Skip to main content

Advertisement

Log in

Antagonistic Activity of Antimicrobial Metabolites Produced from Seaweed-Associated Bacillus amyloliquefaciens MTCC 10456 Against Malassezia spp.

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Members of the genus Malassezia are known to be opportunistic pathogens responsible for causing skin disorders such as seborrheic dermatitis or dandruff, pityriasis versicolor, folliculitis, atopic dermatitis, and psoriasis. Due to the side effects caused by prolonged use of current topical antifungal agents, development of an alternative treatment is necessary. Fermentative production of antimicrobial metabolites from Bacillus amyloliquefaciens MTCC 10456 was carried out, and their antagonistic activity against Malassezia furfur and Malassezia globosa was evaluated. The antifungal metabolites were isolated by acid precipitation, and bioassay-guided simultaneous separation of the antimicrobial compounds was done by reversed-phase high-performance liquid chromatography (RP-HPLC). The fraction which demonstrated antifungal activity consisted of bacilysin, homologues of bacillomycin D, and members of the macrolactin family. The presence of bacilysin was detected using specific inhibitor assays and homologues of bacillomycin D, and macrolactins were identified using liquid chromatography/high-resolution electrospray ionization-mass spectrometry (LC/HRESI-MS/MS) analysis. Synergism among the identified compounds was observed which enhanced the antagonistic activity against Malassezia spp. To our knowledge, this is the first study to report the co-production and separation of members of macrolactin antibiotics, lipopeptides such as bacillomycin D and dipeptide antibiotic bacilysin, by any Bacillus strain from marine environment. Activity of individual compounds against Malassezia has been reported which may facilitate their application in the field of dermatology and in cosmetic products.

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

Similar content being viewed by others

Data Availability

Both the authors have read and approved the final manuscript. The contents of this manuscript have not been copyrighted or published previously.

References

  1. Saunders CW, Scheynius A, Heitman J (2012) Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog 8:e1002701. https://doi.org/10.1371/journal.ppat.100270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Rojas FD, De Los A, Sosa M, Fernández MS (2014) Antifungal susceptibility of Malassezia furfur, Malassezia sympodialis, and Malassezia globosa to azole drugs and amphotericin B evaluated using a broth microdilution method. Med Mycol 52:641–646. https://doi.org/10.1093/mmy/myu010

    Article  CAS  PubMed  Google Scholar 

  3. Ryu S, Choi SY, Acharya S et al (2011) Antimicrobial and anti-inflammatory effects of cecropin A (1–8)–Magainin2 (1–12) hybrid peptide analog P5 against Malassezia furfur infection in human keratinocytes. J Invest Dermatol 131:1677–1683. https://doi.org/10.1038/jid.2011.112

    Article  CAS  PubMed  Google Scholar 

  4. Shah A, Koticha A, Ubale M et al (2013) Identification and speciation of Malassezia in patients clinically suspected of having pityriasis versicolor. Indian J Dermatol 58:239. https://doi.org/10.4103/0019-5154.110841

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sumi CD, Yang BW, Yeo IC et al (2014) Antimicrobial peptides of the genus Bacillus : a new era for antibiotics. Can J Microbiol 61:93–103. https://doi.org/10.1139/cjm-2014-0613

    Article  CAS  PubMed  Google Scholar 

  6. Singh RP, Reddy CRK (2014) Seaweed-microbial interactions: Key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230. https://doi.org/10.1111/1574-6941.12297

    Article  CAS  PubMed  Google Scholar 

  7. Harwood CR, Mouillon JM, Pohl S et al (2018) Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev 42:721–738. https://doi.org/10.1093/femsre/fuy028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yang H, Li X, Li X et al (2015) Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal Bioanal Chem 407:2529–2542. https://doi.org/10.1007/s00216-015-8486-8

    Article  CAS  PubMed  Google Scholar 

  9. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009

    Article  CAS  PubMed  Google Scholar 

  10. Phister TG, O’Sullivan DJ, McKay LL (2004) Identification of bacilysin, chlorotetaine, and iturin A produced by Bacillus sp. strain CS93 isolated from pozol, a Mexican fermented maize dough. Appl. Environ Microbiol 70:631–634. https://doi.org/10.1128/AEM.70.1.631-634.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gustafson K, Roman M, Fenical W (1989) The Macrolactins, a novel class of antiviral and cytotoxic macrolides from a deep-Sea marine bacterium. J Am Chem Sci 111:7519–7524. https://doi.org/10.1021/ja00201a036

    Article  CAS  Google Scholar 

  12. Nastro RA, Arguelles-Arias A, Ongena M et al (2013) Antimicrobial activity of Bacillus amyloliquefaciens ANT1 toward pathogenic bacteria and mold: effects on biofilm formation. Probiotics Antimicrob 5:252–258. https://doi.org/10.1007/s12602-013-9143-1

    Article  CAS  Google Scholar 

  13. Filip R, Davicino R, Anesini C (2010) Antifungal activity of the aqueous extract of Ilex paraguariensis against Malassezia furfur. Phytother Res 24:715–719. https://doi.org/10.1002/ptr.3004

    Article  PubMed  Google Scholar 

  14. Sala A, Cabassi CS, Santospirito D, Polverini E, Flisi S, Cavirani S et al (2018) Novel Naja atra cardiotoxin1 (CTX-1) derived antimicrobial peptides with broad spectrum activity. PLoS ONE 13:e0190778. https://doi.org/10.1371/journal.pone.0190778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Huang N, Siegel MM, Kruppa GH, Laukien FH (1999) Automation of a Fourier transform ion cyclotron resonance mass spectrometer for acquisition, analysis, and e-mailing of high-resolution exact-mass electrospray ionization mass spectral data. J Am Soc Mass Spectrom 10:1166–1173. https://doi.org/10.1021/jasms.8b01270

    Article  CAS  Google Scholar 

  16. Ma Y, Kong Q, Qin C, Chen Y, Chen Y, Lv R, Zhou G (2016) Identification of lipopeptides in Bacillus megaterium by two-step ultrafiltration and LC–ESI–MS/MS. AMB Express 6:79. https://doi.org/10.1186/s13568-016-0252-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tabbene O, Azaiez S, Di Grazia A, Karkouch I et al (2016) Bacillomycin D and its combination with amphotericin B: promising antifungal compounds with powerful antibiofilm activity and wound-healing potency. J Appl Microbiol 120:289–300. https://doi.org/10.1111/jam.13030

    Article  CAS  PubMed  Google Scholar 

  18. Noh K, Kim DH, Shin BS, Yun HY, Kim E, Kang W (2014) Simultaneous determination of 7-O-succinyl macrolactin A and its metabolite macrolactin A in rat plasma using liquid chromatography coupled to tandem mass spectrometry. J Pharm Biomed Anal 98:85–89. https://doi.org/10.1016/j.jpba.2014.05.009

    Article  CAS  PubMed  Google Scholar 

  19. Chen XH, Vater J, Piel J et al (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB42. J Bacteriol 188:4024–4036. https://doi.org/10.1128/JB.00052-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chakraborty K, Thilakan B, Raola VK, Joy M (2017) Antibacterial polyketides from Bacillus amyloliquefaciens associated with edible red seaweed Laurenciae papillosa. Food Chem 218:427–434. https://doi.org/10.1016/j.foodchem.2016.09.066

    Article  CAS  PubMed  Google Scholar 

  21. Mondol MA, Tareq FS, Kim JH, Lee MA, Lee HS, Lee JS, Lee YJ, Shin HJ (2013) New antimicrobial compounds from a marine-derived Bacillus sp. J Antibiot 66:89–95. https://doi.org/10.1038/ja.2012.102

    Article  CAS  Google Scholar 

  22. Nagao T, Adachi K, Sakai M, Nishijima M, Sano H (2001) Novel macrolactins as antibiotic lactones from a marine bacterium. J Antibiot 54:333–339. https://doi.org/10.7164/antibiotics.54.333

    Article  CAS  Google Scholar 

  23. Schneider K, Chen XH, Vater J et al (2007) Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42. J Nat Prod 70:1417–1423. https://doi.org/10.1021/np070070k

    Article  CAS  PubMed  Google Scholar 

  24. Zheng CJ, Lee S, Lee CH, Kim WG (2007) Macrolactins O-R, glycosylated 24-membered lactones from Bacillus sp. AH159–1. J Nat Prod 70:1632–1635. https://doi.org/10.1021/np0701327

    Article  CAS  PubMed  Google Scholar 

  25. Xue C, Tian L, Xu M, Deng Z, Lin W (2008) A new 24-membered lactone and a new polyene δ-lactone from the marine bacterium Bacillus marinus. J Antibiot 61:668–674. https://doi.org/10.1038/ja.2008.94

    Article  CAS  Google Scholar 

  26. Djoumbou-Feunang Y, Pon A, Karu N, Zheng J, Li C, Arndt D, Gautam M, Allen F, Wishart DS (2019) CFM-ID 3.0: Significantly improved ESI-MS/MS prediction and compound identification. Metabolites 9:72. https://doi.org/10.3390/metabo9040072

    Article  CAS  PubMed Central  Google Scholar 

  27. Wu L, Wu H, Chen L, Xie S, Zang H, Borriss R, Gao X (2014) Bacilysin from Bacillus amyloliquefaciens FZB42 has specific bactericidal activity against harmful algal bloom species. Appl Environ Microbiol 80:7512–7520. https://doi.org/10.1128/AEM.02605-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chakraborty K, Thilakan B, Raola VK (2014) Polyketide family of novel antibacterial 7-O-methyl-5′-hydroxy-3′-heptenoate-macrolactin from seaweed-associated Bacillus subtilis MTCC 10403. J Agr Food Chem 62:12194–12208. https://doi.org/10.1021/jf504845m

    Article  CAS  Google Scholar 

  29. Singh RP, Kumari P, Reddy CRK (2015) Antimicrobial compounds from seaweeds-associated bacteria and fungi. Appl Microbiol Biotechnol 99:1571–1586. https://doi.org/10.1007/s00253-014-6334-y

    Article  CAS  PubMed  Google Scholar 

  30. Rahnamaeian M, Vilcinskas A (2015) Short antimicrobial peptides as cosmetic ingredients to deter dermatological pathogens. Appl Microbiol Biot 99:8847–8855. https://doi.org/10.1007/s00253-015-6926-1

    Article  CAS  Google Scholar 

  31. Chen Y, Liu SA, Mou H (2017) Characterization of lipopeptide biosurfactants produced by Bacillus licheniformis MB01 from marine sediments. Front microbiol 8:871. https://doi.org/10.3389/fmicb.2017.00871

    Article  PubMed  PubMed Central  Google Scholar 

  32. Yuan J, Li B, Zhang N et al (2012) Production of bacillomycin- and macrolactin-type antibiotics by Bacillus amyloliquefaciens NJN-6 for suppressing soilborne plant pathogens. J Agr Food Chem 60:2976–2981. https://doi.org/10.1021/jf204868z

    Article  CAS  Google Scholar 

  33. Yuan J, Zhang F, Wu Y et al (2014) Recovery of several cell pellet-associated antibiotics produced by Bacillus amyloliquefaciens NJN-6. J Agr Food Chem 59:169–176. https://doi.org/10.1111/lam.12260

    Article  CAS  Google Scholar 

  34. Wu L, Wu H, Chen L et al (2015) Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci Rep 5:12975. https://doi.org/10.1038/srep12975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang T, Wu MB, Chen ZJ et al (2016) Separation, determination and antifungal activity test of the products from a new Bacillus amyloliquefaciens. Nat Prod Res 30:1215–1218. https://doi.org/10.1080/14786419.2015.1048246

    Article  CAS  PubMed  Google Scholar 

  36. Tabbene O, Di GA, Azaiez S et al (2015) Synergistic fungicidal activity of the lipopeptide bacillomycin D with amphotericin B against pathogenic Candida species. FEMS Yeast Res 15:fov022. https://doi.org/10.1093/femsyr/fov022

  37. Gu Q, Yang Y, Yuan Q, Shi G, Wu L et al (2017) Bacillomycin D produced by Bacillus amyloliquefaciens is involved in the antagonistic interaction with the plant-pathogenic fungus Fusarium graminearum. Appl Environ Microbiol 83:e01075-17. https://doi.org/10.1128/AEM.01075-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Koumoutsi A, Chen XH, Henne A et al (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J bacteriol 186:1084–1096. https://doi.org/10.1128/JB.186.4.1084-1096.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mondol MAM, Shin HJ, Islam MT (2013) Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Mar Drugs 11:2846–2872. https://doi.org/10.3390/md11082846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mondol MAM, Tareq FS, Kim JH et al (2011) Cyclic ether-containing macrolactins, antimicrobial 24-membered isomeric macrolactones from a marine Bacillus sp. J Nat Prod 74:2582–2587. https://doi.org/10.1021/np200487k

    Article  CAS  PubMed  Google Scholar 

  41. Mondol MAM, Shin HJ (2014) Antibacterial and antiyeast compounds from marine-derived bacteria. Mar Drugs 12:2913–2921. https://doi.org/10.3390/md12052913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Choi SW, Bai DH, Yu JH, Shin CS (2003) Characteristics of the squalene synthase inhibitors produced by a Streptomyces species isolated from soils. Can J Microbiol 49:663–668. https://doi.org/10.1139/W03-084

    Article  CAS  PubMed  Google Scholar 

  43. Patel H, Huynh Q, Bärlehner D et al (2014) Additive and synergistic membrane permeabilization by antimicrobial lipopeptides and detergents. Biophys J 106:2115–2125. https://doi.org/10.1016/j.bpj.2014.04.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Compaoré CS, Nielsen DS, Sawadogo-Lingani H et al (2013) Bacillus amyloliquefaciens ssp. plantarum strains as potential protective starter cultures for the production of Bikalga, an alkaline fermented food. J Appl Microbiol 115:133–146. https://doi.org/10.1111/jam.12214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank “Central instrumentation facility,” Savitribai Phule Pune University (SSPU) Maharashtra, India, for mass spectrometric analysis of samples.

Funding

This work was supported by the Praj Industries Ltd.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasmin Mirza.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vairagkar, U., Mirza, Y. Antagonistic Activity of Antimicrobial Metabolites Produced from Seaweed-Associated Bacillus amyloliquefaciens MTCC 10456 Against Malassezia spp.. Probiotics & Antimicro. Prot. 13, 1228–1237 (2021). https://doi.org/10.1007/s12602-021-09742-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09742-2

Keywords

Navigation