Skip to main content
Log in

Effects of crude oil and aromatic compounds on growth and bioluminescence of Vibrio campbellii FS5

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Fifteen native luminescent bacteria were isolated from the Gulf of Thailand, and their sensitivity for the detection of toxicity of crude oil and its aromatic components was investigated. Of these isolates, Vibrio campbellii strain FS5 was one of the two most highly inhibited bacteria at all crude oil concentrations. This bacterium showed a decrease in luminescence intensity of between 10.7 and 80.2% after a 15-min exposure to 0.0001–10 mg/L of crude oil. The degree of bioluminescence inhibition increased with increasing concentrations of crude oil. The presence of crude oil at all concentrations had negative effects on the log bioluminescence per log number of viable cells after 15- to 105-min exposure. About 10 to 100 times, lower half maximal effective concentration (EC50) values were observed for polycyclic aromatic hydrocarbons (PAHs) than those for benzene, toluene, ethylbenzene, and xylene (BTEX). In the presence of each individual BTEX and PAH, the bioluminescence inhibition increased with increasing exposure time (1–32 h). This indigenous bacterium can be used as a simple and general indicator of oil contamination and its impact on coastal waters as well as for assessing potential toxicity during oil bioremediation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  • Daghighi, S., Sjollema, J., Harapanahalli, A., Dijkstra, R. J. B., van der Mei, H. C., & Busscher, H. J. (2015). Influence of antibiotic pressure on bacterial bioluminescence, with emphasis on Staphylococcus aureus. International Journal of Antimicrobial Agents, 46(6), 713–717.

    Article  CAS  Google Scholar 

  • Dunn, A. K., Rader, B. A., Stabb, E. V., & Mandel, M. J. (2015). Regulation of bioluminescence in Photobacterium leiognathi strain KNH6. Journal of Bacteriology, 197, 515–524.

    Article  Google Scholar 

  • El-Alawi, Y. S., Dixon, D. G., & Greenberg, B. M. (2001). Effects of a pre-incubation period on the photoinduced toxicity of polycyclic aromatic hydrocarbons to the luminescent bacterium Vibrio fischeri. Environmental Toxicology, 16(3), 277–286.

    Article  CAS  Google Scholar 

  • El-Alawi, Y. S., Huang, X. D., Dixon, D. G., & Greenberg, B. M. (2002a). Quantitative structure-activity relationship for the photoinduced toxicity of polycyclic aromatic hydrocarbons to the luminescent bacteria Vibrio fischeri. Environmental Toxicology and Chemistry, 21(10), 2225–2232.

    CAS  Google Scholar 

  • El-Alawi, Y. S., McConkey, B. J., George Dixon, D., & Greenberg, B. M. (2002b). Measurement of short- and long-term toxicity of polycyclic aromatic hydrocarbons using luminescent bacteria. Ecotoxicology and Environmental Safety, 51(1), 12–21.

    Article  CAS  Google Scholar 

  • Fernández, M. D., Cagigal, E., Vega, M. M., Urzelai, A., Babín, M., Pro, J., & Tarazona, J. V. (2005). Ecological risk assessment of contaminated soils through direct toxicity assessment. Ecotoxicology and Environmental Safety, 62(2), 174–184.

    Article  Google Scholar 

  • Frischer, M. E., Danforth, J. M., Foy, T. F., & Juraske, R. (2005). Bioluminescent bacteria as indicators of chemical contamination of coastal waters. Journal of Environmental Quality, 34(4), 1328–1336.

    Article  CAS  Google Scholar 

  • Fulladosa, E., Murat, J. C., & Villaescusa, I. (2005). Effect of cadmium(II), chromium(VI), and arsenic(V) on long-term viability- and growth-inhibition assays using Vibrio fischeri marine bacteria. Archives of Environmental Contamination and Toxicology, 49(3), 299–306.

    Article  CAS  Google Scholar 

  • Funao, H., Ishii, K., Nagai, S., Sasaki, A., Hoshikawa, T., Aizawa, M., Okada, Y., Chiba, K., Koyasu, S., Toyama, Y., & Matsumoto, M. (2012). Establishment of a real-time, quantitative, and reproducible mouse model of Staphylococcus osteomyelitis using bioluminescence imaging. Infection and Immunity, 80, 733–741.

    Article  CAS  Google Scholar 

  • Galluzzi, L., & Karp, M. (2007). Intracellular redox equilibrium and growth phase affect the performance of luciferase-based biosensors. Journal of Biotechnology, 127(2), 188–198.

    Article  CAS  Google Scholar 

  • Hartnik, T., Norli, H. R., Eggen, T., & Breedveld, G. D. (2007). Bioassay-directed identification of toxic organic compounds in creosote-contaminated groundwater. Chemosphere, 66(3), 435–443.

    Article  CAS  Google Scholar 

  • Hirmann, D., Loibner, A. P., Braun, R., & Szolar, O. H. J. (2007). Applicability of the bioluminescence inhibition test in the 96-well microplate format for PAH-solutions and elutriates of PAH-contaminated soils. Chemosphere, 67(6), 1236–1242.

    Article  CAS  Google Scholar 

  • ISO. (2007). 11348–3: Water quality: Determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (Luminiscent Bacteria Test). International Organization for Standardization..

    Google Scholar 

  • Kaiser, K. L. E., & Palabrica, V. S. (1991). Photobacterium phosphoreum toxicity data index. Water Quality Research Journal, 26(3), 361–431.

    Article  CAS  Google Scholar 

  • Kang, H.-J., Lee, S.-Y., Roh, J.-Y., Yim, U. H., Shim, W. J., & Kwon, J.-H. (2014). Prediction of ecotoxicity of heavy crude oil: Contribution of measured components. Environmental Science & Technology, 48(5), 2962–2970.

    Article  CAS  Google Scholar 

  • Kasiotis, K. M., & Emmanouil, C. (2015). Advanced PAH pollution monitoring by bivalves. Environmental Chemistry Letters, 13(4), 395–411.

    Article  CAS  Google Scholar 

  • Khan, M. I., Cheema, S. A., Shen, C., Zhang, C., Tang, X., Shi, J., Chen, X., Park, J., & Chen, Y. (2012). Assessment of phenanthrene bioavailability in aged and unaged soils by mild extraction. Environmental Monitoring and Assessment, 184(1), 549–559.

    Article  CAS  Google Scholar 

  • Lee, S.-Y., Kang, H.-J., & Kwon, J.-H. (2013). Toxicity cutoff of aromatic hydrocarbons for luminescence inhibition of Vibrio fischeri. Ecotoxicology and Environmental Safety, 94, 116–122.

    Article  CAS  Google Scholar 

  • Loibner, A. P., Szolar, O. H. J., Braun, R., & Hirmann, D. (2004). Toxicity testing of 16 priority polycyclic aromatic hydrocarbons using Lumistox®. Environmental Toxicology and Chemistry, 23(3), 557–564.

    Article  CAS  Google Scholar 

  • Marín, F., Navarrete, H., & Narvaez-Trujillo, A. (2018). Total petroleum hydrocarbon degradation by endophytic fungi from the Ecuadorian Amazon. Advances in Microbiology, 8(12), 1029–1053.

    Article  Google Scholar 

  • Marques, C. N., Salisbury, V. C., Greenman, J., Bowker, K. E., & Nelson, S. M. (2005). Discrepancy between viable counts and light output as viability measurements, following ciprofloxacin challenge of self-bioluminescent Pseudomonas aeruginosa biofilms. The Journal of antimicrobial chemotherapy, 56(4), 665–671.

    Article  CAS  Google Scholar 

  • Maruyama, A., Ishiwata, H., Kitamura, K., Sunamura, M., Fujita, T., Matsuo, M., & Higashihara, T. (2003). Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill. Microbial Ecology, 46(4), 442–453.

    Article  CAS  Google Scholar 

  • Medvedeva, S. E., Tyulkova, N. A., Kuznetsov, A. M., & Rodicheva, E. K. (2009). Bioluminescent bioassays based on luminous bacteria. Journal of Siberian Federal University, 2(3), 418–452..

    Google Scholar 

  • Mirjani, M., Soleimani, M., & Salari, V. (2021). Toxicity assessment of total petroleum hydrocarbons in aquatic environments using the bioluminescent bacterium Aliivibrio fischeri. Ecotoxicology and Environmental Safety, 207, 111554.

    Article  CAS  Google Scholar 

  • Munkittrick, K. R., Power, E. A., & Sergy, G. A. (1991). The relative sensitivity of MicrotoxTM, Daphnid, rainbow trout and fathead min- now acute lethality tests. Environmental Toxicology and Water Quality, 6, 35–62.

    Article  CAS  Google Scholar 

  • Nealson, K. H. (1978). Isolation, identification, and manipulation of luminous bacteria. Methods in Enzymology, 57, 153–166.

    Article  CAS  Google Scholar 

  • Nyholm, S. v, & McFall-Ngai, M. (2004). The winnowing: establishing the squid–vibrio symbiosis. Nature Reviews Microbiology, 2(8), 632–642..

    Article  CAS  Google Scholar 

  • Ossai, I. C., Ahmed, A., Hassan, A., & Hamid, F. S. (2020). Remediation of soil and water contaminated with petroleum hydrocarbon: A review. Environmental Technology & Innovation, 17, 100526.

    Article  Google Scholar 

  • Parvez, S., Venkataraman, C., & Mukherji, S. (2006). A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environment International, 32(2), 265–268.

    Article  CAS  Google Scholar 

  • Pongpiachan, S., Hattayanone, M., Tipmanee, D., Suttinun, O., Khumsup, C., Kittikoon, I., & Hirunyatrakul, P. (2018). Chemical characterization of polycyclic aromatic hydrocarbons (PAHs) in 2013 Rayong oil spill-affected coastal areas of Thailand. Environmental Pollution, 233, 992–1002.

    Article  CAS  Google Scholar 

  • Ren, S., & Frymier, P. D. (2005). Toxicity of metals and organic chemicals evaluated with bioluminescence assays. Chemosphere, 58(5), 543–550.

    Article  CAS  Google Scholar 

  • Siddig, A. A. H., Ellison, A. M., Ochs, A., Villar-Leeman, C., & Lau, M. K. (2016). How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecological Indicators, 60, 223–230.

    Article  Google Scholar 

  • Sverdrup, L. E., Nielsen, T., & Krogh, P. H. (2002). Soil ecotoxicity of polycyclic aromatic hydrocarbons in relation to soil sorption, lipophilicity, and water solubility. Environmental Science & Technology, 36(11), 2429–2435.

    Article  CAS  Google Scholar 

  • Tanet, L., Tamburini, C., Baumas, C., Garel, M., Simon, G., & Casalot, L. (2019). Bacterial bioluminescence: Light emission in Photobacterium phosphoreum is not under quorum-sensing control. Frontiers in microbiology, 10, 365.

    Article  Google Scholar 

  • Thailand Marine Department. (2013–2019). Reports of oil spill incidents. http://www.md.go.th. Accessed 1 Jul 2020.

  • Tsybulskii, I. E., & Sazykina, M. A. (2010). New biosensors for assessment of environmental toxicity based on marine luminescent bacteria. Applied Biochemistry and Microbiology, 46(5), 505–510.

    Article  CAS  Google Scholar 

  • Verbruggen, E. M. J. (2012). Environmental risk limits for polycyclic aromatic hydrocarbons (PAHs) For direct aquatic, benthic, and terrestrial toxicity. National Institute for Public Health and the Environment, Netherlands. https://www.rivm.nl/bibliotheek/rapporten/607711007.pdf. Accessed 3 Jul 2020.

  • Wang, L., Chen, Y., Huang, H., Huang, Z., Chen, H., & Shao, Z. (2015). Isolation and identification of Vibrio campbellii as a bacterial pathogen for luminous vibriosis of Litopenaeus vannamei. Aquaculture Research, 46(2), 395–404.

    Article  CAS  Google Scholar 

  • Wang, Y., Liu, M., Dai, Y., Luo, Y., & Zhang, S. (2021). Health and ecotoxicological risk assessment for human and aquatic organism exposure to polycyclic aromatic hydrocarbons in the Baiyangdian Lake. Environmental Science and Pollution Research, 28(1), 574–586.

    Article  CAS  Google Scholar 

  • Wang, Y., Yang, X., Wang, J., Cong, Y., Mu, J., & Jin, F. (2016). A DFT-based toxicity QSAR study of aromatic hydrocarbons to Vibrio fischeri: Consideration of aqueous freely dissolved concentration. Journal of Hazardous Materials, 308, 149–156.

    Article  CAS  Google Scholar 

  • Wolska, L., Mechlińska, A., Rogowska, J., & Namieśnik, J. (2012). Sources and fate of PAHs and PCBs in the marine environment. Critical Reviews in Environmental Science and Technology, 42(11), 1172–1189.

    Article  CAS  Google Scholar 

  • Yano, Y., Hamano, K., Satomi, M., Tsutsui, I., Ban, M., & Aue-umneoy, D. (2014). Prevalence and antimicrobial susceptibility of Vibrio species related to food safety isolated from shrimp cultured at inland ponds in Thailand. Food Control, 38, 30–36.

    Article  Google Scholar 

  • Yi, X., Gao, Z., Liu, L., Zhu, Q., Hu, G., & Zhou, X. (2020). Acute toxicity assessment of drinking water source with luminescent bacteria: Impact of environmental conditions and a case study in Luoma Lake, East China. Frontiers of Environmental Science & Engineering, 14(6), 109.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Center of Excellence on Hazardous Substance Management (HSM) for their invaluable support in terms of facilities and scientific equipment.

Funding

This research was supported by the Office of Higher Education Commission (OHEC) and the S&T Postgraduate Education and Research Development Office (PERDO) (contract no. HSM-PJ-CT-17–01). Support was also provided by the Postdoctoral Fellowship from Prince of Songkla University.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, Methodology, Investigation, Formal analysis, Data curation, Writing—original draft: Suriya Palamae; Supervision, Funding acquisition: Penjai Sompongchaiyakul; Supervision, Conceptualization, Methodology, Resources, Data curation, Writing—original draft, Writing—review and editing, Funding acquisition: Oramas Suttinun.

Corresponding author

Correspondence to Oramas Suttinun.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 281 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Palamae, S., Sompongchaiyakul, P. & Suttinun, O. Effects of crude oil and aromatic compounds on growth and bioluminescence of Vibrio campbellii FS5. Environ Monit Assess 193, 291 (2021). https://doi.org/10.1007/s10661-021-09081-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-021-09081-3

Keywords

Navigation