Research Article


DOI :10.26650/experimed.1512454   IUP :10.26650/experimed.1512454    Full Text (PDF)

Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.

Gamze Benli YardımcıEkrem Murat GönülalanNurnehir Baltacı BozkurtEmirhan NemutluEngin KoçakMüjde Eryılmaz

Objective: The objective of this research was to explore the antibacterial, antibiofilm, and anti-quorum sensing (anti-QS) activities of cellfree supernatants (CFSs) of Bacillus sp. and correlate these activities with their metabolite profiles.

Materials and Methods: We used 55 Bacillus sp. isolates from soil samples. The antibacterial activities of the CFSs were investigated using disk diffusion and agar well diffusion methods. Antibiofilm activities were assessed using the crystal violet microplate method and anti-QS activities were evaluated using the disc diffusion method. The identification of biologically active isolates was performed using matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF-MS). The metabolite profiles of active CFSs were analyzed using gas chromatography-mass spectrometry (GC-MS).

Results: Only S-45 exhibited antibacterial activity against Staphylococcus aureus ATCC 25923. Biofilm inhibition percentages of the CFSs against Staphylococcus epidermidis ATCC 35984 and Pseudomonas aeruginosa PAO1 varied between 92.58% - 3.96% and 78.96% - 0.64%, respectively. Only S-37 exhibited anti-QS activity. The most biologically active isolates belonged to the Bacillus cereus group. Based on the GC-MS results, 102 metabolites were identified. According to correlation analyses between the results of antibiofilm activity and metabolite profiles, we determined that compounds belonging to the amino acid and peptide groups, hydroxy acids and derivatives, and fatty acyls exhibited a highly positive correlation. The metabolite profiles of S-45 and S-37 were not significantly different from the negative control (S-46). Therefore, these activities could not be associated with the metabolite content.

Conclusion: The correlation between specific metabolite profiles and bioactivities indicates the potential of these bioactivities for innovative pharmaceutical applications. Future research should focus on isolating and testing these individual metabolites to confirm their specific roles and mechanisms.


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References

  • 1. Peschel A, Sahl HG. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 2006; 4(7): 529-36. google scholar
  • 2. Dadgostar P. Antimicrobial resistance: implications and costs. Infect Drug Resist 2019; 12: 3903-10. google scholar
  • 3. Varela MF, Stephen J, Lekshmi M, Ojha M, Wenzel N, Sanford LM, et al. Bacterial resistance to antimicrobial agents. Antibiotics 2021; 10(5): 593. google scholar
  • 4. Cheng G, Dai M, Ahmed S, Hao H, Wang X, Yuan Z. Antimicrobial drugs in fighting against antimicrobial resistance. Front Microbiol 2016; 7: 470. google scholar
  • 5. Cicek Polat D, Gümüşok S, Rızvanoglu SS, Eryilmaz M. Bioactivities of Cotinus coggygria and its HPLC-DAD phenolic profiles. Plant Biosyst 2023; 157(5): 1061-66. google scholar
  • 6. Tobias NJ, Brehm J, Kresovic D, Brameyer S, Bode HB, Heermann R. New vocabulary for bacterial communication. ChemBioChem 2020; 21(6): 759-68. google scholar
  • 7. Sauer K, Stoodley P, Goeres DM, Hall-Stoodley L, Burm0lle M, Stewart PS, et al. The biofilm life cycle: Expanding the conceptual model of biofilm formation. Nat Rev Microbiol 2022; 20(10): 608-20. google scholar
  • 8. Amedei A, M D’Elios M. New therapeutic approaches by using microorganism-derived compounds. Curr Med Chem 2012; 19(22): 3822-40. google scholar
  • 9. Chevrette MG, Handelsman J. Needles in haystacks: reevaluating old paradigms for the discovery of bacterial secondary metabolites. Nat Prod Rep 2021; 38(11): 2083-99. google scholar
  • 10. Sansinenea E, Ortiz A. Secondary metabolites of soil Bacillus spp. Biotechnol Lett 2011; 33(8): 1523-38. google scholar
  • 11. Wagg C, Bender SF, Widmer F, Van Der Heijden MG. Soil biodiversity and soil community composition determine ecosystem multifunctionality. P Natl A Sci 2014; 111(14): 5266-70. google scholar
  • 12. Singh P, Sharma R, Shukla A K, Singh R. Isolation of Bacillus spp. from soil for antimicrobial production and antibiotic resistance. Adv Biotech & Micro 2018; 8(4): 1-5. google scholar
  • 13. Johnvesly B, Manjunath BR, Naik GR. Pigeon pea waste as a novel, inexpensive, substrate for production of a thermostable alkaline protease from thermoalkalophilic Bacillus sp. JB-99. Bioresource Technol 2002; 82(1): 61-4. google scholar
  • 14. Baruzzi F, Quintieri L, Morea M, Caputo L. Antimicrobial compounds produced by Bacillus spp. and applications in food. Formatex 2011; 2(1): 1102-11. google scholar
  • 15. Wang T, Liang Y, Wu M, Chen Z, Lin J, Yang L. Natural products from Bacillus subtilis with antimicrobial properties. Chinese J Chem Eng 2015; 23(4): 744-54. google scholar
  • 16. Ali SAM, Sayyed RZ, Mir MI, Khan MY, Hameeda B, Alkhanani MF, et al. Induction of systemic resistance in maize and antibiofilm activity of surfactin from Bacillus velezensis MS20. Front Microbiol 2022; 13: 879739. google scholar
  • 17. Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microb 2002; 68(4): 1754-9. google scholar
  • 18. Devi KR, Srinivasan S, Ravi AV. Inhibition of quorum sensing-mediated virulence in Serratia marcescens by Bacillus subtilis R-18. Microb Pathogenesis 2018; 120: 166-75. google scholar
  • 19. El Aichar F, Muras A, Parga A, Otero A, Nateche F. Quorum quenching and anti-biofilm activities of halotolerant Bacillus strains isolated in different environments in Algeria. J Appl Microbiol 2022; 132(3): 1825-39. google scholar
  • 20. Boottanun P, Potisap C, Hurdle JG, Sermswan RW. Secondary metabolites from Bacillus amyloliquefaciens isolated from soil can kill Burkholderia pseudomallei. AMB Express 2017; 7(1): 1-11. google scholar
  • 21. Lay Jr JO. MALDI-TOF mass spectrometry of bacteria. Mass Spectrom Rev 2001; 20(4): 172-94. google scholar
  • 22. Matuschek E, Brown DF, Kahlmeter G. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin Microbiol Infect 2014; 20(4): O255-66. google scholar
  • 23. Eryilmaz M, Gurpinar SS, Palabiyik IM, Guriz H, Gerceker D. Molecular identification and antimicrobial activity of vaginal Lactobacillus sp.. Curr Pharm Biotechno 2018; 19(15): 1241-7. google scholar
  • 24. Eryilmaz M, Kart D, Gürpınar SS. Investigation of antibiofilm activities of Lactobacillus sp. metabolites isolated from vaginal flora. Turk Mikrobiol Cem Derg 2019; 49(3): 169-74. google scholar
  • 25. Junejo B, Eryilmaz M, Rizvanoglu SS, Palabiyik IM, Ghumro T, Mallah A, et al. Pharmacological assessment of Co3O4, CuO, NiO and ZnO nanoparticles via antibacterial, anti-biofilm and anti-quorum sensing activities. Water Sci Technol 2023; 87(11): 2840-51. google scholar
  • 26. Gajdacs M, Spengler G. Standard operating procedure (SOP) for disk diffusion-based quorum sensing inhibition assays. APH 2019; 89(4): 117-125. google scholar
  • 27. Nemutlu E, Zhang S, Xu YZ, Terzic A, Zhong L, Dzeja PD, et al. Cardiac resynchronization therapy induces adaptive metabolic transitions in the metabolomic profile of heart failure. J Card Fail 2015; 21(6): 460-9. google scholar
  • 28. Pang Z, Zhou G, Ewald J, Chang L, Hacariz O, Basu N, et al. Using MetaboAnalyst 5.0 for LC-HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics data. Nature Protocols 2022; 17: 1735-61. google scholar
  • 29. Nithya C, Begum MF, Pandian SK. Marine bacterial isolates inhibit biofilm formation and disrupt mature biofilms of Pseudomonas aeruginosa PAO1. Appl Microbiol Biot 2010; 88(1): 341-58. google scholar
  • 30. Thapa A, Budhathoki A, Sapkota A, Sainju M, Shrestha P, Pant SP. Isolation, identification and screening of Bacillus species with antimicrobial activity from different soil samples of Kathmandu Valley. Nepal J Biotechnol 2021; 9(2): 1-6. google scholar
  • 31. Nalini S, Parthasarathi R, Prabudoss V. Production and characterization of lipopeptide from Bacillus cereus SNAU01 under solid state fermentation and its potential application as anti-biofilm agent. Biocatal Agric Biotechnol 2016; 5:123-32. google scholar
  • 32. Hilpert K, Volkmer-Engert R, Walter T, Hancock RE. High-throughput generation of small antibacterial peptides with improved activity. Nat Biotechnol 2005; 23(8):1008-12. google scholar
  • 33. Sova M. Antioxidant and antimicrobial activities of cinnamic acid derivatives. Mini Rev Med Chem 2012; 12(8): 749-67. google scholar
  • 34. Falardeau J, Wise C, Novitsky L, Avis TJ. Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J Chem Ecol 2013; 39(7): 869-78. google scholar
  • 35. Siebert A, Wysocka M, Krawczyk B, Cholewinski G, Rachon J. Synthesis and antimicrobial activity of amino acid and peptide derivatives of mycophenolic acid. Eur J Med Chem 2018; 143: 646-55. google scholar
  • 36. Demirezer LO, Gonulalan EM, Nemutlu E. Fitoterapide metabolomiks (fitomiks) çalışmalar ve önemi. Ankara: Türkiye Klinikleri Yayınevi. 2022. p. 68-74. google scholar
  • 37. Waris M, Kocak E, Gonulalan EM, Demirezer LÖ, Kır S, Nemutlu E. Metabolomics analysis insight into medicinal plant science. Trac-Trend Anal Chem 2022; 157: 116795. google scholar
  • 38. Kachhadia R, Kapadia C, Singh S, Gandhi K, Jajda H, Alfarraj S, et al. Quorum Sensing Inhibitory and Quenching Activity of Bacillus cereus RC1 Extracts on Soft Rot-Causing Bacteria Lelliottia amnigena. ACS Omega 2022; 7(29): 25291-308. google scholar
  • 39. Khan MM, Kim YK, Cho SS, Jin YY, Suh JW, Lee DY, et al. Response surface optimization of culture conditions for cyclic lipopeptide MS07 from Bacillus siamensis reveals diverse insights targeting antimicrobial and antibiofilm activity. Processes 2020; 8(6): 744. google scholar
  • 40. Moryl M, Spçtana M, Dziubek K, Paraszkiewicz K, Rozalska S, Plaza G, et al. Antimicrobial, antiadhesive and antibiofilm potential of lipopeptides synthesised by Bacillus subtilis, on uropathogenic bacteria. ABP 2015; 62(4): 725-32. google scholar
  • 41. Singh N, Goel G, Raghav M. Prevalence and characterization of Cronobacter spp. from various foods, medicinal plants, and environmental samples. Curr Microbiol 2015; 71:31-8. google scholar
  • 42. Akbas MY, Cag S. Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. Food Sci Technol Int 2016; 22(7): 587-97. google scholar
  • 43. Laverty G, McCloskey AP, Gorman SP, Gilmore BF. Anti-biofilm activity of ultrashort cinnamic acid peptide derivatives against medical device-related pathogens. J Pept Sci 2015; 21(10): 770-8. google scholar
  • 44. Pletzer D, Hancock RE. Antibiofilm peptides: potential as broad-spectrum agents. J Bacteriol 2016; 198(19): 2572-8. google scholar
  • 45. Wu H, Moser C, Wang HZ, H0iby N, Song ZJ. Strategies for combating bacterial biofilm infections. Int J Oral Sci 2015; 7(1): 1-7. google scholar
  • 46. Gowrishankar S, Sivaranjani M, Kamaladevi A, Ravi AV, Balamurugan K, Karutha Pandian S. Cyclic dipeptide cyclo (l-leucyl-l-prolyl) from marine Bacillus amyloliquefaciens mitigates biofilm formation and virulence in Listeria monocytogenes. FEMS Pathog Dis 2016; 74(4): ftw017. google scholar
  • 47. Yu X, Li L, Sun S, Chang A, Dai X, Li H, et al. A cyclic dipeptide from marine fungus Penicillium chrysogenum DXY-1 exhibits anti-quorum sensing activity. ACS Omega 2021; 6(11): 7693-700. google scholar
  • 48. Dostert M, Belanger CR, Hancock RE. Design and assessment of anti-biofilm peptides: steps toward clinical application. J Innate Immun 2019; 11(3): 193-204. google scholar
  • 49. Kamarudheen N, Rao KB. Fatty acyl compounds from marine Streptomyces griseoincarnatus strain HK12 against two major biofilm forming nosocomial pathogens; an in vitro and in silico approach. Microb Pathog 2019; 127: 121-30. google scholar

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APA

Yardımcı, G.B., Gönülalan, E.M., Bozkurt, N.B., Nemutlu, E., Koçak, E., & Eryılmaz, M. (2024). Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.. Experimed, 14(3), 183-193. https://doi.org/10.26650/experimed.1512454


AMA

Yardımcı G B, Gönülalan E M, Bozkurt N B, Nemutlu E, Koçak E, Eryılmaz M. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.. Experimed. 2024;14(3):183-193. https://doi.org/10.26650/experimed.1512454


ABNT

Yardımcı, G.B.; Gönülalan, E.M.; Bozkurt, N.B.; Nemutlu, E.; Koçak, E.; Eryılmaz, M. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.. Experimed, [Publisher Location], v. 14, n. 3, p. 183-193, 2024.


Chicago: Author-Date Style

Yardımcı, Gamze Benli, and Ekrem Murat Gönülalan and Nurnehir Baltacı Bozkurt and Emirhan Nemutlu and Engin Koçak and Müjde Eryılmaz. 2024. “Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities..” Experimed 14, no. 3: 183-193. https://doi.org/10.26650/experimed.1512454


Chicago: Humanities Style

Yardımcı, Gamze Benli, and Ekrem Murat Gönülalan and Nurnehir Baltacı Bozkurt and Emirhan Nemutlu and Engin Koçak and Müjde Eryılmaz. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities..” Experimed 14, no. 3 (Dec. 2024): 183-193. https://doi.org/10.26650/experimed.1512454


Harvard: Australian Style

Yardımcı, GB & Gönülalan, EM & Bozkurt, NB & Nemutlu, E & Koçak, E & Eryılmaz, M 2024, 'Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.', Experimed, vol. 14, no. 3, pp. 183-193, viewed 21 Dec. 2024, https://doi.org/10.26650/experimed.1512454


Harvard: Author-Date Style

Yardımcı, G.B. and Gönülalan, E.M. and Bozkurt, N.B. and Nemutlu, E. and Koçak, E. and Eryılmaz, M. (2024) ‘Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.’, Experimed, 14(3), pp. 183-193. https://doi.org/10.26650/experimed.1512454 (21 Dec. 2024).


MLA

Yardımcı, Gamze Benli, and Ekrem Murat Gönülalan and Nurnehir Baltacı Bozkurt and Emirhan Nemutlu and Engin Koçak and Müjde Eryılmaz. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities..” Experimed, vol. 14, no. 3, 2024, pp. 183-193. [Database Container], https://doi.org/10.26650/experimed.1512454


Vancouver

Yardımcı GB, Gönülalan EM, Bozkurt NB, Nemutlu E, Koçak E, Eryılmaz M. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.. Experimed [Internet]. 21 Dec. 2024 [cited 21 Dec. 2024];14(3):183-193. Available from: https://doi.org/10.26650/experimed.1512454 doi: 10.26650/experimed.1512454


ISNAD

Yardımcı, GamzeBenli - Gönülalan, EkremMurat - Bozkurt, NurnehirBaltacı - Nemutlu, Emirhan - Koçak, Engin - Eryılmaz, Müjde. Metabolomic Profiling and Biological Activities of Cell-Free Supernatants of Bacillus sp. Isolates: Antibacterial, Antibiofilm, and Anti-quorum Sensing Activities.”. Experimed 14/3 (Dec. 2024): 183-193. https://doi.org/10.26650/experimed.1512454



TIMELINE


Submitted08.07.2024
Accepted23.10.2024
Published Online04.12.2024

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