Water, Air, & Soil Pollution

, 224:1648 | Cite as

Isolation and Identification of Toluene-Metabolizing Bacteria from Rhizospheres of Two Indoor Plants

  • Hao Zhang
  • Svoboda V. Pennisi
  • Stanley J. Kays
  • Mussie Y. Habteselassie
Article

Abstract

The role of the rhizosphere microbial community in removing volatile organic compounds has not been well investigated. In this study, two species of indoor foliage plants, Fittonia verschaffeltii var. argyroneura and Hoya carnosa, were primed with toluene exposure for 2 months, followed by isolation and identification of the rhizosphere bacteria that were demonstrated to metabolize toluene. A total of 42 bacterial isolates were obtained. The number of bacterial isolates was narrowed down to 23, which had banding pattern similarities of 80 % or less, using BOX-polymerase chain reaction (PCR) fingerprinting technique. The 23 isolates were further characterized by sequencing part of their 16S rDNA after PCR. Their identities were examined using Basic Local Alignment Search Tool (BLAST), resulting in the isolates having the highest sequence similarities (97–100 %) to eight known bacteria strains, none of which had been previously reported to be capable of degrading toluene. The bacterial isolates were positive for toluene monooxygenase gene, confirming their genetic potential to metabolize toluene. Five of the isolates were further tested with 14C-labeled toluene to directly show their ability to metabolize toluene. Isolate type did not significantly affect the percent of toluene mineralized over 2 weeks' time. However, the isolates had differing response to varying toluene concentrations. Under low (0.05) and high (0.2 μCi/mL) concentrations, they mineralized 43 and 49 % of toluene, respectively. The isolation and characterization of toluene-metabolizing bacteria corroborates previous speculation that the rhizosphere microbial community contributes to the phytoremediation potential of indoor foliage plants.

Keywords

Rhizosphere bacteria Phytoremediation Indoor air quality Foliage plants 

References

  1. ACGIH. (1995). Threshold limit values for chemical substances and physical agents and biological exposure indices. Cincinnati, Ohio: American Conference of Government and Industrial Hygienists.Google Scholar
  2. Ando, M. (2002). Indoor air and human health. Sick-house syndrome and multiple chemical sensitivity. Kokuritsu Iyakuhin Shokuhin Eisei Kenkyūjo Hōkoku, 120, 6–38.Google Scholar
  3. Arutchelvan, V., Kanakasabai, V., Elangovan, R., Nagarajan, S., & Muralikrishnan, V. (2006). Kinetics of high strength phenol degradation using Bacilus brevis. Journal of Hazardous Materials, 129, 216–222.CrossRefGoogle Scholar
  4. ATSDR. (2000). Toxicological profile for toluene. Agency for Toxic Substance and Disease. Atlanta, GA: Registry.Google Scholar
  5. Baldwin, B. R., Nakatsu, C. H., & Nies, L. (2003). Detection and enumeration of aromatic oxygenase genes by multiplex and real-time PCR. Applied and Environmental Microbiology, 69, 3350–3358.CrossRefGoogle Scholar
  6. Brown, S. (1997). Volatile organic compounds in indoor air: sources and control. Chemistry in Australia, 64, 10–13.Google Scholar
  7. Brown, S. K., Sim, M. R., Abramson, M. J., & Gray, C. N. (1994). Concentrations of volatile organic compounds in indoor air—a review. Indoor Air, 4, 123–134.CrossRefGoogle Scholar
  8. Chen, L., Yurimoto, H., Li, K., Orita, I., Akita, M., Kato, N., et al. (2010). Assimilation of formaldehyde in transgenic plants due to the introduction of the bacterial ribulose monophosphate pathway genes. Bioscience, Biotechnology, and Biochemistry, 74, 627–635.CrossRefGoogle Scholar
  9. Cleveland, C. C., & Yavitt, J. B. (1998). Microbial consumption of atmospheric isoprene in a temperate forest soil. Applied and Environmental Microbiology, 6, 172–177.Google Scholar
  10. Chikara, H., Iwamoto, S., & Yoshimura, T. (2009). Indoor air pollution of volatile organic compounds—indoor/outdoor concentrations, sources and exposures. Nippon Eiseigaku Zasshi, 64, 683–688.CrossRefGoogle Scholar
  11. Chun, S. C., Yoo, M. H., Moon, Y. S., Shin, M. H., Son, K. C., Chung, I. M., et al. (2010). Effect of bacterial population from rhizosphere of various foliage plants on removal of indoor volatile organic compounds. Korean Journal of Horticultural Science and Technology, 28, 476–483.Google Scholar
  12. Cohen, Y. (1996). Volatile organic compounds in the environment: A multimedia perspective. Volatile organic compounds in the environment. In W. Wang, J. Schnoor, and J. Doi (eds.) (pp. 7–32). ASTM STP 1261. American Society for Testing and Materials.Google Scholar
  13. Conover, C. A., & Poole, R. T. (1981). Environmental factors. In J. Joiner (Ed.), Foliage plant production (pp. 269–283). New Jersey: Prentice-Hall, Englewood Cliffs.Google Scholar
  14. Darlington, A., Chan, M., Malloch, D., Pilger, C., & Dixon, M. A. (2000). The biofiltration of indoor air: implications for air quality. Indoor Air, 10, 39–46.CrossRefGoogle Scholar
  15. Dastager, S. G., Lee, J., Ju, Y., Park, D., & Kim, C. (2008). Microbacterium kribbense spp. Nov., isolated from soil. International Journal of Systematic and Evolutionary Microbiology, 58, 2536–2540.CrossRefGoogle Scholar
  16. Dawson, H. E., & McAlary, T. (2009). A compilation of statistics for VOCs from post-1990 indoor air concentration studies in North American residences unaffected by subsurface vapor intrusion. Ground Water Monitoring Remediation, 29, 60–69.CrossRefGoogle Scholar
  17. Ellis, D. E., Lutz, E. J., Odom, J. M., Buchanan, R. J., Bartlett, C. L., Lee, M. D., et al. (2000). Bio-augmentation for accelerated in situ anaerobic bioremediation. Environmental Science and Technology, 34, 2254–2260.CrossRefGoogle Scholar
  18. Fantroussi, S. E., & Agathos, S. N. (2005). Is bio-augmentation a feasible strategy for pollutant removal and site remediation? Current Opinion in Microbiology, 8, 268–275.CrossRefGoogle Scholar
  19. Felske, A., Engelen, B., Nübel, U., & Backhaus, H. (1996). Direct ribosome isolation from soil to extract bacterial rRNA for community analysis. Applied and Environmental Microbiology, 62, 4162–4167.Google Scholar
  20. Guieysse, B., Hort, C., Platel, V., Munoz, R., Ondarts, M., & Revah, S. (2008). Biological treatment of indoor air for VOC removal: potential and challenges. Biotechnological Advances, 26, 398–410.CrossRefGoogle Scholar
  21. Godish, T. (1995). Sick building: definition, diagnosis, and mitigation. Boca Raton, FL: Lewis.Google Scholar
  22. Grayston, S. J., Wang, S. Q., Campbell, C. D., & Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biology and Biochemistry, 30, 369–378.CrossRefGoogle Scholar
  23. Hayashi, H., Kunugita, N., Arashidani, K., Fujimaki, H., & Ichikawa, M. (2004). Long-term exposure to low levels of formaldehyde increases the number of tyrosine hydroxylase-immunopositive periglomerular cells in mouse main olfactory bulb. Brain Research, 1007, 192–197.CrossRefGoogle Scholar
  24. Helmke, E., & Weyland, H. (1984). Rhodococcus marinonascens sp. Nov., an actinomycete from the sea. International Journal of Systematic Bacteriology, 34, 127–138.CrossRefGoogle Scholar
  25. Hendrickx, B., Junca, H., Vosahlova, J., Lindner, A., Rüegg, I., Bucheli-Witschel, M., et al. (2006). Alternative primer sets for PCR detection of genotypes involved in bacterial aerobic BTEX degradation: distribution of the genes in BTEX degrading isolates and in subsurface soils of a BTEX contaminated industrial site. Journal of Microbiological Methods, 64, 250–265.CrossRefGoogle Scholar
  26. Ilgen, E., Karfich, N., Levsen, K., Angerer, J., Schneider, P., Heinrich, J., et al. (2001). Aromatic hydrocarbons in the atmospheric environment: part I. Indoor versus outdoor sources, the influence of traffic. Atmospheric Environment, 35, 1235–1252.CrossRefGoogle Scholar
  27. Ingrosso, G. (2002). Free radical chemistry and its concern with indoor air quality: an open problem. Microchemistry Journal, 73, 221–236.CrossRefGoogle Scholar
  28. Jones, A. P. (1999). Indoor air quality and health. Atmospheric Environment, 33, 4535–4564.CrossRefGoogle Scholar
  29. Kays, S. J. (2011). The value creation of plants for future urban agriculture. In K. J. Kim (Ed.), National Institute of Horticulture and Herbal Sciences (pp. 3–21). Suwon, Korea: RDA.Google Scholar
  30. Kim, K. J., & Lee, D. W. (2008). Efficiency of volatile formaldehyde removal of orchids as affected by species and crassulacean acid metabolism (CAM) nature. Horticulture, Environment and Biotechnology, 49, 132–137.Google Scholar
  31. Kim, K. J., Kil, M. J., Song, J. S., Yoo, E. H., Son, K. C., & Kays, S. J. (2008). Efficiency of volatile formaldehyde removal by indoor plants: contribution of aerial plant parts versus the root zone. Journal of American Society for Horticultural Sciences, 133, 521–526.Google Scholar
  32. Kirkeskov, L., Witterseh, T., Funch, L. W., Kristiansen, E., Mølhave, L., Hansen, M. K., et al. (2009). Health evaluation of volatile organic compound (VOC) emission from exotic wood products. Indoor Air, 19, 45–57.CrossRefGoogle Scholar
  33. Kondo, T., Hasegawa, K., Uchida, R., Onishi, M., Mizukami, A., & Omasa, K. (1995). Absorption of formaldehyde by oleander (Nerium indicum). Environmental Science and Technology, 29, 2901–2903.CrossRefGoogle Scholar
  34. Kostiainen, R. (1995). Volatile organic compounds in the indoor air of normal and sick houses. Atmospheric Environment, 29, 693–702.CrossRefGoogle Scholar
  35. Kraffczyk, I., Trolldenier, G., & Beringer, H. (1984). Soluble root exudates of maize influence of potassium supply and rhizosphere microorganisms. Soil Biology and Biochemistry, 16, 315–322.CrossRefGoogle Scholar
  36. Kuiper, I., Lagendijk, E. L., Bloemberg, G. V., & Lugtenberg, J. J. (2004). Rhizoremediation: a beneficial plant–microbe interaction. Molecular Plant-Microbial Interaction, 1, 6–15.CrossRefGoogle Scholar
  37. Liu, Y. J., Mu, Y. J., Zhu, Y. G., Ding, H., & Arens, N. C. (2007). Which ornamental plant species effectively remove benzene from indoor air? Atmospheric Environment, 41, 650–654.CrossRefGoogle Scholar
  38. Macdonald, L. M., Paterson, E., Dawson, L. A., & MacDonald, A. J. S. (2004). Short-term effects of defoliation on the soil microbial community associated with two contrasting Lolium perenne cultivars. Soil Biology and Biochemistry, 36, 489–489.CrossRefGoogle Scholar
  39. Martino, C. D., López, N. I., & Iustman, L. J. R. (2012). Isolation and characterization of benzene, toluene and xylene degrading Pseudomonas sp. selected as candidates for bioremediation. International Biodeterioration and Biodegradation, 67, 15–20.CrossRefGoogle Scholar
  40. McGuinness, M., & Dowling, D. (2009). Plant-associated bacterial degradation of toxic organic compounds in soil. International Journal of Environmental Research and Public Health, 6, 2226–2247.CrossRefGoogle Scholar
  41. Mills, H. A., & Jones, J. B., Jr. (1996). Plant analysis handbook II. Athens, GA: MicroMacro.Google Scholar
  42. Motoyama, T., Kadokura, K., Tatsusawa, S., Arie, T., & Yamaguchi, I. (2001). Application of plant–microbe systems to bioremediation. RIKEN Reviews, 42, 35–38.Google Scholar
  43. Nelson, D. M., Glawe, A. J., Labeda, D. P., Cann, I. K. O., & Mackie, R. I. (2009). Paenibacillus tundrae sp. nov. and Paenibacillus xylanexedens sp. nov., psychrotolerant, xylan-degrading bacteria from Alaskan tundra. International Journal of Systematic Bacteriology, 59, 1708–1714.Google Scholar
  44. Council, N. R. (2011). Climate change, the indoor environment, and health. Washington, DC: The National Academies Press.Google Scholar
  45. NOHSC. (2001). Air toxics and indoor air quality in Australia. National Occupational Health and Safety Commission. http://155.187.3.82/atmosphere/airquality/publications/sok/appa.html
  46. NTP. (2000). Toxicology and carcinogenesis studies of toluene in F344/N rats and B6C3F1 mice (inhalation studies) (Technical report. Series no. 371). National Toxicology Program: National Institute of Health, US Department of Health and Human Service, Public Health Service, Research Triangle, Park, NC.Google Scholar
  47. Orwell, R., Wood, R., Tarran, J., Torpy, F., & Burchett, M. D. (2004). Removal of Benzene by the indoor plant/substrate microcosm and implications for air quality. Water, Air, and Soil Pollution, 157, 193–207.CrossRefGoogle Scholar
  48. Orwell, R., Wood, R., Burchett, M., Tarran, J., & Torpy, F. (2006). The potted-plant microcosm substantially reduces indoor air VOC pollution: II. Laboratory study. Water, Air, and Soil Pollution, 177, 59–80.CrossRefGoogle Scholar
  49. Park, M. J., Kim, H. B., An, D. S., Yang, H. C., Oh, S. T., Chung, J. J., et al. (2007). Paenibacillus soli sp. Nov., a xylanolytic bacterium isolated from soil. International Journal of Systematic Bacteriology, 57, 146–150.Google Scholar
  50. Plangklang, P., & Reungsand, A. (2011). Bioaugmentation of carbofuran residues in soil by Burkholderia cepacia PCL3: a small-scale field study. International Biodeterioration and Biodegradation, 65, 902–905.CrossRefGoogle Scholar
  51. Rademaker, J. L., Louws, R. J., Versalovic, J., & Bruijn, F. J. (2004). Characterization of the diversity of ecologically important microbes by rep-PCR genomic fingerprinting. In Kowalchuk, G.A. et al. (eds.) Molecular microbial ecology manual (pp. 611–643). Vol. 1. Boston, MA: Kluwer Academic.Google Scholar
  52. Reed, D. W. (1996). A grower's guide to water, media, and nutrition for greenhouse crops. Batavia, IL: Ball.Google Scholar
  53. Rivas, R., Garcia-Fratile, P., Mateos, P. F., Martinez-Molina, E., & Velazquez, E. (2006). Paenibacillus cellolosilyticus sp. Nov., a cellulotic and xylanolytic bacterium isolated from the bract phyllosphere of Phoenix dactylifera. International Journal of Systematic Bacteriology, 56, 2777–2781.Google Scholar
  54. Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J., & Dowling, D. N. (2008). Bacterial endophytes: recent developments and applications. FEMS Microbiology Ecology, 278, 1–9.CrossRefGoogle Scholar
  55. Schwab, A. P., Al-Assi, A. A., & Banks, M. K. (1998). Adsorption of napthtalene onto plant roots. Journal of Environmental Quality, 27, 220–224.CrossRefGoogle Scholar
  56. Shapir, N., & Mandelbaum, R. T. (1997). Atrazine degradation in subsurface soil by indigenous and introduced microorganisms. Journal of Agriculture and Food Chemistry, 45, 4481–4486.CrossRefGoogle Scholar
  57. Shinoda, Y., Sakai, Y., Uenishi, H., Uchihashi, Y., Hiraishi, A., Yukawa, H., et al. (2004). Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Applied and Environmental Microbiology, 70, 1385–1392.CrossRefGoogle Scholar
  58. Shinohara, N., Mizukoshi, A., & Yanagisawa, Y. (2004). Identification of responsible volatile chemicals that induce hypersensitive reactions to multiple chemical sensitivity patients. Journal of Exposure Analysis and Environmental Epidemiology, 14, 84–91.CrossRefGoogle Scholar
  59. Smith, A. E., Hristova, K., Wood, I., Mackay, D. M., Lory, E., Lorenzana, D., et al. (2005). Comparison of biostimulation versus bioaugmentation with bacterial strain PM1 for treatment of groundwater contaminated with methyl tertiary butyl ether (MTBE). Environ. Health Perspective, 113, 317–322.CrossRefGoogle Scholar
  60. Sterling, D. A. (1985). Indoor air and human health. In R. B. Gammage, S. B. Kaye, & V. A. Jacobs (Eds.), Volatile organic compounds in indoor air: An overview of sources, concentrations, and health effects (p. 387). New York: Lewis.Google Scholar
  61. Strong, L. C., McTavish, H., Sadowsky, M. J., & Wackett, L. P. (2000). Field-scale remediation of atrazine-contaminated soil using recombinant Escherichia coli expressing atrazine chlorohydrolase. Environmental Microbiology, 2, 91–98.CrossRefGoogle Scholar
  62. Suh, H.-H., Baiadon, T., Vallanno, J., & Spellgler, J. D. (2000). Criteria air pollutants and toxic air pollutants. Environmental Health Perspectives, 108, 625–633.Google Scholar
  63. Tani, K., Muneta, M., Nakamura, K., Shibuya, K., & Nasu, M. (2002). Monitoring of Ralstonia eutropha KT1 in groundwater in an experimental bio-augmentation field by in situ PCR. Applied and Environmental Microbiology, 68, 412–416.CrossRefGoogle Scholar
  64. van Veen, J. A., van Overbeek, L. S., & van Elsas, J. D. (1997). Fate and activity of microorganisms introduced into soil. Microbiology and Molecular Biology Reviews, 61, 121–135.Google Scholar
  65. Wenzel, W. W. (2009). Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant and Soil, 321, 385–408.CrossRefGoogle Scholar
  66. Wichmann, F. A., Muller, A., Busi, L. W., Cianni, N., Massolo, L., Schlink, U., et al. (2009). Increased asthma and respiratory symptoms in children exposed to petrochemical pollution. The Journal of Allergy and Clinical Immunology, 123, 632–638.CrossRefGoogle Scholar
  67. Wolkoff, P., & Nielsen, G. D. (2001). Organic compounds in indoor air—their relevance for perceived indoor air quality. Atmospheric Environment, 35, 4407–4417.CrossRefGoogle Scholar
  68. Wolf, D. C., Legg, J. O., & Boutton, T. W. (1994). Isotopic methods for the study of soil organic matter dynamics. In Weaver et al. (eds.) Methods in soil analysis. Part 2—Microbiological and biochemical properties (pp. 865–906). No. 5. Madison, WI: Soil Science Society of America, Inc.Google Scholar
  69. Wollum, A. G., II. (1994). Soil sampling for microbiological analysis. In Weaver et al. (Eds.), Methods in soil analysis. Part 2—Microbiological and biochemical properties (pp. 1–14). Madison, WI: Soil Science Society of America, Inc. No. 5.Google Scholar
  70. Wolverton, B. C., Johnson, A., & Bounds, K. (1989). Interior landscape plants for indoor air pollution abatement. NASA, Stennis Space Center: Final report. MS.Google Scholar
  71. Wolverton, B. C., Watkins, E. A., Jr., & McDonald, R. C. (1984). Foliage plants for removing indoor air pollutants from energy-efficient homes. Economic Botany, 38, 224–228.CrossRefGoogle Scholar
  72. Wood, R. A., Orwell, R. L., Tarran, J., Torpy, F., & Burchett, M. (2002). Potted-plant/growth media interactions and capacities for removal of volatiles from indoor air. Horticultural Science and Biotechnology, 77, 120–129.Google Scholar
  73. Won, D., Lusztyk, E., & Shaw, C. Y. (2005). Target VOC list. Final report. Ottawa, Ontario: National Research Council Canada.Google Scholar
  74. Yang, D. S., Pennisi, S. V., Son, K. C., & Kays, S. (2009). Screening indoor plants for volatile organic pollutant removal efficiency. Hort Science, 44, 1377–1381.Google Scholar
  75. Yeager, T., Gilliam, C., Bilderback, T., Fare, D., Niemiera, A., & Tilt, K. (1997). Best management practices: Guide for producing container-grown plants. Marietta, GA: Southern Nurserymen's Association.Google Scholar
  76. Yoo, M. H., Kwon, Y. J., Son, K. C., & Kays, S. J. (2006). Efficacy of indoor plants for the removal of single and mixed volatile organic pollutants and physiological effects of the volatiles on the plants. Journal of American Society for Horticultural Sciences, 131, 452–458.Google Scholar
  77. Yu, C., & Crump, D. (1998). A review of the emission of VOCs from polymeric materials used in buildings. Building and Environment, 33, 357–374.CrossRefGoogle Scholar
  78. Zabiegała, B. (2006). Organic compounds in indoor environments. Polish Journal of Environmental Studies, 15, 383–393.Google Scholar
  79. Zlamala, C., Schumann, P., Kampfer, P., Valens, M., Rossello-Mora, R., Lubitz, W., et al. (2002). Microbacterium aerolatum sp. nov., isolated from the air in the ‘Virgilkapelle’ in Vienna. International Journal of Systematic Bacteriology, 52, 1229–1234.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Hao Zhang
    • 1
  • Svoboda V. Pennisi
    • 2
  • Stanley J. Kays
    • 3
  • Mussie Y. Habteselassie
    • 1
  1. 1.Department of Crop and Soil SciencesThe University of Georgia—Griffin CampusGriffinUSA
  2. 2.Department of HorticultureThe University of Georgia—Griffin CampusGriffinUSA
  3. 3.Department of HorticultureThe University of GeorgiaAthensUSA

Personalised recommendations