Abstract
Phyllosphere bacteria on ornamental plants were characterized based on their diversity and activity towards the removal of polycyclic aromatic hydrocarbons (PAHs), the major air pollutants in urban area. The amounts of PAH-degrading bacteria were about 1–10% of the total heterotrophic phyllosphere populations and consisted of diverse bacterial species such as Acinetobacter, Pseudomonas, Pseudoxanthomonas, Mycobacterium, and uncultured bacteria. Bacterial community structures analyzed by polymerase chain reaction–denaturing gradient gel electrophoresis from each plant species showed distinct band patterns. The uniqueness of these phyllosphere bacterial communities was partly due to the variation in leaf morphology and chemical properties of ornamental plants. The PAH degradation activity of these bacteria was monitored in gas-tight systems containing sterilized or unsterilized leaves. The results indicated that phyllosphere bacteria on unsterilized leaves were able to enhance the activity of leaves for phenanthrene removal. When compared between plant species, phenanthrene removal efficiency corresponded to the size of phenanthrene-degrading bacteria. In addition, phyllosphere bacteria on Wrightia religiosa were able to reduce other PAHs such as acenaphthylene, acenaphthene, and fluorine in 60-ml glass vials and in a 14-l glass chamber. Thus, phyllosphere bacteria on ornamental plants may play an important role in natural attenuation of airborne PAHs in urban areas.
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Bakker MI, Tolls J, Kolloffel C (2001) Deposition of atmospheric semivolatile organic compounds to vegetation. In: Lipnick RL, Hermens JLM, Jones KC, Muir DCG (eds) Persistent, bioaccumulative, and toxic chemicals I: fate and exposure. American Chemical Society, Washington, pp 218–236
Bohme F, Welsch-Pausch K, Mclachlan MS (1999) Uptake of airborne semivolatile organic compounds in agricultural plants: field measurements of interspecies variability. Environ Sci Technol 33:1805–1813
Boonyatumanond R, Murakami M, Wattayakorn G, Togo A, Takada H (2007) Sources of polycyclic aromatic hydrocarbons (PAHs) in street dust in a tropical Asian mega-city, Bangkok, Thailand. Sci Total Environ 384:420–432
Choi S-D, Staebler RM, Li H, Su Y, Gevao B, Harner T, Wania F (2008) Depletion of gaseous polycyclic aromatic hydrocarbons by a forest canopy. Atmos Chem Phys 8:4105–4113
Darlington AB, Dat JF, Dixon MA (2001) The biofiltration of indoor air: air flux and temperature influences the removal of toluene, ethylbenzene, and xylene. Environ Sci Technol 35:240–246
De Kempeneer L, Sercu B, Vanbrabant W, Van Langenhove H, Verstraete W (2004) Bioaugmentation of the phyllosphere for the removal of toluene from indoor air. Appl Microbiol Biotechnol 64:284–288
Hong Y-J, Jeng HA, Gau Y-Y, Lin C, Lee I-L (2006) Distribution of volatile organic compounds in ambient air of Kaohsiung, Taiwan. Environ Monit Assess 119:43–56
Johnsen AR, Bendixen K, Karlson U (2002) Detection of microbial growth on polycyclic aromatic hydrocarbons in microtiter plates by using the respiration indicator WST-1. Appl Environ Microbiol 68:2683–2689
Johnsen AR, Karlson U (2007) Diffuse PAH contamination of surface soils: environmental occurrence, bioavailability, and microbial degradation. Appl Microbiol Biotechnol 76:533–543
Karnchanasest B, Satayavibul A (2005) Orange jasmine leaves as an indicator of atmospheric polycyclic aromatic hydrocarbons. Songklanakarin J Sci Technol 27:877–888
Kasuga K, Nojiri H, Yamane H, Kodama T, Omori T (1997) Cloning and characterization of the genes involved in the degradation of dibenzofuran by Terrabacter sp. strain DBF63. J Ferment Bioeng 84:387–399
Kipopoulou AM, Manoli E, Samara C (1999) Bioconcentration of polycyclic aromatic hydrocarbons in vegetables grown in an industrial area. Environ Pollut 106:369–380
Kolar K, Ciganek M, Malecha J (2004) Air/polymer distribution coefficients for polycyclic aromatic hydrocarbons by solid-phase microextraction sampling. J Chromatogr A 1029:263–266
Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917
Lanzerstorfer CH, Puxbaum H (1990) Volatile hydrocarbons in and around Vienna, Austria. Water Air Soil Pollut 51:345–355
Librando V, Perrini G, Tomasello M (2002) Biomonitoring of atmospheric PAHs by evergreen plants: correlations and applicability. Polycycl Aromat Compd 22:549–559
Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883
Liu YN, Tao S, Dou H, Zhang TW, Zhang XL, Dawson R (2007) Exposure of traffic police to polycyclic aromatic hydrocarbons in Beijing, China. Chemosphere 66:1922–1928
Pathirana S, Connell DW, Vowles PD (1994) Distribution of polycyclic aromatic hydrocarbons (PAHs) in an urban roadway system. Ecotoxicol Environ Saf 28:256–269
Ruchirawat M, Settachan D, Navasumrit P, Tuntaviroon J, Autrup H (2007) Assessment of potential cancer risk in children exposed to urban air pollution in Bangkok, Thailand. Toxicol Lett 168:200–209
Sandhu A, Halverson LJ, Beattie GA (2007) Bacterial degradation of airborne phenol in the phyllosphere. Environ Microbiol 9:383–392
Sandhu A, Halverson LJ, Beattie GA (2009) Identification and genetic characterization of phenol-degrading bacteria from leaf microbial communities. Microb Ecol 57:276–285
Schauer C, Niessner R, Poschl U (2003) Polycyclic aromatic hydrocarbons in urban air particulate matter: decadal and seasonal trends, chemical degradation, and sampling artifacts. Environ Sci Technol 37:2861–2868
Simonich SL, Hites RA (1994) Vegetation-atmosphere partitioning of polycyclic aromatic hydrocarbons. Environ Sci Technol 28:939–943
Tsai Y-L, Olson BH (1991) Rapid method for direct extraction of DNA from soil and sediments. Appl Environ Microbiol 57:1070–1074
Waight K, Pinyakong O, Luepromchai E (2007) Degradation of phenanthrene deposited on plant leaves by phyllosphere bacteria. J Gen Appl Microbiol 53:265–272
Wang YQ, Tao S, Jiao XC, Coveney RM, Wu SP, Xing BS (2008) Polycyclic aromatic hydrocarbons in leaf cuticles and inner tissues of six species of trees in urban Beijing. Environ Pollut 151:158–164
Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755
Yadav RKP, Halley JM, Karamanoli K, Constantinidou H-I, Vokou D (2004) Bacterial populations on the leaves of Mediterranean plants: quantitative features and testing of distribution models. Environ Exp Bot 52:63–77
Yadav RKP, Karamanoli K, Vokou D (2005) Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb Ecol 50:185–196
Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci U S A 98:3889–3894
Acknowledgements
The authors thank Prof. Rudolf Müller, Technical University Hamburg-Harburg, Germany, for his invaluable suggestions. This work was supported by a grant from the Thailand Research Fund (TRF) and The Commission on Higher Education. In addition, it is partially funded by the Chulalongkorn University Graduate Thesis Grant and Research Funds from the Faculty of Science, Chulalongkorn University.
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Yutthammo, C., Thongthammachat, N., Pinphanichakarn, P. et al. Diversity and Activity of PAH-Degrading Bacteria in the Phyllosphere of Ornamental Plants. Microb Ecol 59, 357–368 (2010). https://doi.org/10.1007/s00248-009-9631-8
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DOI: https://doi.org/10.1007/s00248-009-9631-8