Abstract
Aquatic and terrestrial associations of phototrophic and heterotrophic microorganisms active in hydrocarbon bioremediation have been described earlier. The question arises: do similar consortia also occur in the atmosphere? Dust samples at the height of 15 m were collected from Kuwait City air, and analyzed microbiologically for phototrophic and heterotrophic hydrocarbon-utilizing microorganisms, which were subsequently characterized according to their 16S rRNA gene sequences. The hydrocarbon utilization potential of the heterotrophs alone, and in association with the phototrophic partners, was measured quantitatively. The chlorophyte Gloeotila sp. and the two cyanobacteria Nostoc commune and Leptolyngbya thermalis were found associated with dust, and (for comparison) the cynobacteria Leptolyngbya sp. and Acaryochloris sp. were isolated from coastal water. All phototrophic cultures harbored oil vapor-utilizing bacteria in the magnitude of 105 g−1. Each phototrophic culture had its unique oil-utilizing bacteria; however, the bacterial composition in Leptolyngbya cultures from air and water was similar. The hydrocarbon-utilizing bacteria were affiliated with Acinetobacter sp., Aeromonas caviae, Alcanivorax jadensis, Bacillus asahii, Bacillus pumilus, Marinobacter aquaeolei, Paenibacillus sp., and Stenotrophomonas maltophilia. The nonaxenic cultures, when used as inocula in batch cultures, attenuated crude oil in light and dark, and in the presence of antibiotics and absence of nitrogenous compounds. Aqueous and diethyl ether extracts from the phototrophic cultures enhanced the growth of the pertinent oil-utilizing bacteria in batch cultures, with oil vapor as a sole carbon source. It was concluded that the airborne microbial associations may be effective in bioremediating atmospheric hydrocarbon pollutants in situ. Like the aquatic and terrestrial habitats, the atmosphere contains dust-borne associations of phototrophic and heterotrophic hydrocarbon-utilizing bacteria that are active in hydrocarbon attenuation.
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References
Ali N, Sorkhoh N, Salamah S, Eliyas M, Radwan SS (2012) The potential of epiphytic hydrocarbon-utilizing bacteria on legume leaves for attenuation of atmospheric hydrocarbon pollutants. J Environ Manag 93:113–120
Al-Mailem DM, Sorkhoh NA, Salamah S, Eliyas M, Radwan SS (2010) Oil-bioremediation potential of Arabain Gulf mud flats rich in diazotrophic hydrocarbon-utilizing bacteria. Int Biodeter Biodegrad 64:218–225
Altschul SF, Madden TL, Schafter AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res 25:3389–3402
Amato P, Menager M, Sancelme M, Laj P, Mailhot G, Delort AM (2005) Microbial population in cloud water at the Puy de Dume: implications for the chemistry of clouds. Atmos Environ 39:4143–4153
Amato P, Parazols M, Sancelme M, Mailhot G, Laj P, Delort AM (2007) An important oceanic source of micro-organisms for cloud water at the Puy de Dome (France). Atmos Environ 41:8253–8263
Atlas RM, Bartha R (1997) Microbial ecology, fundamentals and applications, 4th edn. Benjamin Cummings, California
Blumthaler M, Ambach W, Rehwald W (1992) Solar UV-A and UV-B radiation fluxes at two alpine stations at different altitudes. Theor Appl Climatol 46:39–44
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 75:5121–5130
Brinkhoff T, Santegoeds CM, Sahm K, Kuever J, Muyzer G (1998) A polyphasic approach to study the diversity of sulfur-oxidizing Thiomicrospira species in coastal sediments of the German Wadden Sea. Appl Environ Microbiol 64:4650–4657
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 U S A 104:299–304
Burrows SM, Elber W, Lawrence MG, Pöschl U (2009) Bacteria in the global atmosphere—part 1: review and synthesis of literature data for different ecosystems. Atmos Chem Phys 9:9263–9280
Fahlgren C, Hagstrom A, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability and origin of airborne bacteria. Appl Environ Microbiol 76:3015–3025
Fiere 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 74:200–207
Fuzzi S, Mandrioli P, Perfetto A (1997) Fog droplets: an atmospheric source of secondary biological aerosol particles. Atmos Environ 31:287–290
Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507
Hube AE, Heyduck-Söller B, Fischer U (2009) Phylogenetic classification of heterotrophic bacteria associated with filamentous marine cyanobacteria in culture. Syst Appl Microbiol 32:256–265
Jones B, Grant W, Duckworth A, Owenson G (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200
Kellogg CA, Griffin DW (2006) Aerobiology and the global transport of desert dust. Trends Ecol Evol 21:638–644
Kiske CR, Banton KL, Adorada DL, Strak PC, Hill KK, Jackson PJ (1998) Small scale DNA sample preparation method for field PCR detection of microbial cells and spores in soil. Appl Environ Microbiol 64:2463–2472
Klug MJ, Markovetz AJ (1971) Utilization of aliphatic hydrocarbons by microorganisms. Adv Microb Physiol 5:1–43
Lighthart B, Shaffer BT (1995) Airborne bacteria in the atmospheric surface layer: temporal distribution above a grass seed field. Appl Environ Microbiol 61:1492–1496
Mancinelli RL, Shulls WA (1978) Airborne bacteria in an urban environment. Appl Environ Microbiol 35:1095–1101
Marita R (1975) Psychrophilic bacteria. Microbiol Mol Biol Rev 39:144–167
Maron PA, Lejon DPH, 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 39:3687–3695
Millner PD (2009) Bioaerosols associated with animal production operations. Bioresour Technol 100:5379–5385
Moletta-Denat M, Bru-Adan V, Delgenes JP, Hamelin J, Wery N, Godon JJ (2010) Selective microbial aerosolization in biogas demonstrated by quantitative PCR. Bioresour Technol 101:7252–7257
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes encoding for 16S rRNA. Appl Environ Microbiol 59:695–700
Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69:143–157
Radosevich JL, Wilson WJ, Shinn JH, DeSantis TZ, Andersen GL (2002) Development of a high-volume aerosol collection system for the identification of air-borne micro-organisms. Lett Appl Microbiol 34:162–167
Radwan SS (2008) Microbiology of oil-contaminated desert soils and coastal areas in the Arabian Gulf. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Soil biology, vol 13. Springer, Heidelberg, pp 275–297
Radwan SS, Al-Hasan RH (2001) Potential application of coastal biofilm-coated gravel particles for treating oily waste. Aquat Microb Ecol 23:113–117
Radwan SS, Al-Hasan RH, Salamah S, Khanafer M (2005) Oil-consuming microbial consortia floating in the Arabian Gulf. Int Biodeter Biodegrad 56:28–33
Radwan SS, Mahmoud H, Khanafer M, Al-Habib A, Al-Hasan R (2010) Bacterial consortia with combined potential for hydrocarbon-utilization and nitrogen-fixation from epilithic biofilms along the Arabian Gulf coasts. Microb Ecol 60:354–363
Raltledge C (1978) Degradation of aliphatic hydrocarbons. In: Watkinson I (ed) Developments in biodeterioration of hydrocarbons, vol 1. Applied Science, Essex, pp 1–45
Rehm HJ, Reiff I (1981) Mechanisms and occurrence of microbial oxidation of long-chain alkanes. Adv Biochem Eng 19:175–216
Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27
Rotheschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Sandhu A, Halverson LJ, Beattie GA (2007) Bacterial degradation of airborne phenol in the phyllosphere. Environ Microbiol 2:383–392
Santegoeds CM, Ferdelman TG, Muyzer G, Beer D (1998) Structural and functional dynamics of sulfate-reduction populations in bacterial biofilms. Appl Environ Microbiol 64:3731–3739
Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophy Res Lett 28:239–242
Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk H, 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 177:7050–7059
Sorkhoh NA, Ghannoum MA, Ibrahim AS, Stretton RJ, Radwan SS (1990) Crude oil and hydrocarbon degrading strains of Rhodococcus rhodochrous isolated from soil and marine environments in Kuwait. Environ Pollut 65:1–17
Sorkhoh NA, Al-Hasan RH, Radwan SS, Hopner T (1992) Self-cleaning of the gulf. Nature 359:109
Sorkhoh NA, Al-Mailem DM, Ali N, Al-Awadhi H, Salamah S, Eliyas M, Radwan SS (2011) Bioremediation of volatile oil hydrocarbons by epiphytic bacteria associated with American grass (Cynodon sp.) and broad bean (Vicia faba) leaves. Int Biodeter Biodeg 65:797–802
Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratified Fjord (Maiagar Fjord, Denmark) as evaluated by most-probable number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl Environ Microbiol 62:1405–1415
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Tong Y, Lighthart B (1999) Diurnal distribution of total and culturable atmospheric bacteria at rural site. Aerosol Sci Tech 30:246–254
Tong Y, 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
Warneck P (1988) Chemistry of the natural atmosphere. Academic, New York
Wawer C, Muyzer G (1995) Genetic diversity of Desulfouvibrio spp. in environmental samples analyzed by denaturing gradient gel electrophoresis of [NiFe] hydrogenase gene fragments. Appl Environ Microbiol 62:2203–2210
Womack AM, Bohannan BJM, Green JL (2010) Biodiversity and biogeography of the atmosphere. Phil Trans R Soc B 365:3645–3653
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The work was supported by the University of Kuwait, Research Grant SL 09/08. Thanks are due to the SAF unit and GRF, Kuwait University for providing GLC (GS 02/01) and the genetic analyzer (GS 01/02) facilities.
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Al-Bader, D., Eliyas, M., Rayan, R. et al. Air–dust-borne associations of phototrophic and hydrocarbon-utilizing microorganisms: promising consortia in volatile hydrocarbon bioremediation. Environ Sci Pollut Res 19, 3997–4005 (2012). https://doi.org/10.1007/s11356-012-0897-x
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DOI: https://doi.org/10.1007/s11356-012-0897-x