Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Screening of Anti-Biofilm Compounds from Marine-Derived Fungi and the Effects of Secalonic Acid D on Staphylococcus aureus Biofilm

  • Wang, Jie (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences) ;
  • Nong, Xu-Hua (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences) ;
  • Zhang, Xiao-Yong (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences) ;
  • Xu, Xin-Ya (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences) ;
  • Amin, Muhammad (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences) ;
  • Qi, Shu-Hua (Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Material Medical, RNAM Center for Marine Microbiology, South China Sea Institute of Oceanology, Chinese Academy of Sciences)
  • Received : 2016.09.27
  • Accepted : 2017.03.15
  • Published : 2017.06.28
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Abstract

Biofilm formation of Staphylococcus aureus is one of its mechanisms of drug resistance. Anti-biofilm screening of 106 compounds from marine-derived fungi displayed that 12 compounds inhibited S. aureus biofilm formation by >50% at the concentration of $100{\mu}g/ml$, and only secalonic acid D (SAD) and B inhibited by >90% at $6.25{\mu}g/ml$ without inhibiting cell growth after 24-h incubation. Meanwhile, it was found that the double bond between C-1 and C-10 of citrinin derivatives and the C-C connection position of two chromone monomers may be important for their anti-biofilm activities. Moreover, SAD slightly facilitated biofilm eradication and influenced its architecture. Furthermore, SAD slowed the cell growth rate in the preceding 18-h incubation and differentially regulated transcriptional expression of several genes, such as agr, isaA, icaA, and icaD, associated with biofilm formation in planktonic and biofilm cells, which may be the reason for the anti-biofilm activity of SAD. Finally, SAD acted synergistically against S. aureus growth and biofilm formation with other antibiotics. These findings indicated that various natural products from marine-derived fungi, such as SAD, could be used as a potential biofilm inhibitor against S. aureus.

Keywords

References

  1. Guo N, Zhao X, Li W, Shi C, Meng R, Liu Z, et al. 2015. The synergy of berberine chloride and totarol against Staphylococcus aureus grown in planktonic and biofilm cultures. J. Med. Microbiol. 64: 891-900. https://doi.org/10.1099/jmm.0.000106
  2. Ohlsen K, Koller KP, Hacker J. 1997. Analysis of expression of the alpha-toxin gene (hla) of Staphylococcus aureus by using a chromosomally encoded hla::lacZ gene fusion. Infect. Immun. 65: 3606-3614.
  3. Lee J, Kim Y, 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
  4. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322. https://doi.org/10.1126/science.284.5418.1318
  5. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6: 199-210. https://doi.org/10.1038/nrmicro1838
  6. Stowe SD, Richards JJ, Tucker AT, Thompson R, Melander C, Cavanagh J. 2011. Anti-biofilm compounds derived from marine sponges. Mar. Drugs 9: 2010-2035. https://doi.org/10.3390/md9102010
  7. Armstrong E, Boyd KG, Burgess JG. 2000. Prevention of marine biofouling using natural compounds from marine organisms. Biotechnol. Annu. Rev. 6: 221-241.
  8. Donia M, Hamann MT. 2003. Marine natural products and their potential applications as anti-infective agents. Lancet Infect. Dis. 3: 338-348. https://doi.org/10.1016/S1473-3099(03)00655-8
  9. Lee JH, Park JH, Cho HS, Joo SW, Cho MH, Lee J. 2013. Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling 29: 491-499. https://doi.org/10.1080/08927014.2013.788692
  10. Park JH, Lee JH, Kim CJ, Lee JC, Cho MH, Lee J. 2012. Extracellular protease in actinomycetes culture supernatants inhibits and detaches Staphylococcus aureus biofilm formation. Biotechnol. Lett. 34: 655-661. https://doi.org/10.1007/s10529-011-0825-z
  11. Hertiani T, Edrada-Ebel R, Ortlepp S, van Soest RWM, de Voogd NJ, Wray V, et al. 2010. From anti-fouling to biofilm inhibition: new cytotoxic secondary metabolites from two Indonesian Agelas sponges. Bioorg. Med. Chem. 18: 1297-1311. https://doi.org/10.1016/j.bmc.2009.12.028
  12. Huigens RW III, Richards JJ, Parise G, Ballard TE, Zeng W, Deora R, et al. 2007. Inhibition of Pseudomonas aeruginosa biofilm formation with bromoageliferin analogues. J. Am. Chem. Soc. 129: 6966-6967. https://doi.org/10.1021/ja069017t
  13. Melander C, Moeller PDR, Ballard TE, Richards JJ, Huigens RW III, Cavanagh J. 2009. Evaluation of dihydrooroidin as an antifouling additive in marine paint. Int. Biodeterior. Biodegrad. 63: 529-532. https://doi.org/10.1016/j.ibiod.2008.08.009
  14. Richards JJ, Huigens RW III, Ballard TE, Basso A, Cavanagh J, Melander C. 2008. Inhibition and dispersion of proteobacterial biofilms. Chem. Commun. (Camb.) 14: 1698-1700.
  15. Rogers SA, Huigens RW III, Cavanagh J, Melander C. 2010. Synergistic effects between conventional antibiotics and 2- aminoimidazole-derived antibiofilm agents. Antimicrob. Agents Chemother. 54: 2112-2118. https://doi.org/10.1128/AAC.01418-09
  16. Skindersoe M, Ettinger-Epstein P, Rasmussen T, Bjarnsholt T, de Nys R, Givskov M. 2008. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 10: 56-63. https://doi.org/10.1007/s10126-007-9036-y
  17. Boles BR, Horswill AR. 2011. Staphylococcal biofilm disassembly. Trends Microbiol. 19: 449-455. https://doi.org/10.1016/j.tim.2011.06.004
  18. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, et al. 2009. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4: e5822. https://doi.org/10.1371/journal.pone.0005822
  19. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, Smeltzer MS, et al. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104: 8113-8118. https://doi.org/10.1073/pnas.0610226104
  20. Wang D, Jin Q, Xiang H, Wang W, Guo N, Zhang K, et al. 2011. Transcriptional and functional analysis of the effects of magnolol: inhibition of autolysis and biofilms in Staphylococcus aureus. PLoS One 6: e26833. https://doi.org/10.1371/journal.pone.0026833
  21. Rogers SA, Huigens RW III, Melander C. 2009. A 2-amino benzimidazole that inhibits and disperses gram-positive biofilms through a zinc-dependent mechanism. J. Am. Chem. Soc. 131: 9868-9869. https://doi.org/10.1021/ja9024676
  22. do Valle Gomes MZ, Nitschke M. 2012. Evaluation of rhamnolipid and surfactin to reduce the adhesion and remove biofilms of individual and mixed cultures of food pathogenic bacteria. Food Control 25: 441-447. https://doi.org/10.1016/j.foodcont.2011.11.025
  23. Bao J, Sun YL, Zhang XY, Han Z, Gao HC, He F, et al. 2013. Antifouling and antibacterial polyketides from marine gorgonian coral-associated fungus Penicillium sp. SCSGAF 0023. J. Antibiot. 66: 219-223. https://doi.org/10.1038/ja.2012.110
  24. Dong JJ, Bao J, Zhang XY, Xu XY, Nong XH, Qi SH. 2014. Alkaloids and citrinins from marine-derived fungus Nigrospora oryzae SCSGAF 0111. Tetrahedron Lett. 55: 2749-2753. https://doi.org/10.1016/j.tetlet.2014.03.060
  25. Bao J, Xu XY, Zhang XY, Qi SH. 2013. A new macrolide from a marine-derived fungus Asperillus sp. Nat. Prod. Commun. 8: 1127-1128.
  26. Bao J, Zhang XY, Xu XY, He F, Nong XH, Qi SH. 2013. New cyclic tetrapeptides and asteltoxins from gorgonian-derived fungus Aspergillus sp. SCSGAF 0076. Tetrahedron 69: 2113-2117. https://doi.org/10.1016/j.tet.2013.01.021
  27. Yao QF, Wang J, Zhang XY, Nong XH, Xu XY, Qi SH. 2014. Cytotoxic polyketides from the deep-sea-derived fungus Engyodontium album DFFSCS021. Mar. Drugs 12: 5902-5915. https://doi.org/10.3390/md12125902
  28. Peng J, Zhang XY, Tu ZC, Xu XY, Qi SH. 2013. Alkaloids from the deep-sea-derived fungus Aspergillus westerdijkiae DFFSCS013. J. Nat. Prod. 76: 983-987. https://doi.org/10.1021/np400132m
  29. Zhou G, Li L, Shi Q, Ouyang Y, Chen Y, Hu W. 2013. Effect of nutritional and environmental conditions on planktonic growth and biofilm formation of Citrobacter werkmanii BF-6. J. Microbiol. Biotechnol. 23: 1673-1682. https://doi.org/10.4014/jmb1307.07041
  30. Shukla SK, Rao TS. 2013. Effect of calcium on Staphylococcus aureus biofilm architecture: a confocal laser scanning microscopic study. Colloids Surf. B 103: 448-454. https://doi.org/10.1016/j.colsurfb.2012.11.003
  31. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersholl BK, et al. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407. https://doi.org/10.1099/00221287-146-10-2395
  32. Sharks RM, Meehl MA, Brothers KM, Martinez RM, Donegan NP, Graber ML, et al. 2008. Genetic evidence for an alternative citrate-dependent biofilm formation pathway in Staphylococcus aureus that is dependent on fibronectin binding proteins and the GraRS two-component regulatory system. Infect. Immun. 76: 2469-2477. https://doi.org/10.1128/IAI.01370-07
  33. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{−{\Delta}{\Delta}Ct}$ method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  34. Tang QY, Feng MG. 2007. Statistical analysis of the test, pp. 59-142. In Yan DP, Zhao YC, Yang R (eds.). DPS Data Processing System: Experimental Design, Statistical Analysis and Data Mining. Science Press, Beijing. China.
  35. Coenye T, Honraet K, Rigole P, Nadal JP, Nelis HJ. 2007. In vitro inhibition of Streptococcus mutans biofilm formation on hydroxyapatite by subinhibitory concentrations of anthraquinones. Antimicrob. Agents Chemother. 51: 1541-1544. https://doi.org/10.1128/AAC.00999-06
  36. Liu C, Tang X, Li P, Li G. 2012. Suberitine A-D, four new cytotoxic dimeric aaptamine alkaloids from the marine sponge Aaptos suberitoides. Org. Lett. 14: 1994-1997. https://doi.org/10.1021/ol3004589
  37. Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4: e1000052. https://doi.org/10.1371/journal.ppat.1000052
  38. Payne DE, Martin NR, Parzych KR, Rickard AH, Underwood A, Boles BR. 2013. Tannic acid inhibits Staphylococcus aureus surface colonization in an IsaA-dependent manner. Infect. Immun. 81: 496-504. https://doi.org/10.1128/IAI.00877-12
  39. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, et al. 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl. Acad. Sci. USA 109: 1281-1286. https://doi.org/10.1073/pnas.1115006109
  40. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP. 2004. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186: 1838-1850. https://doi.org/10.1128/JB.186.6.1838-1850.2004
  41. Marti M, Trotonda MP, Tormo-Mas MA, Vergara-Irigaray M, Cheung AL, Lasa I, et al. 2010. Extracellular proteases inhibit protein-dependent biofilm formation in Staphylococcus aureus. Microbes Infect. 12: 55-64. https://doi.org/10.1016/j.micinf.2009.10.005
  42. Mootz JM, Malone CL, Shaw LN, Horswill AR. 2013. Staphopains modulate Staphylococcus aureus biofilm integrity. Infect. Immun. 81: 3227-3238. https://doi.org/10.1128/IAI.00377-13
  43. Kiedrowski MR, Crosby HA, Hernandez FJ, Malone CL, McNamara JO, Horswill AR. 2014. Staphylococcus aureus Nuc2 is a functional, surface-attached extracellular nuclease. PLoS One 9: e95574. https://doi.org/10.1371/journal.pone.0095574
  44. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 67: 5427-5433.
  45. O'Gara JP. 2007. ica and beyond: biofilm mechanisms and regulation in Staphyloccus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270: 179-188. https://doi.org/10.1111/j.1574-6968.2007.00688.x
  46. Lauderdale KJ, Boles BR, Cheung AL, Horswill AR. 2009. Interconnections between sigma B, agr and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect. Immun. 77: 1623-1635. https://doi.org/10.1128/IAI.01036-08

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