Skip to main content
SpringerLink
Log in

Neuropharmacological Alterations by a Rice Contaminant Stenotrophomonas maltophilia: a Detailed Bio-molecular and Mechanistic Landscape

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Contaminated rice is a major source of food poisoning in human communities where our earlier study showed Stenotrophomonas maltophilia, a Gram-negative bacillus, has been a major contaminant of the stored rice. In the present study, mono- and di-unsaturated fatty acids (UFAs) such as 18:1 ω 7 c, 16:1 ω 6 c, 16:1 ω 7 c, and 18:2 ω 6,9 c long-chain fatty acids have been found as the chief constituents of S. maltophilia boiled cell lysate. Throughout the study, both acute and chronic exposure of the cell lysate showed a decrease in the locomotor activity and a time-dependent increase of the depression (p < 0.001–0.0001, two-way ANOVA), supported by bioamine (dopamine, noradrenaline, adrenaline, serotonin, and GABA) depletion in rodents’ brain possibly due to UFA-amino acid decarboxylase interaction favoring bioamine depletion as revealed by our study. Furthermore, the UFA-rich cell lysate revealed dose-dependent inhibition of murine brain microglial cell viability in vitro with concomitant increase of reactive oxygen species (ROS) inside the cell. Destruction of neuroprotective and neurotrophin releasing microglial cells, augmentation of brain ROS, and inflaming brain tissue resulting in infiltration of polymorphonuclear leucocytes also suggest to cause neurotoxicity by UFA derived from Stenotrophomonas maltophilia.

Graphical abstract

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Availability of Data and Materials

All data and materials support published claims and comply with field standards.

References

  1. Kumar, D., & Kalita, P. (2017). Reducing postharvest losses during storage of grain crops to strengthen food security in developing countries. Foods., 6, 1–22.

    Article  Google Scholar 

  2. Abedin, M. Z., Rahman, M. Z., Mia, M. I. A., & Rahman, K. M. M. (2012). In-store losses of rice and ways of reducing such losses at farmers’ level: An assessment in selected regions of Bangladesh. J. Bangladesh. Agri. Univ., 10, 133–144.

    Article  Google Scholar 

  3. Baumgardner, D. J. (2012). Soil-related bacterial and fungal infections. Journal of the American Board of Family Medicine, 25, 734–744.

    Article  Google Scholar 

  4. Leyva Salas, M., Mounier, J., Valence, F., Coton, M., Thierry, A., & Coton, E. (2017). Antifungal microbial agents for food biopreservation—A review. Microorganisms., 5, 1–35.

    Article  Google Scholar 

  5. Food Safety-World Health Organization. Available from: https://www.who.int/news-room/fact-sheets/detail/food-safety. Accessed March 15, 2019.

  6. Chattopadhyay, M., Das, D., Das, D., Gupta, M., & Bagchi, G. (2018). Assessment of hematological and biochemical effects of acute and chronic administration of the Stenotrophomonas maltophilia lysates in mice. Journal of Microbiology, Biotechnology and Food Sciences, 8, 936–939.

    Article  Google Scholar 

  7. Lin, C. M., Fernando, S. Y., & Wei, C. (1996). Occurrence of Listeria monocytogenes, Salmonella spp., Escherichia coli and E. coli O157:H7 in vegetable salads. Food Control, 7, 135–140.

    Article  CAS  Google Scholar 

  8. Zhu, B., Liu, H., Tian, W. X., Fan, X. Y., Li, B., Zhou, X. P., Jin, G., & Xie, G. (2018). Genome sequence of Stenotrophomonas maltophilia RR-10, isolated as an endophyte from rice root. Journal of Bacteriology, 194, 1280–1291.

    Article  Google Scholar 

  9. Denton, M., & Kerr, K. G. (1998). Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clinical Microbiology Reviews, 11, 57–80.

    Article  CAS  Google Scholar 

  10. Steinmann, J., Mamat, U., Abda, E., Kirchhoff, L., Streit, W., Schaible, U., Niemann, S., & Kohl, T. (2018). Analysis of phylogenetic variation of Stenotrophomonas maltophilia reveals human-specific branches. Frontiers in Microbiology, 9, 1–10.

    Article  Google Scholar 

  11. O’Leary, W. M. (1962). The fatty acids of bacteria. Bacteriological Reviews, 26, 421–447.

    Article  Google Scholar 

  12. Sekora, N. S., Lawrence, K. S., Agudelo, P., Santen, E., & McInroy, J. A. (2009). Using FAME analysis to compare, differentiate, and identify multiple nematode species. Journal of Nematology, 41, 163–173.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Jayasree, T., Naveen, A., Chandrasekhar, N., Sunil, M., Kishan, P., & Rao, N. (2012). Evaluation of muscle relaxant activity of aqueous extract of Sapindustri foliatus (pericarp) in Swiss albino mice. J. Chem. Pharm. Res, 4, 1960–1964.

    Google Scholar 

  14. Can, A., Dao, D. T., Arad, M., Terrillion, C. E., Piantadosi, S. C., & Gould, T. D. (2012). The mouse forced swim test. Journal of Visualized Experiments, 59, 1–5.

    Google Scholar 

  15. Atack, C. V. (1973). The determination of dopamine by a modification of the dihydroxyindolefluorimetric assay. British Journal of Pharmacology, 48, 699–714.

    Article  CAS  Google Scholar 

  16. Carmona, E., Gomes, C., & Trolin, G. (1980). Purification of GABA on small columns of Dowex 50 w; combination with a method for separation of biogenic amines. Acta Pharmacologica et Toxicologica, 46, 235–240.

    Article  CAS  Google Scholar 

  17. Drury, R. A., Wallington, E. A., & Cameron, R. (1967). Carlton’s histological technique (4th ed.). Oxford University Pres.

    Google Scholar 

  18. Alturkistani, H. A., Tashkandi, F. M., & Mohammedsaleh, Z. M. (2016). Histological stains: A literature review and case study. Glob. J. Health Sci., 8, 72–79.

    Article  Google Scholar 

  19. Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011). Brain–gut–microbe communication in health and disease. Frontiers in Physiology, 2, 94–105.

    Article  Google Scholar 

  20. Barret, A.D.T. and Stanberry, L. (2009). Vaccine adjuvants. Vaccines for biodefense and emerging and neglected diseases. 1st ed.; Academic Press, Cambridge, Massachusetts.

  21. Ryan, J. (2004). Endotoxins and cell culture. Corning Life Sci. Tech. Bull. 1–8.

  22. Figuera-Losada, M., Rojas, C., & Slusher, B. S. (2014). Inhibition of microglia activation as a phenotypic assay in early drug discovery. Journal of Biomolecular Screening, 19, 17–31.

    Article  CAS  Google Scholar 

  23. Kelly, M. A., Rubinstein, M., Phillips, T. J., Lessov, C. N., Burkhart-Kasch, S., Zhang, G., Bunzow, J. R., Fang, Y., Gerhardt, G. A., Grandy, D. K., & Low, M. J. (1998). Locomotor activity in D2 dopamine receptor-deficient mice is determined by gene dosage, genetic background, and developmental adaptations. Journal of Neuroscience, 18, 3470–3479.

    Article  CAS  Google Scholar 

  24. Krishnan, V., & Nestler, E. J. (2011). Models of depression: Molecular perspectives Curr. Top. Behav. Neurosci., 7, 121–147.

    Article  Google Scholar 

  25. Jacobsen, J. P., Medvedev, I. O., & Caron, M. G. (2012). The 5-HT deficiency theory of depression: Perspectives from a naturalistic 5-HT deficiency model, the tryptophan hydroxylase 2Arg439His knockin mouse. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 367, 2444–2459.

    Article  CAS  Google Scholar 

  26. Luscher, B., Shen, Q., & Sahir, N. (2011). The GABAergic deficit hypothesis of major depressive disorder. Molecular Psychiatry, 16, 383–406.

    Article  CAS  Google Scholar 

  27. Fogaca, M. V., & Duman, R. S. (2019). Cortical GABAergic dysfunction in stress and depression: New insights for therapeutic interventions. Frontiers in Cellular Neuroscience, 13, 87. https://doi.org/10.3389/fncel.2019.00087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cryan, J. F., & Slattery, D. A. (2010). GABAB receptors and depression. Current status. Adv. Pharmacol., 58, 427–451.

    Article  CAS  Google Scholar 

  29. Kobayashi, K. (2001). Role of catecholamine signaling in brain and nervous system functions: New insights from mouse molecular genetic study. The Journal of Investigative Dermatology, 6, 115–121.

    CAS  PubMed  Google Scholar 

  30. Nicolson, G. L. (2008). Chronic bacterial and viral infections in neurodegenerative and neurobehavioural disease. Laboratoriums Medizin, 39, 1–5.

    Google Scholar 

  31. Precht, W., & Yoshida, M. (1971). Blockage of caudate-evoked inhibition of neurons in the substantia nigra by picrotoxin. Brain Research, 32, 229–233.

    Article  CAS  Google Scholar 

  32. Chen, Y., Garcia, G. E., Huang, W., & Constantini, S. (2014). The involvement of secondary neuronal damage in the development of neuropsychiatric disorders following brain insults. Frontiers in Neuroscience, 5, 22–26.

    Google Scholar 

  33. Menniti, F. S., & Diliberto, J. E., Jr. (1989). Newly synthesized dopamine as the precursor for norepinephrine synthesis in bovine adrenomedullary chromaffin cells. Journal of Neurochemistry, 53, 890–897.

    Article  CAS  Google Scholar 

  34. Hallenbeck, J. M., Dutka, A. J., Tanishima, T., Kochanek, P. M., Kumaroo, K. K., Thompson, C. B., Obrenovitch, T. P., & Contreras, T. J. (1986). Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke, 17, 246–253.

    Article  CAS  Google Scholar 

  35. Liu, Y. W., Li, S., & Dai, S. S. (2018). Neutrophils in traumatic brain injury (TBI): Friend or foe? Journal of Neuroinflammation, 15, 1–18.

    Article  Google Scholar 

Download references

Acknowledgements

We are thankful to the NCCS (National Centre for Cell Science), Pune, India, for helping us in finding the free fatty acid present in bacteria and Bose Institute, Kolkata, India, to carry out the analytical work in their Central Instrumentation Facility. We are also thankful to the CPCSEA approved animal house of Dr. B.C. Roy College of Pharmacy & Allied Health Sciences, Durgapur, WB, India, for providing us the facility for conducting the animal studies in the research.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Science and Technology, Maulana Abul Kalam Azad University of Technology, Kalyani, Nadia, West Bengal, India

    Moitreyee Chattopadhyay

  2. Department of Pharmaceutical Technology, Dr. B.C. Roy College of Pharmacy & Allied Health Sciences, Durgapur, West Bengal, India

    Souvik Basak, Dibyajyoti Das & Tanushree Karmakar

  3. Chittaranjan National Cancer Institute, Kolkata, West Bengal, India

    Atish Barua

  4. Emeritus Professor, Department of Pharmaceutical Technology, Jadavpur University, Kolkata, West Bengal, India

    Malaya Gupta

  5. Department of Pharmacology, Techno India College of Pharmacy, Kolkata, West Bengal, India

    Gautam Kumar Bagchi

Authors
  1. Moitreyee Chattopadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Souvik Basak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atish Barua
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Malaya Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dibyajyoti Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tanushree Karmakar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gautam Kumar Bagchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Experimental investigations (animal studies, bioamine determination)—Moitreyee Chattopadhyay, Dibyajyoti Das; work plan and conceptualization, molecular docking analyses, bioamine determination—Souvik Basak; data interpretation, original writing—Moitreyee Chattopadhyay, Souvik Basak; cell culture assays, data interpretation—Atish Barua; planning and guiding—Malaya Gupta, Gautam Kumar Bagchi; statistical analyses—Tanushree Karmakar.

Corresponding authors

Correspondence to Moitreyee Chattopadhyay or Souvik Basak.

Ethics declarations

Ethics Approval

The experimentation on laboratory animals was conducted according to the regulations of Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA) in India and the protocol was approved by Institutional Animal Ethics Committee of Dr. B.C. Roy College of Pharmacy and Allied Sciences, Durgapur, India (Approval Number: BCRCP/IAEC/1/2014).

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Competing Interests

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 54.4 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chattopadhyay, M., Basak, S., Barua, A. et al. Neuropharmacological Alterations by a Rice Contaminant Stenotrophomonas maltophilia: a Detailed Bio-molecular and Mechanistic Landscape. Appl Biochem Biotechnol 194, 1955–1980 (2022). https://doi.org/10.1007/s12010-022-03810-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-03810-1

Keywords

Search

Navigation