Skip to main content
Log in

Quorum Sensing-Linked agrA Expression by Ethno-Synthesized Gold Nanoparticles in Tilapia Streptococcus agalactiae Biofilm Formation

  • Published:
BioNanoScience Aims and scope Submit manuscript

Abstract

The inevitable occurrence of diseases caused by bacterial pathogens is one of the main constraints in tilapia industry that has resulted in major economic losses. The study reveals the advantages of quorum sensing inhibition through nanotechnology in developing antivirulence drugs to control aquaculture pathogens using scientifically untapped medicinal plants, the ethnobotanicals. The ethnobotanical crude extracts (CEs) and biologically synthesized gold nanoparticles (CEs + AuNPs) of the Ilongot-Eǵongot community exhibit quorum sensing inhibition (QSI) activity through inhibition of the biofilm formation against gram-positive Streptococcus agalactiae. Furthermore, ethnobotanical CEs + AuNPs show much greater activity than its counterpart CEs in antibacterial and biofilm formation assay in S. agalactiae which is molecularly confirmed by gene expression analysis. The results indicate the potential of these ethnobotanicals for therapeutic approach in which it showed minimal expression of agrA gene linked in biofilm formation and connotes maximal inhibition of QS in S. agalactiae thereby can possibly inhibit bacterial resistance and virulence.

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

Similar content being viewed by others

References

  1. Ali, A., Hassan, D., Saleha, A. A., Siti-Khairani, B., & Milud, A. (2010). Streptococcus agalactiae the etiological agent of mass mortality in farmed red tilapia (Oreochromis sp.). Journal of Animal and Veterinary Advances, 9, 2640–2646.

    Google Scholar 

  2. Amal, M. N. A., Zamri-Saad, M., Siti-Zahrah, A., Zulkafli, R., Misri, S., Nur-Nazifah, M., & Shahidan, H. (2010). Prevalence of Streptococcus agalactiae in tilapia kept in different water bodies. Online Journal of Veterinary Research, 14, 153–162.

    Google Scholar 

  3. Balberona, A. N., Noveno, J. J., Angeles, M. G. B., Santos, R. I., & Cachin, E. (2018). Ethnomedicinal plants utilized by the Ilongot-Eǵongot community of Bayanihan, Maria Aurora, Aurora, Philippines. International Journal of Agricultural Technology, 14(2), 145–159.

    Google Scholar 

  4. Bauer, W. D., & Mathesius, U. (2004). Plant responses to bacterial quorum sensing signals. Current Opinion in Plant Biology, 7, 429–433.

    Google Scholar 

  5. Chaffin, D. O., Beres, S. B., Yim, H. H., & Rubens, C. E. (2000). The serotype of type Ia and III group B streptococci is determined by the polymerase gene within the polycistronic capsule operon. Journal of Bacteriology, 182, 4466–4477.

    Google Scholar 

  6. Daniel, M. C., & Astruc, D. (2004). Chemical Reviews, 104, 293.

    Google Scholar 

  7. Djordjevic, D., Wiedmann, M., & McLandsborough, L. A. (2002). Microtiter plate assay for assessment of listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6), 2950–2958.

  8. Dobretsov, S., Teplitski, M., Bayer, M., Gunasekera, S., Proksch, P., & Paul, V. J. (2011). Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling., 27, 893–905.

    Google Scholar 

  9. Domingo, D., & Lopez, M. (2003). Plantas con Acción Antimicrobiana (plants with antimicrobial action). Revista Espaňola de Quimioterapia, 16(4), 385–393.

  10. Dunman, P. M., Murphy, E., Haney, S., Palacios, D., Tucker-Kellogg, G., Wu, S., Brown, E. L., Zagursky, R. J., Shlaes, D., & Projan, S. J. (2001). Journal of Bacteriology., 183, 7341.

    Google Scholar 

  11. Duremdez, R., Al-Marzouk, A., Qasem, J. A., Al-Harbi, A., & Gharabally, A. (2004). Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. Journal of Fish Diseases, 27, 307–310.

    Google Scholar 

  12. Eldar, A., Bejerano, Y., Livoff, A., Horovitcz, A., & Bercovier, H. (1995). Experimental streptococcal meningo-encephalitis in cultured fish. Veterinary Microbiology, 43, 33–40.

  13. Emmanuel, R., Saravanan, M., Ovais, M., Padmavathy, S., Shinwari, Z. K., & Prakash, P. (2017). Antimicrobial efficacy of drug blended biosynthesized colloidal gold nanoparticles from Justicia glauca against oral pathogens: a nanoantibiotic approach, Microbial Pathogenesis. Journal of Micpathology. https://doi.org/10.1016/2017.10.055.

  14. Evans, J. J., Klesius, P. H., & Shoemaker, C. A. (2006). An overview of Streptococcus in warm water fish. Aquaculture Health International, 7, 10–14.

    Google Scholar 

  15. Fernando, S. I. D., & Judan Cruz, K. G. (2020). Ethnobotanical biosynthesis of gold nanoparticles and its downregulation of quorum sensing-linked AhyR gene in Aeromonas hydrophila. SN Appl. Sci, 2, 570. https://doi.org/10.1007/s42452-020-2368-1.

    Article  Google Scholar 

  16. Fernando, S. I. D., Judan-Cruz, K. G., & De Guia, A. C. M. (2017). Biologically synthesized gold nanoparticles (Aunp) using pine (Pinus kesiya) pollen extract show antifungal activity against Candida albicans. International Journal of Agricultural Technology, 13(7.3), 2615–2622.

    Google Scholar 

  17. Fleming, V., Feil, E., Sewell, A. K., Day, N., Buckling, A., & Massey, R. C. (2006). Agr interference between clinical Staphylococcus aureus strains in an insect model of virulence. Journal of Bacteriology., 188, 7686–7688.

    Google Scholar 

  18. Glaser, P., Rusniok, C., Buchrieser, C., Chevalier, F., Frangeul, L., Msadek, T., et al. (2002). Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Molecular Microbiology, 45, 1499–1513.

  19. Grossman, A. D. (1995). Annual Review of Genetics, 29, 477.

    Google Scholar 

  20. Gutiérrez-Barranquero, J. A., Jerry Reen, F., McCarthy, R. R., & O’Gara, F. (2015). Deciphering the role of coumarin as a novel quorum sensing inhibitor suppressing virulence phenotypes in bacterial pathogens. Applied Microbiology and Biotechnology, 99(7), 3303–3316.

  21. Gutowski-Eckel, Z., Klein, C., Siegers, K., Bohm, K., Hammelmann, M., & Entian, K. D. (1994). Applied Environmental Microbiology, 60, 1.

    Google Scholar 

  22. Hashimoto, M., Hirotomo, Y., Haruaki, K., Satoshi, Y., Honda, Y., & Imazato, S. (2017). Effect of metal nanoparticles on biofilm formation of Streptococcus mutans. Nano Biomedicine, 9(2), 61–68.

    Google Scholar 

  23. Hentzer, M. (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. The EMBO Journal, 22(15), 3803–3815.

  24. Kalia, V. C., Rani, A., Lal, S., Cheema, S., & Raut, C. P. (2007). Combing databases reveals potential antibiotic producers. Expert Opinion on Drug Discovery, 2(2), 211–224.

    Google Scholar 

  25. Kamat, P. V., Barazzouk, S., & Hotchandani, S. (2002). Electrochemical modulation of fluorophore emission on a nanostructured gold film. Angewandte Chemie International Edition, 10, 1002/1521–1002/3773.

    Google Scholar 

  26. Khatami, M., Heli, H., Jahani, P. M., Azizi, H., & Lima, N. M. (2017). Copper/copper oxide nanoparticles synthesis using Stachys lavandulifolia and its antibacterial activity. IET Nanobiotech., 2017, 11. https://doi.org/10.1049/iet-nbt.2016.0189.

    Article  Google Scholar 

  27. Kleerebezem, M., Quadri, L. E., Kuipers, O. P., & de Vos, W. M. (1997). Quorum sensing by peptide pheromones and two-component signal-transduction systems in gram-positive bacteria. Molecular Microbiology, 24, 895–904.

    Google Scholar 

  28. Kumar, P. S. M., MubarakAli, D., Saratale, R. G., Saratale, G. D., Pugazhendhi, A., Gopalakrishnan, K., & Thajuddin, N. (2017). Synthesis of nano-cuboidal gold particles for effective antimicrobial property against clinical human pathogens. Microbial Pathogenesis. Journal of Micropathology. doi, 10, 1016.

    Google Scholar 

  29. Lee, M. S., & Morrison, D. A. (1999). Identification of a new regulator in streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. Journal of Bacteriology, 181(16), 5004–5016.

  30. Li, Y. H., Tang, N., Aspiras, M. B., Lau, P. C., Lee, J. H., Ellen, R. P., & Cvitkovitch, D. G. (2002). Journal of Bacteriology, 184, 2699.

    Google Scholar 

  31. Li, W. R., Xie, X. B., Shi, Q. S., Duan, S. S., Ouyang, Y. S., & Chen, Y. B. (2011). 2011. Antibacterial effect of silver nanoparticles of noble metals. Biometals, 24, 135–141.

    Google Scholar 

  32. Lindahl, G., Stålhammar-Carlemalm, M., & Areschoug, T. (2005). Surface proteins of streptococcus agalactiae and related proteins in other bacterial pathogens. Clinical Microbiology Reviews, 18(1), 102–127.

  33. Mian, G. F., Godoy, D. T., Leal, C. A. G., Yuhara, T. Y., Costa, G. M., et al. (2009). Aspects of the natural history and virulence of S. agalactidae infection in Nile tilapia. Veterinary Microbiology., 136, 180–183.

    Google Scholar 

  34. Miller, S. T., Xavier, K. B., Campagna, S. R., Taga, M. E., Semmelhack, M. F., Bassler, B. L., & Hughson, F. M. (2004). Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Molecular Cell, 15, 677.

    Google Scholar 

  35. Muzquiz, J. L., Royo, F. M., Ortega, C., De Blias, I., Ruiz, I., & Alonso, J. L. (1999). Pathogenicity of streptococcosis in rainbow trout (Oncorhynchus mykiss): dependence on age of diseased ®sh. Bulletin of the European Association of Fish Pathologists, 19, 114–119.

    Google Scholar 

  36. Najiah, M., Lee, S. W., Nadirah, M., Ruhil, H., Lee, K. L., Wendy, W., Amal, M. N. A., Basiriah, M. K., & Siti-Zahrah, A. (2009). Streptococcosis in red hybrid tilapia (Oreochromis niloticus) commercial farms in Malaysia. Aquaculture Research, 40, 630–632.

    Google Scholar 

  37. Navarre, W. W., & Schneewind, O. (1999). Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiology and Molecular Biology Reviews, 63, 174–229.

    Google Scholar 

  38. Nazzaro, F., Fratianni, F., & Coppola, R. (2013). Quorum sensing and phytochemicals. International Journal of Molecular Sciences, 14(6), 12607–12619. https://doi.org/10.3390/ijms10612607.

    Article  Google Scholar 

  39. Novick, R. P., & Geisinger, E. (2008). Quorum sensing in staphylococci. Annual Review in Genetics, 42, 541–564. https://doi.org/10.1146/annurev.genet.42.110807.091640.

    Article  Google Scholar 

  40. Ong, K. S., Cheow, Y. L., & Lee, S. M. (2017). The role of reactive oxygen species in the antimicrobial activity of pyochelin. Journal of Advance Researches, 8, 393–398.

    Google Scholar 

  41. Pallen, M. J., & Wren, B. W. (2007). Bacterial pathogenomics. Nature, 449, 835–842.

    Google Scholar 

  42. Paza, C., Carcamo, G., Silva, M., Becerra, J., Urrutia, H., & Sossa, K. (2013). Drimendiol, a drimane sesquiterpene with quorum sensing inhibition activity. Natural Product Communications, 8, 147–148.

    Google Scholar 

  43. Pereira, U. P., Mian, G. F., Oliveira, I. C., Benchetrit, L. C., Costa, G. M., & Figueiredo, H. C. (2010). Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Veterinary Microbiology, 140, 186–192.

    Google Scholar 

  44. Perera, R. P., Collins, M. D., Johnson, S. K., & Lewis, D. H. (1994). Streptococcus iniae associated with mortality of Tilapia niloticus X T. aurea. Journal of Aquatic Animal Health, 6, 335–340.

    Google Scholar 

  45. Perera, R. P., Johnson, S. K., & Lewis, D. H. (1997). Epizootiological aspects of Streptococcus iniae affecting tilapia in Texas. Aquaculture, 152, 25–33.

    Google Scholar 

  46. Petersen, F. C., Pecharki, D., & Scheie, A. (2004). American Journal of Bacteriology, 186, 6327.

    Google Scholar 

  47. Pretto-Giordano, L. G., Muller, E. E., Klesius, P., & Silva, V. G. (2010). Efficacy of an experimentally inactivated Streptococcus agalactiae vaccine in Nile tilapia (Oreochromis niloticus) reared in Brazil. Aquaculture Research, 41, 1539–1544.

    Google Scholar 

  48. Pugazhendhi, A., Dhanarani, S., Shankar, C., Prakash, P., Ranganathan, K., Saratale, R. G., & Thamaraiselvi, K. (2017). Electrophoretic pattern of glutathione S-transferase (GST) in antibiotic resistance gram-positive bacteria from poultry litter. Microbial Pathogenesis, 110, 285–290.

    Google Scholar 

  49. Ramanujam, P. A., Abinaya, B., & Pandian, S. K. (2014). Phenol, 2,4-bis (1,1-dimethylethyl) of marine bacterial origin inhibits quorum sensing mediated biofilm formation in the Uropathogen Serratia marcescens. Biofouling, 30(9), 1111–1122. https://doi.org/10.1080/08927014.2014.972386.

    Article  Google Scholar 

  50. Rasmussen, T. B., & Givskov, M. (2006). Quorum sensing inhibitors: a bargain of effects. Microbiology, 152(4), 895–904.

    Google Scholar 

  51. Recsei, P., Kreiswirth, B., O’Reilly, M., Schlievert, P., Gruss, A., & Novick, R. P. (1986). Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Molecular & General Genetics, 202, 58–61.

    Google Scholar 

  52. Robinson, J. A., & Meyer, F. P. (1966). Streptococcal fish pathogen. Journal of Bacteriology, 92, 512.

    Google Scholar 

  53. Roux, A., Payne, S. M., & Gilmore, M. S. (2009). Microbial telesensing: probing the environment for friends, foes, and food. Cell Host and Microbe, 6(2), 115–124. https://doi.org/10.1016/j.chom.2009.07.004.

    Article  Google Scholar 

  54. Saravanan, M., Vemu, A. K., & Barik, S. K. (2011). Rapid biosynthesis of silver nanoparticles from bacillus megaterium (NCIM 2326) and their antibacterial activity on multi drug resistant clinical pathogens. Colloids and Surfaces. B, Biointerfaces, 88, 325–331.

    Google Scholar 

  55. Shanmuganathan, R., MubarakAli, D., Prabakar, D., Muthukumar, H., Thajuddin, N., Kumar, S. S., et al. (2017). An enhancement of antimicrobial efficacy of biogenic and ceftriaxone-conjugated silver nanoparticles: green approach. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-017-9367-9.

  56. Shoemaker C. & Klesius P. (1997) Streptococcal disease problems and control: a review. In: Tilapia aquaculture 2 (ed. by K. Fitzsimmons), pp. 671±689. Northeast regional agricultural engineering service, Ithaca, NY.

  57. Song, C., Ma, H., Zhao, Q., Song, S., & Jia, A. Z. (2012). Inhibition of quorum sensing activity by ethanol extract of Scutellaria baicalensis Georgi. Journal of Plant Pathology and Microbiology, S7, 001. https://doi.org/10.4172/2157-7471.S7-001.

    Article  Google Scholar 

  58. Suanyuk, N., Kong, F. R., Ko, D., Gilbert, G. L., & Supamattaya, K. (2008). Occurrence of rare genotypes of Streptococcus agalactiae in cultured red tilapia Oreochromis sp. and Nile tilapia O. niloticus in Thailand-Relationship to human isolates. Aquaculture, 284, 35–40.

    Google Scholar 

  59. Sully, E. K., Malachowa, N., Elmore, B. O., Alexander, S. M., Femling, J. K., et al. (2014). Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance. PLOS Pathogens Journal, 10(6), e1004174. https://doi.org/10.1371/journal.ppat.1004174.

    Article  Google Scholar 

  60. Tan, L. Y., Yin, W. F., & Chan, K. G. (2013). Piper nigrum, Piper betle and Gnetum gnemon-natural food source with anti-quorum sensing properties. Sensors, 13(3), 3975–3985.

    Google Scholar 

  61. Thoendel, M., Kavanaugh, J. S., Flack, C. E., & Horswill, A. R. (2011). Peptide signaling in the Staphylococci. Chemical Reviews, 111(1), 117–151. https://doi.org/10.1021/cr100370n.

    Article  Google Scholar 

  62. Trotonda, M. P., Manna, A. C., Cheung, A. L., Lasa, I., & Penades, J. R. (2005). Sar A positively controls bap-dependent biofilm formation in Staphylococcus auereus. Journal of Bacteriology, 187, 5790–5798.

    Google Scholar 

  63. Truchado, P., Bastida, J. A., Larrosa, M., Castro, I., Espin, J. C., & Barberan, F. A. T. (2012). Inhibition of quorum sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. Journal of Agricultural and Food Chemistry., 60(36), 8885–8894. https://doi.org/10.1021/jf301365a.

    Article  Google Scholar 

  64. Vijendra Kumar, N., Murthy, P. S., Manjunatha, J. R., & Bettadaiah, B. K. (2014). Synthesis and quorum sensing inhibitory activity of key phenolic compounds of ginger and their derivatives. Food Chemistry, 159, 451–457.

  65. Wolf-Rainer, A. (2006). Controlling biofilms of gram-positive pathogenic bacteria. Current Medicinal Chemistry, 2006(13), 1509–1524.

    Google Scholar 

  66. Yamamoto, S., Miyake, K., Koike, Y., Watanabe, M., Machida, Y., Ohta, M., & Iijima, S. (1999). Molecular characterization of type-specific capsular polysaccharide biosynthesis genes of Streptococcus agalactiae type Ia. Journal of Bacteriology, 181, 5176–5184.

    Google Scholar 

  67. Yarwood, J. M., & Schlievert, P. M. (2003). Quorum sensing in Staphylococcus infections. Journal of Clinical Investigations, 112, 1620–1625.

    Google Scholar 

  68. Ye, X., Li, J., Lu, M., Deng, G., Jiang, X., et al. (2011). Identification and molecular typing of Streptococcus agalactiae isolated from pond-cultured tilapia in China. Fisheries Sci, 77, 623–632.

    Google Scholar 

  69. Yu, Z. Z., L. W. Xue, P. Gang, R. Hui, W. Jing, X. Q. Lin, X. H. Hui, W. F. Hao And T. J. Wen. (2013). Phenolics from Ageratina adenophora Roots and Their Phytotoxic Effects on Arabidopsis thaliana Seed Germination and Seedling Growth. Journal of Agricultural and Food Chemistry, 61(48), 11792–11799

  70. Zanni, E., Chandraiahgari, C. R., De Bellis, G., Montereali, M. R., Armiento, G., Ballirano, P., Polimeni, A., Sarto, M. S., & Uccelletti, D. (2016). Zinc nano-oxides, nanorods-decorated graphene nanoplatelets: a promising antimicrobial agent against the cariogenic bacterium Streptococcus mutans. Nanomaterials, 6(10), 179.

    Google Scholar 

  71. Zeng, Z., Qian, L., Cao, L., Tan, H., Huang, Y., Xue, X., Shen, Y., & Zhou, S. (2008). Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Applied Microbiology and Biotechnology, 79(1), 119–126.

  72. Ziebandt, A. K., Becher, D., Ohlsen, K., Hacker, J., Hecker, M., & Engelmann, S. (2004). Proteomics, 4, 3034.

    Google Scholar 

Download references

Acknowledgments

The authors acknowledge the support of the Molecular Biology and Biotechnology Laboratory of the College of Fisheries and the Molecular Laboratory of the College of Veterinary Science and Medicine of the Central Luzon State University, Science City of Munoz, Nueva Ecija, Philippines for the use of their facilities and the DOST-Applied Science and Technology Human Resource Development Program (DOST-ASTHRDP) Philippines.

Data Availability Statement

The authors are more than willing to share the research data upon reasonable request.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Somar Israel D. Fernando.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Research Involving Humans and Animals Statement

No experimental animals were distressed and harmed in the study. Bacterial isolates were obtained from the external surface of the infected fishes and no surgical procedures were conducted.

Informed consent

None.

Funding Statement

None.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernando, S.I.D., Judan Cruz, K.G. & Watanabe, K. Quorum Sensing-Linked agrA Expression by Ethno-Synthesized Gold Nanoparticles in Tilapia Streptococcus agalactiae Biofilm Formation. BioNanoSci. 10, 696–704 (2020). https://doi.org/10.1007/s12668-020-00758-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12668-020-00758-6

Keywords

Navigation