DOI QR코드

DOI QR Code

Arabidopsis thaliana as Bioindicator of Fungal VOCs in Indoor Air

  • Lee, Samantha (Department of Plant Biology and Pathology, Rutgers, The State University of New Jersey) ;
  • Hung, Richard (Department of Biology, Kean University) ;
  • Yin, Guohua (Department of Plant Biology and Pathology, Rutgers, The State University of New Jersey) ;
  • Klich, Maren A. (Southern Regional Research Laboratory) ;
  • Grimm, Casey (Southern Regional Research Laboratory) ;
  • Bennett, Joan W. (Department of Plant Biology and Pathology, Rutgers, The State University of New Jersey)
  • Received : 2016.06.07
  • Accepted : 2016.07.06
  • Published : 2016.09.30

Abstract

In this paper, we demonstrate the ability of Arabidopsis thaliana to detect different mixtures of volatile organic compounds (VOCs) emitted by the common indoor fungus, Aspergillus versicolor, and demonstrate the potential usage of the plant as a bioindicator to monitor fungal VOCs in indoor air. We evaluated the volatile production of Aspergillus versicolor strains SRRC 108 (NRRL 3449) and SRRC 2559 (ATCC 32662) grown on nutrient rich fungal medium, and grown under conditions to mimic the substrate encountered in the built environment where fungi would typically grow indoors (moist wallboard and ceiling tiles). Using headspace solid phase microextraction/gas chromatography-mass spectrometry, we analyzed VOC profiles of the two strains. The most abundant compound produced by both strains on all three media was 1-octen-3-ol. Strain SRRC 2559 made several terpenes not detected from strain SRRC 108. Using a split-plate bioassay, we grew Arabidopsis thaliana in a shared atmosphere with VOCs from the two strains of Aspergillus versicolor grown on yeast extract sucrose medium. The VOCs emitted by SRRC 2559 had an adverse impact on seed germination and plant growth. Chemical standards of individual VOCs from the Aspergillus versicolor mixture (2-methyl-1-butanol, 3-methyl-1-butanol, 1-octen-3-ol, limonene, and ${\beta}-farnesene$), and ${\beta}-caryophyllene$ were tested one by one in seed germination and vegetative plant growth assays. The most inhibitory compound to both seed germination and plant growth was 1-octen-3-ol. Our data suggest that Arabidopsis is a useful model for monitoring indoor air quality as it is sensitive to naturally emitted fungal volatile mixtures as well as to chemical standards of individual compounds, and it exhibits relatively quick concentration- and duration-dependent responses.

Keywords

References

  1. Morath SU, Hung R, Bennett JW. Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 2012;26:73-83. https://doi.org/10.1016/j.fbr.2012.07.001
  2. Bitas V, Kim HS, Bennett JW, Kang S. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact 2013;26:835-43. https://doi.org/10.1094/MPMI-10-12-0249-CR
  3. Korpi A, Jarnberg J, Pasanen AL. Microbial volatile organic compounds. Crit Rev Toxicol 2009;39:139-93. https://doi.org/10.1080/10408440802291497
  4. Heddergott C, Calvo AM, Latge JP. The volatome of Aspergillus fumigatus. Eukaryot Cell 2014;13:1014-25. https://doi.org/10.1128/EC.00074-14
  5. Bennett JW, Hung R, Lee S, Padhi S. Fungal and bacterial volatile organic compounds: an overview and their role as ecological signaling agents. In: Hock B, editor. The Mycota IX Fungal Interactions. Berlin: Springer-Verlag; 2013. p. 373-93.
  6. WHO Regional Office for Europe. Guidelines for indoor air quality: dampness and mold. Rheinbach: Druckpartner Moser; 2009.
  7. Institute of Medicine. Damp indoor spaces and health. Washington, DC: National Academies; 2004.
  8. Polizzi V, Adams A, Picco AM, Adriaens E, Lenoir J, Van Peteghem C, De Saeger S, De Kimpe N. Influence of environmental conditions on production of volatiles by Trichoderma atroviride in relation with the sick building syndrome. Build Environ 2011;46:945-54. https://doi.org/10.1016/j.buildenv.2010.10.024
  9. Markert BA, Breure AM, Zechmeister HG. Trace metals and other contaminants in the environment. Vol. 6. Bioindicators and biomonitors: principles, concepts and applications. Amsterdam: Elsevier; 2003.
  10. Augusto S, Máguas C, Matos J, Pereira MJ, Branquinho C. Lichens as an integrating tool for monitoring PAH atmospheric deposition: a comparison with soil, air, and pine needles. Environ Pollut 2010;158:483-9. https://doi.org/10.1016/j.envpol.2009.08.016
  11. Hasselbach L, Ver Hoef JM, Ford J, Neitlich P, Crecelius E, Berryman S, Wolk B, Bohle T. Spatial patterns of cadmium and lead deposition on and adjacent to National Park Service lands in the vicinity of Red Dog Mine, Alaska. Sci Total Environ 2005;348:211-30. https://doi.org/10.1016/j.scitotenv.2004.12.084
  12. Rainio J, Niemela J. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers Conserv 2003;12:487-506. https://doi.org/10.1023/A:1022412617568
  13. Miller SW, Wooster D, Li J. Resistance and resilience of macroinvertebrates to irrigation water withdrawals. Freshw Biol 2007;52:2494-510. https://doi.org/10.1111/j.1365-2427.2007.01850.x
  14. Gregson S, Clifton S, Roberts RD. Plants as bioindicators of natural and anthropogenically derived contamination. Appl Biochem Biotechnol 1994;48:15-22. https://doi.org/10.1007/BF02825354
  15. Lee S, Hung R, Schink A, Mauro J, Bennett JW. Arabidopsis thaliana for testing the phytotoxicity of volatile organic compounds. Plant Growth Regul 2014;74:177-86. https://doi.org/10.1007/s10725-014-9909-9
  16. Borjesson T, Stollman U, Adamek P, Kaspersson A. Analysis of volatile compounds for detection of molds in stored cereals. Cereal Chem 1989;66:300-4.
  17. Chambers ST, Syhre M, Murdoch DR, McCartin F, Epton MJ. Detection of 2-pentylfuran in the breath of patients with Aspergillus fumigatus. Med Mycol 2009;47:468-76. https://doi.org/10.1080/13693780802475212
  18. Wessen B, Strom G, Palmgren U, Schoeps KO, Nilsson M. Analysis of microbial volatile organic compounds. In: Flannigan B, Samson RA, Miller, JD, editors. Microorganisms in home and indoor work environments. London: Taylor & Francis; 2001. p. 267-74.
  19. Pasanen P, Korpi A, Kalliokoski P, Pasanen AL. Growth and volatile metabolite production of Aspergillus versicolor in house dust. Environ Int 1997;23:425-32. https://doi.org/10.1016/S0160-4120(97)00027-5
  20. Gao P, Korley F, Martin J, Chen BT. Determination of unique microbial volatile organic compounds produced by five Aspergillus species commonly found in problem buildings. AIHA J (Fairfax, Va) 2002;63:135-40. https://doi.org/10.1080/15428110208984696
  21. McNeal KS, Herbert BE. Volatile organic metabolites as indicators of soil microbial activity and community composition shifts. Soil Sci Soc Am J 2009;73:579-88. https://doi.org/10.2136/sssaj2007.0245
  22. Molhave L. Volatile organic compounds and the sick building syndrome. In: Lippmann M, editor. Environmental toxicants: human exposures and their health effects, 3rd ed. New York: Wiley-Interscience; 2009. p. 241-56.
  23. Lee S, Hung R, Yap M, Bennett JW. Age matters: the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth. Arch Microbiol 2015;197:723-7. https://doi.org/10.1007/s00203-015-1104-5
  24. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 2011;13:1499-510.
  25. Juhrén M, Nobel W, Went FW. The standardization of Poa annua as an indicator of smog concentrations. I. Effects of temperature, photoperiod, and light intensity during growth of the test-plants. Plant Physiol 1957;32:576-86. https://doi.org/10.1104/pp.32.6.576
  26. Thomas MD. Gas damage to plants. Annu Rev Plant Physiol 1951;2:293-322. https://doi.org/10.1146/annurev.pp.02.060151.001453
  27. Misyura M, Colasanti J, Rothstein SJ. Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. J Exp Bot 2012;64:229-40.
  28. Kottb M, Gigolashvili T, GroBkinsky DK, Piechulla B. Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi. Front Microbiol 2015;6:995.
  29. Junker RR, Tholl D. Volatile organic compound mediated interactions at the plant-microbe interface. J Chem Ecol 2013;39:810-25. https://doi.org/10.1007/s10886-013-0325-9
  30. Heller J, Tudzynski P. Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 2011;49:369-90. https://doi.org/10.1146/annurev-phyto-072910-095355
  31. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 2003;100:4927-32. https://doi.org/10.1073/pnas.0730845100