Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Inhibition of Microbial Quorum Sensing Mediated Virulence Factors by Pestalotiopsis sydowiana

  • Parasuraman, Paramanantham (Department of Microbiology, School of Life Sciences, Pondicherry University) ;
  • Devadatha, B (Department of Biotechnology, School of Life Sciences, Pondicherry University) ;
  • Sarma, V. Venkateswara (Department of Biotechnology, School of Life Sciences, Pondicherry University) ;
  • Ranganathan, Sampathkumar (Centre for Bioinformatics, School of Life Sciences, Pondicherry University) ;
  • Ampasala, Dinakara Rao (Centre for Bioinformatics, School of Life Sciences, Pondicherry University) ;
  • Reddy, Dhanasekhar (Department of Genomic Science, School of Biological Sciences, Central University of Kerala) ;
  • Kumavath, Ranjith (Department of Genomic Science, School of Biological Sciences, Central University of Kerala) ;
  • Kim, In-Won (Department of Chemical Engineering, Konkuk University) ;
  • Patel, Sanjay K.S. (Department of Chemical Engineering, Konkuk University) ;
  • Kalia, Vipin Chandra (Department of Chemical Engineering, Konkuk University) ;
  • Lee, Jung-Kul (Department of Chemical Engineering, Konkuk University) ;
  • Siddhardha, Busi (Department of Microbiology, School of Life Sciences, Pondicherry University)
  • Received : 2019.07.15
  • Accepted : 2020.01.17
  • Published : 2020.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

Quorum sensing (QS)-mediated infections cause severe diseases in human beings. The control of infectious diseases by inhibiting QS using antipathogenic drugs is a promising approach as antibiotics are proving inefficient in treating these diseases. Marine fungal (Pestalotiopsis sydowiana PPR) extract was found to possess effective antipathogenic characteristics. The minimum inhibitory concentration (MIC) of the fungal extract against test pathogen Pseudomonas aeruginosa PAO1 was 1,000 ㎍/ml. Sub-MIC concentrations (250 and 500 ㎍/ml) of fungal extract reduced QS-regulated virulence phenotypes such as the production of pyocyanin, chitinase, protease, elastase, and staphylolytic activity in P. aeruginosa PAO1 by 84.15%, 73.15%, 67.37%, 62.37%, and 33.65%, respectively. Moreover, it also reduced the production of exopolysaccharides (74.99%), rhamnolipids (68.01%), and alginate (54.98%), and inhibited the biofilm formation of the bacteria by 90.54%. In silico analysis revealed that the metabolite of P. sydowiana PPR binds to the bacterial QS receptor proteins (LasR and RhlR) similar to their respective natural signaling molecules. Cyclo(-Leu-Pro) (CLP) and 4-Hydroxyphenylacetamide (4-HPA) were identified as potent bioactive compounds among the metabolites of P. sydowiana PPR using in silico approaches. The MIC values of CLP and 4-HPA against P. aeruginosa PAO1 were determined as 250 and 125 ㎍/ml, respectively. All the antivirulence assays were conducted at sub-MIC concentrations of CLP (125 ㎍/ml) and 4-HPA (62.5 ㎍/ml), which resulted in marked reduction in all the investigated virulence factors. This was further supported by gene expression studies. The findings suggest that the metabolites of P. sydowiana PPR can be employed as promising QS inhibitors that target pathogenic bacteria.

Keywords

References

  1. Kalia VC. 2013. Quorum sensing inhibitors: An overview. Biotechnol. Adv. 31: 224-245. https://doi.org/10.1016/j.biotechadv.2012.10.004
  2. Kalia VC, Patel SKS, Kang YC, Lee J-K. 2019. Quorum sensing inhibitors as antipathogens: biotechnological applications. Biotechnol. Adv. 37: 68-90. https://doi.org/10.1016/j.biotechadv.2018.11.006
  3. Kalia VC. 2014. In search of versatile organisms for quorum-sensing inhibitors: acyl homoserine lactones (AHL)-acylase and AHLlactonase. FEMS Microbiol. Lett. 359: 143-143. https://doi.org/10.1111/1574-6968.12585
  4. Kalia VC. 2014. Microbes, antimicrobials and resistance: The battle goes on. Indian J. Microbiol. 54: 1-2. https://doi.org/10.1007/s12088-013-0443-7
  5. Kalia VC, Purohit HJ. 2011. Quenching the quorum sensing system: potential antibacterial drug targets. Crit. Rev. Microbiol. 37: 121-140. https://doi.org/10.3109/1040841X.2010.532479
  6. Kumar P, Patel SKS, Lee J-K, Kalia VC. 2013. Extending the limits of Bacillus for novel biotechnological applications. Biotechnol. Adv. 31: 1543-1561. https://doi.org/10.1016/j.biotechadv.2013.08.007
  7. Kalia VC, Raju SC, Purohit HJ. 2011. Genomic analysis reveals versatile organisms for quorum quenching enzymes: Acyl- Homoserine lactone-Acylase and -Lactonase. Open Microbiol. J. 3: 1-11. https://doi.org/10.2174/1874285800903010001
  8. Huma N, Shankar P, Kushwah J, Bhushan A, Joshi J, Mukherjee T, et al. 2011. Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J. Microbiol. Biotechnol. 21: 1001-1011. https://doi.org/10.4014/jmb.1105.05056
  9. Kostylev M, Kim DY, Smalley NE, Salukhe I, Greenberg EP, Dandekar AA. 2019. Evolution of the Pseudomonas aeruginosa quorumsensing hierarchy. Proc. Natl. Acad. Sci. USA 116: 7027-7032. https://doi.org/10.1073/pnas.1819796116
  10. Lee K, Yoon SS. 2017. Pseudomonas aeruginosa biofilm, a programmed bacterial life for fitness. J. Microbiol. Biotechnol. 27: 1053-1064. https://doi.org/10.4014/jmb.1611.11056
  11. Yong Y-C, Zhong J-J. 2013. Impacts of quorum sensing on microbial metabolism and human health, pp. 25-61. In Zhong J-J (ed.), Future Trends in Biotechnology, Advances in Biochemical Engineering/Biotechnology, vol. 131. Springer, Berlin, Heidelberg.
  12. Mulcahy LR, Isabella VM, Lewis K. 2014. Pseudomonas aeruginosa biofilms in disease. Microb. Ecol. 68: 1-12. https://doi.org/10.1007/s00248-013-0297-x
  13. Ding F, Oinuma K-I, Smalley NE, Schaefer AL, Hamwy O, Peter Greenberg E, et al. 2018. The Pseudomonas aeruginosa orphan quorum sensing signal receptor QscR regulates global quorum sensing gene expression by activating a single linked operon. mBio. 9: e01274-18.
  14. Sun S, Dai X, Sun J, Bu X, Weng C, Li H, Zhu H. 2016. A diketopiperazine factor from Rheinheimera aquimaris QSI02 exhibits antiquorum sensing activity. Sci. Rep. 6: 39637. https://doi.org/10.1038/srep39637
  15. Kim A-L, Park S-Y, Lee CH, Lee C-H, Lee J-K. 2014. Quorum quenching bacteria isolated from the sludge of a wastewater treatment plant and their application for controlling biofilm formation. J. Microbiol. Biotechnol. 24: 1574-1582. https://doi.org/10.4014/jmb.1407.07009
  16. Lade H, Paul D, Kweon JH. 2015. Combined effects of curcumin and (-)-epigallocatechin gallate on inhibition of n-acylhomoserine lactone-mediated biofilm formation in wastewater bacteria from membrane bioreactor. J. Microbiol. Biotechnol. 25: 1908-1919. https://doi.org/10.4014/jmb.1506.06010
  17. Yap PSX, Krishnan T, Chan K-G, Lim SHE. 2015. Antibacterial mode of action of Cinnamomum verum bark essential oil, alone and in combination with piperacillin, against a multi-drug-resistant Escherichia coli strain. J. Microbiol. Biotechnol. 25: 1299-1306. https://doi.org/10.4014/jmb.1407.07054
  18. Jo SJ, Kwon H, Jeong S-Y, Lee SH, Oh H-S, Yi T, et al . TG. 2016. Effects of quorum quenching on the microbial community of biofilm in an anoxic/oxic MBR for wastewater treatment. J. Microbiol. Biotechnol. 26: 1593-1604. https://doi.org/10.4014/jmb.1604.04070
  19. Zhang L, Guo Z, Gao H, Peng X, Li Y, Sun S, Lee J-K, et al. 2016. Interaction of Pseudostellaria heterophylla with quorum sensing and quorum quenching bacteria mediated by root exudates in a consecutive monoculture system. J. Microbiol. Biotechnol. 26: 2159-2170. https://doi.org/10.4014/jmb.1607.07073
  20. Choi H-A, Cheong D-E, Lim H-D, Kim W-H, Ham M-H, Oh M-H, et al. 2017. Antimicrobial and anti-biofilm activities of the methanol extracts of medicinal plants against dental pathogens Streptococcus mutans and Candida albicans. J. Microbiol. Biotechnol. 27: 1242-1248. https://doi.org/10.4014/jmb.1701.01026
  21. Kang S-Y, Kim B-M, Heo KT, Jang J-H, Kim W-G, Hong Y-S. 2017. Production of bacterial quorum sensing antagonists, caffeoyland feruloyl-HSL, by an artificial biosynthetic pathway. J. Microbiol. Biotechnol. 27: 2104-2111. https://doi.org/10.4014/jmb.1705.05033
  22. Lee SH, Lee S, Lee K, Nahm CH, Jo SJ, Lee J, et al. 2017. Enhancing the physical properties and lifespan of bacterial quorum quenching media through combination of ionic cross-linking and dehydration. J. Microbiol. Biotechnol. 27: 552-560. https://doi.org/10.4014/jmb.1611.11016
  23. Wang J, Nong X-H, Zhang X-Y, Xu X-Y, Amin M, Qi S-H. 2017. Screening of anti-biofilm compounds from marine-derived fungi and the effects of secalonic acid D on Staphylococcus aureus biofilm. J. Microbiol. Biotechnol. 27: 1078-1089. https://doi.org/10.4014/jmb.1609.09053
  24. Ham Y, Kim T-J. 2018. Nitrogen sources inhibit biofilm formation of Xanthomonas oryzae pv. oryzae. J. Microbiol. Biotechnol. 28: 2071-2078. https://doi.org/10.4014/jmb.1807.08025
  25. Ahmad MS, El-Gendy AO, Ahmed RR, Hassan HM, El-Kabbany HM, Merdash AG. 2017. Exploring the antimicrobial and antitumor potentials of Streptomyces sp. AGM12-1 isolated from Egyptian soil. Front. Microbiol. 8: 438.
  26. Vasavi HS, Arun AB, Rekha PD. 2016. Anti-quorum sensing activity of flavonoid-rich fraction from Centella asiatica L. against Pseudomonas aeruginosa PAO1. J. Microbiol. Immunol. Infect. 49: 8-15. https://doi.org/10.1016/j.jmii.2014.03.012
  27. Miao L, Xu J, Yao Z, Jiang Y, Zhou H, Jiang W, Dong K. 2017. The anti-quorum sensing activity and bioactive substance of a marine derived Streptomyces. Biotechnol. Biotechnol. Equip. 31: 1007-1015. https://doi.org/10.1080/13102818.2017.1348253
  28. Shukla V, Bhathena Z. 2016. Broad spectrum anti-quorum sensing activity of tannin-rich crude extracts of Indian medicinal plants. Scientifica (Cairo). 2016: 1-8.
  29. Kalia M, Yadav VK, Singh PK, Sharma D, Pandey H, Narvi SS, Agarwal V. 2015. Effect of cinnamon oil on quorum sensingcontrolled virulence factors and biofilm formation in Pseudomonas aeruginosa. PLoS One 10: e0135495. https://doi.org/10.1371/journal.pone.0135495
  30. Ma Z-P, Song Y, Cai Z-H, Lin Z-J, Lin G-H, Wang Y, et al. 2018. Anti-quorum sensing activities of selected coral symbiotic bacterial extracts from the South China sea. Front. Cell. Infect. Microbiol. 8: 144. https://doi.org/10.3389/fcimb.2018.00144
  31. Hossain MA, Lee S-J, Park N-H, Mechesso AF, Birhanu BT, Kang J, et al. 2017. Impact of phenolic compounds in the acyl homoserine lactone-mediated quorum sensing regulatory pathways. Sci. Rep. 7: 10618. https://doi.org/10.1038/s41598-017-10997-5
  32. Musthafa KS, Saroja V, Pandian SK, Ravi AV. 2011. Antipathogenic potential of marine Bacillus sp. SS4 on N-acyl-homoserinelactone-mediated virulence factors production in Pseudomonas aeruginosa (PAO1). J. Biosci. 36: 55-67. https://doi.org/10.1007/s12038-011-9011-7
  33. Husain FM, Ahmad I, Al-thubiani AS, Abulreesh HH, AlHazza IM, Aqil F. 2017. Leaf extracts of Mangifera indica L. inhibit quorum sensing - regulated production of virulence factors and biofilm in test bacteria. Front. Microbiol. 8: 1-12.
  34. Adonizio A, Kong K-F, Mathee K. 2008. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob. Agents Chemother. 52: 198-203. https://doi.org/10.1128/AAC.00612-07
  35. Li T, Mei Y, He B, Sun X, Li J. 2019. Reducing quorum sensing-mediated virulence factor expression and biofilm formation in hafnia alvei by using the potential quorum sensing inhibitor L-carvone. Front. Microbiol. 9: 3324. https://doi.org/10.3389/fmicb.2018.03324
  36. Yin H, Deng Y, Wang H, Liu W, Zhuang X, Chu W. 2015. Tea polyphenols as an antivirulence compound disrupt quorum-sensing regulated pathogenicity of Pseudomonas aeruginosa. Sci. Rep. 5: 16158. https://doi.org/10.1038/srep16158
  37. Lee J-H, Kim Y-G, Yong Ryu S, Lee J. 2016. Calcium-chelating alizarin and other anthraquinones inhibit biofilm formation and the hemolytic activity of Staphylococcus aureus. Sci. Rep. 6: 19267. https://doi.org/10.1038/srep19267
  38. Luo J, Dong B, Wang K, Cai S, Liu T, Cheng X, et al. 2017. Baicalin inhibits biofilm formation, attenuates the quorum sensingcontrolled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS One 12: e0176883. https://doi.org/10.1371/journal.pone.0176883
  39. Gopu V, Meena CK, Shetty PH. 2015. Quercetin influences quorum sensing in food borne bacteria: in-vitro and in-silico evidence. PLoS One 10: e0134684. https://doi.org/10.1371/journal.pone.0134684
  40. Singh G, Kumar P. 2013. Extraction, gas chromatography-mass spectrometry analysis and screening of fruits of Terminalia chebula Retz. for its antimicrobial potential. Pharmacognosy Res. 5: 162. https://doi.org/10.4103/0974-8490.112421
  41. Lovell SC, Davis IW, Arendall WB, de Bakker PIW, Word JM, Prisant MG, et al. 2003. Structure validation by $C{\alpha}$ geometry: $\phi$,$\psi$ and $C{\beta}$ deviation. Proteins 50: 437-450. https://doi.org/10.1002/prot.10286
  42. Husain FM, Ahmad I, Baig MH, Khan MS, Khan MS, Hassan I, et al. 2016. Broad-spectrum inhibition of AHL-regulated virulence factors and biofilms by sub-inhibitory concentrations of ceftazidime. RSC Adv. 6: 27952-27962. https://doi.org/10.1039/c6ra02704k
  43. Friesner RA, Murphy RB, Repasky MP, Frye LL, Greenwood JR, Halgren TA, et al. 2006. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J. Med. Chem. 49: 6177-6196. https://doi.org/10.1021/jm051256o
  44. Abraham MJ, Murtola T, Schulz R, Pall S, Smith JC, Hess B, et al. 2015. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 2: 19-25.
  45. Rajkumari J, Borkotoky S, Reddy D, Mohanty SK, Kumavath R, Murali A, et al. 2019. Anti-quorum sensing and anti-biofilm activity of 5-hydroxymethylfurfural against Pseudomonas aeruginosa PAO1: Insights from in vitro, in vivo and in silico studies. Microbiol. Res. 226: 19-26. https://doi.org/10.1016/j.micres.2019.05.001
  46. Hnamte S, Parasuraman P, Ranganathan S, Ampasala DR, Reddy D, Kumavath RN, et al. 2019. Mosloflavone attenuates the quorum sensing controlled virulence phenotypes and biofilm formation in Pseudomonas aeruginosa PAO1: In vitro, in vivo and in silico approach. Microb. Pathog. 131: 128-134. https://doi.org/10.1016/j.micpath.2019.04.005
  47. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2: a012427. https://doi.org/10.1101/cshperspect.a012427
  48. Hussain MS, Oh D-H. 2018. Impact of the isolation source on the biofilm formation characteristics of Bacillus cereus. J. Microbiol. Biotechnol. 28: 77-86. https://doi.org/10.4014/jmb.1707.07023
  49. Jin W, Lin H, Gao H, Guo Z, Li J, Xu Q, et al. 2019. N-acyl-homoserine lactone quorum sensing switch from acidogenesis to solventogenesis during the fermentation process in Serratia marcescens MG1. J. Microbiol. Biotechnol. 29: 596-606. https://doi.org/10.4014/jmb.1810.10026
  50. Lim ES, Kim J-S. 2017. Role of eptC in biofilm formation by Campylobacter jejuni NCTC11168 on polystyrene and glass surfaces. J. Microbiol. Biotechnol. 27: 1609-1616. https://doi.org/10.4014/jmb.1610.10046
  51. Hancer Aydemir D, Cifci G, Aviyente V, Bosgelmez-Tinaz G. 2018. Quorum-sensing inhibitor potential of trans -anethole aganist Pseudomonas aeruginosa. J. Appl. Microbiol. 125: 731-739. https://doi.org/10.1111/jam.13892
  52. Lindequist U. 2016. Marine-derived pharmaceuticals - challenges and opportunities. Biomol. Ther. (Seoul). 24: 561-571. https://doi.org/10.4062/biomolther.2016.181
  53. Chen J, Wang B, Lu Y, Guo Y, Sun J, Wei B, Zhang H, Wang H. 2019. Quorum sensing inhibitors from marine microorganisms and their synthetic derivatives. Mar. Drugs. 17: 80. https://doi.org/10.3390/md17020080
  54. Zhang M, Wang M, Zhu X, Yu W, Gong Q. 2018. Equisetin as potential quorum sensing inhibitor of Pseudomonas aeruginosa. Biotechnol. Lett. 40: 865-870. https://doi.org/10.1007/s10529-018-2527-2
  55. Sharma D, Pramanik A, Agrawal PK. 2016. Evaluation of bioactive secondary metabolites from endophytic fungus Pestalotiopsis neglecta BAB-5510 isolated from leaves of Cupressus torulosa D.Don. 3 Biotech 6: 210. https://doi.org/10.1007/s13205-016-0518-3
  56. Koh CL, Sam CK, Yin WF, Tan LY, Krishnan T, Chong YM, et al. 2013. Plant-derived natural products as sources of anti-quorum sensing compounds. Sensors (Basel). 13: 6217-6228. https://doi.org/10.3390/s130506217

Cited by

  1. Nanostructured Antimicrobial Peptides: Crucial Steps of Overcoming the Bottleneck for Clinics vol.12, 2020, https://doi.org/10.3389/fmicb.2021.710199
  2. Resistance risk induced by quorum sensing inhibitors and their combined use with antibiotics: Mechanism and its relationship with toxicity vol.265, 2020, https://doi.org/10.1016/j.chemosphere.2020.129153
  3. Recent Clinical Trials on Natural Products and Traditional Chinese Medicine Combating the COVID-19 vol.61, pp.1, 2021, https://doi.org/10.1007/s12088-020-00919-x
  4. Quorum sensing: a new prospect for the management of antimicrobial-resistant infectious diseases vol.19, pp.5, 2020, https://doi.org/10.1080/14787210.2021.1843427
  5. Benefits of Usage of Immobilized Silver Nanoparticles as Pseudomonas aeruginosa Antibiofilm Factors vol.23, pp.1, 2020, https://doi.org/10.3390/ijms23010284