Skip to main content
Log in

Toxic effect of sodium perfluorononyloxy-benzenesulfonate on Pseudomonas stutzeri in aerobic denitrification, cell structure and gene expression

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

The toxicities of sodium perfluorononyloxy-benzenesulfonate (OBS) to animals and plants are similar to those of perfluorooctane sulfonate. However, the mechanism of its toxicity to aerobic denitrifying bacteria is still unclear. In the present study, the ecotoxicity of OBS on an aerobic denitrifying strain, Pseudomonas stutzeri, was evaluated. The results showed that a dosage of OBS clearly affected the growth and aerobic denitrification of P. stutzeri. When compared with an unamended control, the degradation efficiency of the total nitrogen decreased by 30.13% during exposure to 200 mg/L of OBS, and the complete degradation time of nitrate-nitrogen was delayed by 4 h. The lactate dehydrogenase and superoxide dismutase produced by the bacteria increased with the concentration of OBS, and reactive oxygen species were also detected by confocal laser scanning microscope imaging. Transmission electron microscope imaging revealed chromosome deformation of the cells and damage to cell content; moreover, outer membrane vesicles were secreted from the bacteria, which was the important detoxification mechanism of P. stutzeri to OBS. Expression of the genes involved in aerobic nitrification and oxidative stress were also changed under OBS stress, which further confirmed the toxicity of OBS to P stutzeri. This study reveals the environmental exposure risk of OBS from the perspective of microorganisms.

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.

Similar content being viewed by others

References

  • Bao Y, Qu Y, Huang J, Cagnetta G, Yu G, Weber R (2017). First assessment on degradability of sodium p-perfluorous nonenoxybenzene sulfonate (OBS), a high volume alternative to perfluorooctane sulfonate in fire-fighting foams and oil production agents in China. RSC Advances, 7(74): 46948–46957

    Article  CAS  Google Scholar 

  • Beveridge T J (1999). Structures of gram-negative cell walls and their derived membrane vesicles. Journal of Bacteriology, 181(16): 4725–4733

    Article  CAS  Google Scholar 

  • Chen D, Xiao Z, Wang H, Yang K (2018). Toxic effects of vanadium (V) on a combined autotrophic denitrification system using sulfur and hydrogen as electron donors. Bioresource Technology, 264: 319–326

    Article  CAS  Google Scholar 

  • Chen H, Yao J, Wang F, Cai M, Liu H (2013). Toxicity of perfluorooctanoic acid to Pseudomonas putida in the aquatic environment. Journal of Hazardous Materials, 262: 726–731

    Article  CAS  Google Scholar 

  • Chen L, Tsui M M P, Lam J C W, Wang Q, Hu C, Wai O W H, Zhou B, Lam P K S (2019). Contamination by perfluoroalkyl substances and microbial community structure in Pearl River Delta sediments. Environmental Pollution, 245: 218–225

    Article  CAS  Google Scholar 

  • Chen Q, Li T, Gui M, Liu S, Zheng M, Ni J (2017). Effects of ZnO nanoparticles on aerobic denitrification by strain Pseudomonas stutzeri PCN-1. Bioresource Technology, 239: 21–27

    Article  CAS  Google Scholar 

  • Cortez N, Carrillo N, Pasternak C, Balzer A, Klug G (1998). Molecular cloning and expression analysis of the Rhodobacter capsulatus sodB gene, encoding an iron superoxide dismutase. Journal of Bacteriology, 180(20): 5413–5420

    Article  CAS  Google Scholar 

  • Durán N, Durán M, De Jesus M B, Seabra A B, Favaro W J, Nakazato G (2016). Silver nanoparticles: A new view on mechanistic aspects on antimicrobial activity. Nanomedicine; Nanotechnology, Biology, and Medicine, 12(3): 789–799

    Article  Google Scholar 

  • Ellis T N, Kuehn M J (2010). Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiology and Molecular Biology Reviews, 74(1): 81–94

    Article  CAS  Google Scholar 

  • Giesy J P, Kannan K (2002). Peer reviewed: Perfluorochemical surfactants in the environment. Environmental Science & Technology, 36(7): 146A–152A

    Article  CAS  Google Scholar 

  • Gill S S, Tuteja N (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12): 909–930

    Article  CAS  Google Scholar 

  • Gui M, Chen Q, Ma T, Zheng M, Ni J (2017a). Effects of heavy metals on aerobic denitrification by strain Pseudomonas stutzeri PCN-1. Applied Microbiology and Biotechnology, 101(4): 1717–1727

    Article  CAS  Google Scholar 

  • Gui M, Chen Q, Ni J (2017b). Effect of sulfamethoxazole on aerobic denitrification by strain Pseudomonas stutzeri PCN-1. Bioresource Technology, 235: 325–331

    Article  CAS  Google Scholar 

  • Hartop K R, Sullivan M J, Giannopoulos G, Gates A J, Bond P L, Yuan Z, Clarke T A, Rowley G, Richardson D J (2017). The metabolic impact of extracellular nitrite on aerobic metabolism of Paracoccus denitrificans. Water Research, 113: 207–214

    Article  CAS  Google Scholar 

  • Ighodaro O M, Akinloye O A (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine, 54(4): 287–293

    Article  Google Scholar 

  • Jia R, Han C, Lei J L, Liu B L, Huang B, Huo H H, Yin S T (2015). Effects of nitrite exposure on haematological parameters, oxidative stress and apoptosis in juvenile turbot (Scophthalmus maximus). Aquatic Toxicology (Amsterdam, Netherlands), 169: 1–9

    Article  CAS  Google Scholar 

  • Ke Y, Chen J, Hu X, Tong T, Huang J, Xie S (2020). Emerging perfluoroalkyl substance impacts soil microbial community and ammonia oxidation. Environmental Pollution, 257: 113615

    Article  CAS  Google Scholar 

  • Kobayashi H, Uematsu K, Hirayama H, Horikoshi K (2000). Novel toluene elimination system in a toluene-tolerant microorganism. Journal of Bacteriology, 182(22): 6451–6455

    Article  CAS  Google Scholar 

  • Li C (2016). Contamination Characteristics of F-53B, OBS and Other Poly- and Per Fluoroalky Substances in Typical Areas. Master Dissertation. Qingdao: Qingdao Technological University (in Chinese)

    Google Scholar 

  • Liao T T, Shi Y L, Jia J W, Jia R W, Wang L (2010). Sensitivity of morphological change of Vero cells exposed to lipophilic compounds and its mechanism. Journal of Hazardous Materials, 179(1–3): 10550–1064

    Google Scholar 

  • Liu G, Zhang S, Yang K, Zhu L, Lin D (2016). Toxicity of perfluorooctane sulfonate and perfluorooctanoic acid to Escherichia coli: Membrane disruption, oxidative stress, and DNA damage induced cell inactivation and/or death. Environmental Pollution, 214: 806–815

    Article  CAS  Google Scholar 

  • Manning A J, Kuehn M J (2011). Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiology, 11(1): 258–272

    Article  CAS  Google Scholar 

  • McBroom A J, Kuehn M J (2007). Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Molecular Microbiology, 63(2): 545–558

    Article  CAS  Google Scholar 

  • Ning H Q, Li Y Q, Tian Q W, Wang Z S, Mo H Z (2019). The apoptosis of Staphylococcus aureus induced by glycinin basic peptide through ROS oxidative stress response. Lebensmittel-Wissenschaft + Technologie, 99: 62–68

    Article  CAS  Google Scholar 

  • Özen H, Kamber U, Karaman M, Gul S, Atakisi E, Ozcan K, Atakisi O (2014). Histopathologic, biochemical and genotoxic investigations on chronic sodium nitrite toxicity in mice. Experimental and Toxicologic Pathology, 66(8): 367–375

    Article  Google Scholar 

  • Presentato A, Lampis S, Vantini A, Manea F, Dapra F, Zuccoli S, Vallini G (2020). On the ability of perfluorohexane sulfonate (PFHxS) bioaccumulation by two Pseudomonas sp. strains isolated from PFAS-contaminated environmental matrices. Microorganisms, 8(1): 92

    Article  CAS  Google Scholar 

  • Qian Y, Zhang Y, Zuh A A, Qiao W (2020). New application of rutin: Repair the toxicity of emerging perfluoroalkyl substance to Pseudomonas stutzeri. Ecotoxicology and Environmental Safety, 201: 110879

    Article  CAS  Google Scholar 

  • Qiao W, Xie Z, Zhang Y, Liu X, Xie S, Huang J, Yu L (2018). Perfluoroalkyl substances (PFASs) influence the structure and function of soil bacterial community: Greenhouse experiment. Science of the Total Environment, 642: 1118–1126

    Article  CAS  Google Scholar 

  • Qiao W, Zhang Y, Xie Z, Luo Y, Zhang X, Sang C, Xie S, Huang J (2019). Toxicity of perfluorooctane sulfonate on Phanerochaete chrysosporium: Growth, pollutant degradation and transcriptomics. Ecotoxicology and Environmental Safety, 174: 66–74

    Article  CAS  Google Scholar 

  • Qu B, Zhao H, Zhou J (2010). Toxic effects of perfluorooctane sulfonate (PFOS) on wheat (Triticum aestivum L.) plant. Chemosphere, 79(5): 555–560

    Article  CAS  Google Scholar 

  • Ruan Y, Awasthi M K, Cai L, Lu H, Xu X, Li W (2020). Simultaneous aerobic denitrification and antibiotics degradation by strain Marinobacter hydrocarbonoclasticus RAD-2. Bioresource Technology, 313: 123609

    Article  CAS  Google Scholar 

  • Slotkin T A, Mackillop E A, Melnick R L, Thayer K A, Seidler F J (2008). Developmental neurotoxicity of perfluorinated chemicals modeled in vitro. Environmental Health Perspectives, 116(6): 716–722

    Article  CAS  Google Scholar 

  • Sun Y, Feng L, Li A, Zhang X, Yang J, Ma F (2017). Ammonium assimilation: An important accessory during aerobic denitrification of Pseudomonas stutzeri T13. Bioresource Technology, 234: 264–272

    Article  CAS  Google Scholar 

  • Tang Y, Li M, Xu D, Huang J, Sun J (2018). Application potential of aerobic denitrifiers coupled with a biostimulant for nitrogen removal from urban river sediment. Environmental Science and Pollution Research International, 25(6): 5980–5993

    Article  CAS  Google Scholar 

  • Xu L, Krenitsky D M, Seacat A M, Butenhoff J L, Anders M W (2004). Biotransformation of N-ethyl-N-(2-hydroxyethyl)perfluorooctane-sulfonamide by rat liver microsomes, cytosol, and slices and by expressed rat and human cytochromes P450. Chemical Research in Toxicology, 17(6): 767–775

    Article  CAS  Google Scholar 

  • Yang J, Feng L, Pi S, Cui D, Ma F, Zhao H P, Li A (2020a). A critical review of aerobic denitrification: Insights into the intracellular electron transfer. Science of the Total Environment, 731: 139080

    Article  CAS  Google Scholar 

  • Yang T, Xin Y, Zhang L, Gu Z, Li Y, Ding Z, Shi G (2020b). Characterization on the aerobic denitrification process of Bacillus strains. Biomass and Bioenergy, 140: 105677

    Article  CAS  Google Scholar 

  • Yang X, Ye C, Liu Y, Zhao F J (2015). Accumulation and phytotoxicity of perfluorooctanoic acid in the model plant species Arabidopsis thaliana. Environmental Pollution, 206: 560–566

    Article  CAS  Google Scholar 

  • Zhang M, Li A, Yao Q, Wu Q, Zhu H (2020). Nitrogen removal characteristics of a versatile heterotrophic nitrifying-aerobic denitrifying bacterium, Pseudomonas bauzanensis DN13-1, isolated from deep-sea sediment. Bioresource Technology, 305: 122626

    Article  CAS  Google Scholar 

  • Zheng X, Su Y, Chen Y, Wan R, Liu K, Li M, Yin D (2014). Zinc oxide nanoparticles cause inhibition of microbial denitrification by affecting transcriptional regulation and enzyme activity. Environmental Science & Technology, 48(23): 13800–13807

    Article  CAS  Google Scholar 

  • Zhou S, Zhang Y, Huang T, Liu Y, Fang K, Zhang C (2019). Microbial aerobic denitrification dominates nitrogen losses from reservoir ecosystem in the spring of Zhoucun Reservoir. Science of the Total Environment, 651: 998–1010

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the Natural Science Foundation of Jiangsu Province (BK20201388) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weichuan Qiao.

Ethics declarations

The authors declare that they have no competing interests.

Additional information

Highlights

• OBS inhibited the growth of P. stutzeri and destroyed its structure.

• OBS was toxic to the aerobic denitrification process of P. stutzeri.

• OBS induced the production of ROS in P. stutzeri.

• OBS affected the expression of key genes involved in denitrification and SOD.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qian, Y., Qiao, W. & Zhang, Y. Toxic effect of sodium perfluorononyloxy-benzenesulfonate on Pseudomonas stutzeri in aerobic denitrification, cell structure and gene expression. Front. Environ. Sci. Eng. 15, 100 (2021). https://doi.org/10.1007/s11783-021-1391-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-021-1391-9

Keywords

Speciality

Navigation