of Saharan dust transported over northwestern tropical Atlantic Ocean in relation to source regions. J. Geophys. Res. Atmos. 107:4251. doi: 10.1029/2000jd000247
18. Chanal, A., Chapon, V., Benzerara, K., Barakat, M., Christen, R., Achouak, W., et al. (2006). The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ. Microbiol. 8, 514-525. doi: 10.1111/j.1462-2920.2005.00921.x
19. Chappell, A., Warren, A., O'Donoghue, A., Robinson, A., Thomas, A., and Bristow, C. (2008). The implications for dust emission modeling of spatial and vertical variations in horizontal dust flux and particle size in the Bodele Depression, Northern Chad. J. Geophys. Res. Atmos. 113:D04214. doi: 10.1029/2007JD009032
20. Chuvochina, M. S., Alekhina, I. A., Normand, P., Petit, J. R., and Bulat, S. A. (2011a). Three events of Saharan dust deposition on the Mont Blanc glacier associated with different snow-colonizing bacterial phylotypes. Microbiology 80, 125-131. doi: 10.1134/S0026261711010061
21. Chuvochina, M. S., Marie, D., Chevaillier, S., Petit, J.-R., Normand, P., Alekhina, I. A., et al. (2011b). Community variability of bacteria in alpine snow (mont blanc) containing saharan dust deposition and their snow colonisation potential. Microb. Environ. 26, 237-247. doi: 10.1264/jsme2.ME11116
22. Claquin, T., Schulz, M., and Balkanski, Y. J. (1999). Modeling the mineralogy of atmospheric dust sources. J. Geophys. Res. 104, 22243. doi: 10.1029/1999JD900416
23. Collaud Coen, M., Weingartner, E., Schaub, D., Hueglin, C., Corrigan, C., Henning, S., et al. (2004). Saharan dust events at the Jungfraujoch: detection by wavelength dependence of the single scattering albedo and first climatology analysis. Atmos. Chem. Phys. 4, 2465-2480. doi: 10.5194/acp-4-2465-2004
24. Conen, F., Rodríguez, S., Hüglin, C., Henne, S., Herrmann, E., Bukowiecki, N., et al. (2015). Atmospheric ice nuclei at the high-altitude observatory Jungfraujoch, Switzerland. Tellus B 67:25014. doi: 10.3402/tellusb.v67.25014
25. Crits-Christoph, A., Robinson, C. K., Barnum, T., Fricke, W. F., Davila, A. F., Jedynak, B., et al. (2013). Colonization patterns of soil microbial communities in the Atacama Desert. Microbiome 1, 28. doi: 10.1186/2049-2618-1-28
26. D'Almeida, G. A. (1986). A model for saharan dust transport. J. Appl. Meteorol. Climatol. 25, 903-916.
27. Darwin, C. (1846). An account of the fine dust which often falls on vessels in the Atlantic Ocean. Q. J. Geol. Soc. Lond. 2, 26-30. doi: 10.1144/GSL.JGS.1846.002.01-02.09
28. Debruyn, J. M., Nixon, L. T., Fawaz, M. N., Johnson, A. M., and Radosevich, M. (2011). Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl. Environ. Microbiol. 77, 6295-6300. doi: 10.1128/AEM.05005-11
29. De Deckker, P., Munday, C. I., Brocks, J., O'Loingsigh, T., Allison, G. E., Hope, J., et al. (2014). Characterisation of the major dust storm that traversed over eastern Australia in September 2009; a multidisciplinary approach. Aeolian Res. 15, 133-149. doi: 10.1016/j.aeolia.2014.07.003
30. De Groot, A., Chapon, V., Servant, P., Christen, R., Saux, M. F., Sommer, S., et al. (2005). Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int. J. Syst. Evol. Microbiol. 55, 2441-2446. doi: 10.1099/ijs.0.63717-0
31. Deleon-Rodriguez, N., Lathem, T. L., Rodriguez, R. L., Barazesh, J. M., Anderson, B. E., Beyersdorf, A. J., et al. (2013). Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc. Natl. Acad. Sci. U.S.A. 110, 2575-2580. doi: 10.1073/pnas.1212089110
32. Després, V. R., Huffman, J. A., Burrows, S. M., Hoose, C., Safatov, A. S., Buryak, G., et al. (2012). Primary biological aerosol particles in the atmosphere: a review. Tellus B Chem. Phys. Meteorol. 64:15598. doi: 10.3402/tellusb.v64i0.15598
33. Dimmick, R. L., Straat, P. A., Wolochow, H., Levin, G. V., Chatigny, M. A., and Schrot, J. R. (1975). Evidence for metabolic activity of airborne bacteria. J. Aerosol Sci. 6, 387-393. doi: 10.1016/0021-8502(75)90054-3
34. Draxler, R. R., and Rolph, G. D. (2003). HYSPLIT (Hybrid Single-Particle Lagrangian Integrated Trajectory) Model, NOAA Air Resources Laboratory. Silver Spring, MD. Available online at: http://www.arl.noaa.gov/ready/hysplit4.html
35. Drees, K. P., Neilson, J. W., Betancourt, J. L., Quade, J., Henderson, D. A., Pryor, B. M., et al. (2006). Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl. Environ. Microbiol. 72, 7902-7908. doi: 10.1128/AEM.01305-06
36. Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996-998. doi: 10.1038/nmeth.2604
37. Elbert, W., Taylor, P. E., Andreae, M. O., and Poschl, 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, 4569-4588. doi: 10.5194/acp-7-4569-2007
38. Evans, R. D., Jefferson, I. F., Kumar, R., O'Hara-Dhand, K., and Smalley, I. J. (2004). The nature and early history of airborne dust from North Africa; in particular the Lake Chad basin. J. Afr. Earth Sci. 39, 81-87. doi: 10.1016/j.jafrearsci.2004.06.001
39. Fahlgren, C., Hagström, A., Nilsson, D., and Zweifel, U. L. (2010). Annual variations in the diversity, viability, and origin of airborne bacteria. Appl. Environ. Microbiol. 76, 3015-3025. doi: 10.1128/AEM.02092-09
40. Favet, J., Lapanje, A., Giongo, A., Kennedy, S., Aung, Y. Y., Cattaneo, A., et al. (2013). Microbial hitchhikers on intercontinental dust: catching a lift in Chad. ISME J. 7, 850-867. doi: 10.1038/ismej.2012.152
41. Fierer, N., Leff, J. W., Adams, B. J., Nielsen, U. N., Bates, S. T., Lauber, C. L., et al. (2012). Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl. Acad. Sci. U.S.A. 109, 21390-21395. doi: 10.1073/pnas.1215210110
42. Flentje, H., Briel, B., Beck, C., Collaud Coen, M., Fricke, M., Cyrys, J., et al. (2015). Identification and monitoring of Saharan dust: an inventory representative for south Germany since 1997. Atmos. Environ. 109, 87-96. doi: 10.1016/j.atmosenv.2015.02.023
43. Frey, B., Rieder, S. R., Brunner, I., Plötze, M., Koetzsch, S., Lapanje, A., et al. (2010). Weathering-associated bacteria from the Damma glacier forefield: physiological capabilities and impact on granite dissolution. Appl. Environ. Microbiol. 76, 4788-4796. doi: 10.1128/AEM.00657-10
44. González-Toril, E., Amils, R., Delmas, R. J., Petit, J.-R., Komárek, J., and Elster, J. (2009). Bacterial diversity of autotrophic enriched cultures from remote, glacial Antarctic, Alpine and Andean aerosol, snow and soil samples. Biogeosciences 6, 33-44. doi: 10.5194/bg-6-33-2009
45. Goodison, B. E., Ferguson, H. L., and McKay, G. A. (1981). "Measurement and data analysis, " in Handbook of Snow: Principles, Processes, Management and Use, eds D. M. Gray and D. H. Male (Caldwell, NJ: The Blackburn Press), 191-274.
46. Gorbushina, A. A., Kort, R., Schulte, A., Lazarus, D., Schnetger, B., Brumsack, H. J., et al. (2007). Life in Darwin's dust: intercontinental transport and survival of microbes in the nineteenth century. Environ. Microbiol. 9, 2911-2922. doi: 10.1111/j.1462-2920.2007.01461.x
47. Goudie, A., and Middleton, N. (2006). Desert Dust in the Global System. Berlin; New York, NY: Springer.
48. Griffin, D., Kellogg, C., Garrison, V., Lisle, J., Borden, T., and Shinn, E. (2003). Atmospheric microbiology in the northern Caribbean during African dust events. Aerobiologia 19, 143-157. doi: 10.1023/B:AERO.0000006530.32845.8d
49. Griffin, D. W. (2007). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin. Microbiol. Rev. 20, 459-477, table of contents. doi: 10.1128/cmr.00039-06
50. Griffin, D. W., Kubilay, N., Kocak, M., Gray, M. A., Borden, T. C., and Shinn, E. A. (2007). Airborne desert dust and aeromicrobiology over the Turkish Mediterranean coastline. Atmos. Environ. 41, 4050-4062. doi: 10.1016/j.atmosenv.2007.01.023
51. Griffiths, A. D., Conen, F., Weingartner, E., Zimmermann, L., Chambers, S. D., Williams, A. G., et al. (2014). Surface-to-mountaintop transport characterised by radon observations at the Jungfraujoch. Atmos. Chem. Phys. 14, 12763-12779. doi: 10.5194/acp-14-12763-2014
52. Hanada, S., and Sekiguchi, Y. (2014). "The phylum gemmatimonadetes, " in The Prokaryotes, eds E. Rosenberg, E. Delong, S. Lory, E. Stackebrandt, and F. Thompson (Berlin; Heidelberg: Springer), 677-681.
53. Herlemann, D. P., Labrenz, M., Jürgens, K., Bertilsson, S., Waniek, J. J., and Andersson, A. F. (2011). Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5, 1571-1579. doi: 10.1038/ismej.2011.41
54. Hervas, A., Camarero, L., Reche, I., and Casamayor, E. O. (2009). Viability and potential for immigration of airborne bacteria from Africa that reach high mountain lakes in Europe. Environ. Microbiol. 11, 1612-1623. doi: 10.1111/j.1462-2920.2009.01926.x
55. Hervas, A., and Casamayor, E. O. (2009). High similarity between bacterioneuston and airborne bacterial community compositions in a high mountain lake area. FEMS Microbiol. Ecol. 67, 219-228. doi: 10.1111/j.1574-6941.2008.00617.x
56. Hill, K. A., Shepson, P. B., Galbavy, E. S., Anastasio, C., Kourtev, P. S., Konopka, A., et al. (2007). Processing of atmospheric nitrogen by clouds above a forest environment. J. Geophys. Res. 112:D11301. doi: 10.1029/2006jd008002
57. Hiranuma, N., Möhler, O., Yamashita, K., Tajiri, T., Saito, A., Kiselev, A., et al. (2015). Ice nucleation by cellulose and its potential contribution to ice formation in clouds. Nat. Geosci. 8, 273-277. doi: 10.1038/ngeo2374
58. Hirsch, P., Gallikowski, C. A., Siebert, J., Peissl, K., Kroppenstedt, R., Schumann, P., et al. (2004). Deinococcus frigens sp. nov., Deinococcus saxicola sp. nov., and Deinococcus marmoris sp. nov., low temperature and draught-tolerating, UV-resistant bacteria from continental Antarctica. Syst. Appl. Microbiol. 27, 636-645. doi: 10.1078/0723202042370008
59. Jaenicke, R. (2005). Abundance of cellular material and proteins in the atmosphere. Science 308, 73. doi: 10.1126/science.1106335
60. Jeon, E. M., Kim, H. J., Jung, K., Kim, J. H., Kim, M. Y., Kim, Y. P., et al. (2011). Impact of Asian dust events on airborne bacterial community assessed by molecular analyses. Atmos. Environ. 45, 4313-4321. doi: 10.1016/j.atmosenv.2010.11.054
61. Katra, I., Arotsker, L., Krasnov, H., Zaritsky, A., Kushmaro, A., and Ben-Dov, E. (2014). Richness and diversity in dust stormborne biomes at the southeast mediterranean. Sci. Rep. 4, 5265. doi: 10.1038/srep05265
62. Kim, S. J., Shin, S. C., Hong, S. G., Lee, Y. M., Lee, H., Lee, J., et al. (2012). Genome sequence of Janthinobacterium sp. strain PAMC 25724, isolated from alpine glacier cryoconite. J. Bacteriol. 194, 2096. doi: 10.1128/JB.00096-12
63. Kindt, R., and Coe, R. (2005). Tree Diversity Analysis: A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies. Nairobi: World Agrofirestry Centre.
64. Krueger, B. J., Grassian, V. H., Cowin, J. P., and Laskin, A. (2004). Heterogeneous chemistry of individual mineral dust particles from different dust source regions: the importance of particle mineralogy. Atmos. Environ. 38, 6253-6261. doi: 10.1016/j.atmosenv.2004.07.010
65. Kulkarni, P., Baron, P. A., and Willeke, K. (eds.). (2011). "Introduction to aerosol characterization, " in Aerosol Measurement: Principles, Techniques, and Applications, 3rd Edition (Hoboken, NJ: John Wiley & Sons, Inc.). doi: 10.1002/9781118001684.ch1
66. Labhart, T. P. (2001). Geologie der Schweiz. Thun: Ott.
67. Lazzaro, A., Wismer, A., Schneebeli, M., Erny, I., and Zeyer, J. (2015). Microbial abundance and community structure in a melting alpine snowpack. Extremophiles 19, 631-642. doi: 10.1007/s00792-015-0744-3
68. Legendre, P., and Anderson, M. J. (1999). Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments Ecol. Monogr. 69, 512-512. doi: 10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
69. Letunic, I., and Bork, P. (2011). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475-W478. doi: 10.1093/nar/gkr201
70. Liu, Y., Yao, T., Jiao, N., Kang, S., Zeng, Y., and Liu, X. (2009). Abundance and diversity of snow bacteria in two glaciers at the Tibetan Plateau. Front. Earth Sci. China 3, 80-90. doi: 10.1007/s11707-009-0016-6
71. Mandal, J., and Brandl, H. (2011). Bioaerosols in indoor environment-a review with special reference to residential and occupational locations. Open Environ. Biol. Monit. J. 4, 83-96. doi: 10.2174/1875040001104010083
72. McMurdie, P. J., and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. doi: 10.1371/journal.pone.0061217
73. Möhler, O., Demott, P. J., Vali, G., and Levin, Z. (2007). Microbiology and atmospheric processes: the role of biological particles in cloud physics. Biogeosciences 4, 1059-1071. doi: 10.5194/bg-4-1059-2007
74. Moreno, T. (2003). The geology of ambient aerosols: characterising urban and rural/coastal silicate PM10-2.5 and PM2.5 using high-volume cascade collection and scanning electron microscopy. Atmos. Environ. 37, 4265-4276. doi: 10.1016/S1352-2310(03)00534-X
75. Moreno, T., Querol, X., Castillo, S., Alastuey, A., Cuevas, E., Herrmann, L., et al. (2006). Geochemical variations in aeolian mineral particles from the Sahara-Sahel Dust Corridor. Chemosphere 65, 261-270. doi: 10.1016/j.chemosphere.2006.02.052
76. Morris, C. E., Sands, D. C., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., et al. (2011). Microbiology and atmospheric processes: research challenges concerning the impact of airborne micro-organisms on the atmosphere and climate. Biogeosciences 8, 17-25. doi: 10.5194/bg-8-17-2011
77. Nicolás, J. F., Crespo, J., Yubero, E., Soler, R., Carratalá, A., and Mantilla, E. (2014). Impacts on particles and ozone by transport processes recorded at urban and high-altitude monitoring stations. Sci. Total Environ. 466-467, 439-446. doi: 10.1016/j.scitotenv.2013.07.060
78. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R., et al. (2015). vegan: Community Ecology Package. R package version 2.3-2. Available online at: http://CRAN.R-project.org/package=vegan
79. Pantanella, F., Berlutti, F., Passariello, C., Sarli, S., Morea, C., and Schippa, S. (2007). Violacein and biofilm production in Janthinobacterium lividum. J. Appl. Microbiol. 102, 992-999. doi: 10.1111/j.1365-2672.2006.03155.x
80. Papayannis, A., Amiridis, V., Mona, L., Tsaknakis, G., Balis, D., Bösenberg, J., et al. (2008). Systematic lidar observations of Saharan dust over Europe in the frame of EARLINET (2000-2002). J. Geophys. Res. 113:D10204. doi: 10.1029/2007jd009028
81. Peter, H., Hörtnagl, P., Reche, I., and Sommaruga, R. (2014). Bacterial diversity and composition during rain events with and without Saharan dust influence reaching a high mountain lake in the Alps. Environ. Microbiol. Rep. 6, 618-624. doi: 10.1111/1758-2229.12175
82. Pointing, S. B., and Belnap, J. (2012). Microbial colonization and controls in dryland systems. Nat. Rev. Microbiol. 10, 551-562. doi: 10.1038/nrmicro2831
83. Pointing, S. B., Chan, Y., Lacap, D. C., Lau, M. C. Y., Jurgens, J. A., and Farrell, R. L. (2010). Highly specialized microbial diversity in hyper-arid polar desert (vol 106, pg 19964, 2009). Proc. Natl. Acad. Sci. U.S.A. 107, 1254-1254. doi: 10.1073/pnas.0913882107
84. Polymenakou, P. N. (2012). Atmosphere: a source of pathogenic or beneficial microbes? Atmosphere 3, 87-102. doi: 10.3390/atmos3010087
85. Polymenakou, P. N., Mandalakis, M., Stephanou, E. G., and Tselepides, A. (2008). Particle size distribution of airborne microorganisms and pathogens during an Intense African dust event in the eastern Mediterranean. Environ. Health Perspect. 116, 292-296. doi: 10.1289/ehp.10684
86. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490
87. Prospero, J. M., Blades, E., Mathison, G., and Naidu, R. (2005). Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21, 1-19. doi: 10.1007/s10453-004-5872-7
88. Rainey, F. A., Ray, K., Ferreira, M., Gatz, B. Z., Nobre, M. F., Bagaley, D., et al. (2005). Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran Desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl. Environ. Microbiol. 71, 5225-5235. doi: 10.1128/AEM.71.9.5225-5235.2005
89. R Core Team (2015). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: http://www.R-project.org/
90. Rime, T., Hartmann, M., Brunner, I., Widmer, F., Zeyer, J., and Frey, B. (2015). Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol. Ecol. 24, 1091-1108. doi: 10.1111/mec.13051
91. Romero, O. E., Lange, C. B., Swap, R., and Wefer, G. (1999). Eolian-transported freshwater diatoms and phytoliths across the equatorial Atlantic record: temporal changes in Saharan dust transport patterns. J. Geophys. Res. 104, 3211. doi: 10.1029/1998JC900070
92. Sánchez De La Campa, A., García-Salamanca, A., Solano, J., De La Rosa, J., and Ramos, J. L. (2013). Chemical and microbiological characterization of atmospheric particulate matter during an intense African dust event in Southern Spain. Environ. Sci. Technol. 47, 3630-3638. doi: 10.1021/es3051235
93. Šantl-Temkiv, T., Finster, K., Dittmar, T., Hansen, B. M., Thyrhaug, R., Nielsen, N. W., et al. (2013). Hailstones: a window into the microbial and chemical inventory of a storm cloud. PLoS ONE 8:e53550. doi: 10.1371/journal.pone.0053550
94. Scheuvens, D., Schütz, L., Kandler, K., Ebert, M., and Weinbruch, S. (2013). Bulk composition of northern African dust and its source sediments-A compilation. Earth Sci. Rev. 116, 170-194. doi: 10.1016/j.earscirev.2012.08.005
95. Schwikowski, M., Seibert, P., Baltensperger, U., and Gaggeler, H. W. (1995). A study of an outstanding saharan dust event at the high-alpine site jungfraujoch, Switzerland. Atmos. Environ. 29, 1829-1842. doi: 10.1016/1352-2310(95)00060-C
96. Segawa, T., Miyamoto, K., Ushida, K., Agata, K., Okada, N., and Kohshima, S. (2005). Seasonal change in bacterial flora and biomass in mountain snow from the Tateyama Mountains, Japan, analyzed by 16S rRNA gene sequencing and real-time PCR. Appl. Environ. Microbiol. 71, 123-130. doi: 10.1128/AEM.71.1.123-130.2005
97. Shao, Y., Wyrwoll, K.-H., Chappell, A., Huang, J., Lin, Z., McTainsh, G. H., et al. (2011). Dust cycle: an emerging core theme in Earth system science. Aeolian Res. 2, 181-204. doi: 10.1016/j.aeolia.2011.02.001
98. Smith, D. J., Griffin, D. W., and Schuerger, A. C. (2009). Stratospheric microbiology at 20 km over the Pacific Ocean. Aerobiologia 26, 35-46. doi: 10.1007/s10453-009-9141-7
99. Sodemann, H., Palmer, A. S., Schwierz, C., Schwikowski, M., and Wernli, H. (2006). The transport history of two Saharan dust events archived in an Alpine ice core. Atmos. Chem. Phys. 6, 667-688. doi: 10.5194/acp-6-667-2006
100. Solomon, S., Daniel, J. S., Neely Iii, R. R., Vernier, J.-P., Dutton, E. G., and Thomason, L. W. (2011). The persistently variable "background" stratospheric aerosol layer and global climate change. Science 333, 866-870. doi: 10.1126/science.1206027
101. Thevenon, F., Anselmetti, F. S., Bernasconi, S. M., and Schwikowski, M. (2009). Mineral dust and elemental black carbon records from an Alpine ice core (Colle Gnifetti glacier) over the last millennium. J. Geophys. Res. Atmos. 114:D17102. doi: 10.1029/2008jd011490
102. Tong, Y. Y., and Lighthart, B. (1997). Solar radiation is shown to select for pigmented bacteria in the ambient outdoor atmosphere. Photochem. Photobiol. 65, 103-106. doi: 10.1111/j.1751-1097.1997.tb01884.x
103. Yamaguchi, N., Park, J., Kodama, M., Ichijo, T., Baba, T., and Nasu, M. (2014). Changes in the airborne bacterial community in outdoor environments following Asian dust events. Microb. Environ. 29, 82-88. doi: 10.1264/jsme2.ME13080
104. Yuan, M., Zhang, W., Dai, S., Wu, J., Wang, Y., Tao, T., et al. (2009). Deinococcus gobiensis sp. nov., an extremely radiation-resistant bacterium. Int. J. Syst. Evol. Microbiol. 59, 1513-1517. doi: 10.1099/ijs.0.004523-0
105. Zhang, H. (2003). Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int. J. Syst. Evol. Microbiol. 53, 1155-1163. doi: 10.1099/ijs.0.02520-0