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3 Biotech

, 8:444 | Cite as

Isolation and characterization of cyclic lipopeptides with broad-spectrum antimicrobial activity from Bacillus siamensis JFL15

  • Ben-Hong Xu
  • Zhi-Wei Ye
  • Qian-Wang Zheng
  • Tao Wei
  • Jun-Fang Lin
  • Li-Qiong Guo
Original Article

Abstract

In this research, the antimicrobial substance anti-JFL15 was partially purified using a simple two-step extraction process from the cell-free supernatants of Bacillus siamensis JFL15. Anti-JFL15 exhibited a strong antibacterial activity against various multidrug-resistant aquatic bacterial pathogens, including Escherichia coli, Edwardsiella tarda, Pseudomonas aeruginosa, Aeromonas hydrophila, and Vibrio. Liquid chromatography–mass spectrometry revealed that anti-JFL15 contained eight cyclic lipopeptides belonging to two families: bacillomycin F (m/z 1056.56–1084.59) and surfactin (m/z 1007.65–1049.70) analogs. PCR analysis showed the presence of genes (i.e., sfp gene, surfactin synthetase D, fengycin synthetase B, iturin synthetase A, iturin synthetase C and bacillomycin synthetase D) involved in the biosynthesis of cyclic lipopeptides. This study is the first to identify cyclic lipopeptides from B. siamensis and use them to suppress the growth of various multidrug-resistant aquatic bacterial pathogens. Results indicated that B. siamensis JFL15 is a promising biocontrol agent for the effective and environmentally friendly control of various multidrug-resistant aquatic bacterial pathogens.

Keywords

Bacillus siamensis Cyclic lipopeptide Multidrug-resistant aquatic bacterial pathogen Pathogenic fungi Antimicrobial activity 

Notes

Acknowledgements

We would like to thank the Projects of Science and Technology of Guangdong Province (Grant numbers 2015A020209121, 2015A030313425 and 2015A030310225), and the Project of Science and Technology of Guangzhou City (Grant number 201607010197) supported this work. We are grateful to Professor Erxun Zhou for his kind providing of indicator fungi strains M. grisea and R. solani, and Professor Zaiguang Fang of Hainan University Institute of Marine for his kind providing of indicator bacteria.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest about this research.

References

  1. Abdullah, Asghar A, Butt MS, Shahid M, Huang Q (2017) Evaluating the antimicrobial potential of green cardamom essential oil focusing on quorum sensing inhibition of Chromobacterium violaceum. J Food Sci Technol 54(8):2306–2315.  https://doi.org/10.1007/s13197-017-2668-7 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abriouel H, Franz CMAP, Omar NB, Galvez A (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35:201–232.  https://doi.org/10.1111/j.1574-6976.2010.00244.x CrossRefPubMedGoogle Scholar
  3. Ali SS, Shaaban MT, Abomohra AE-F, El-Safity K (2016) Macroalgal activity against multiple drug resistant Aeromonas hydrophila: a novel treatment study towards enhancement of fish growth performance. Microb Pathog 101:89–95.  https://doi.org/10.1016/j.micpath.2016.10.026 CrossRefPubMedGoogle Scholar
  4. An J, Zhu W, Liu Y, Zhang XM, Sun LJ, Hong PZ, Wang YL, Xu CH, Xu DF, Liu HM (2015) Purification and characterization of a novel bacteriocin CAMT2 produced by Bacillus amyloliquefaciens isolated from marine fish Epinephelus areolatus. Food Control 51:278–282.  https://doi.org/10.1016/j.foodcont.2014.11.038 CrossRefGoogle Scholar
  5. Baltz RH (2017) Gifted microbes for genome mining and natural product discovery. J Ind Microbiol Biotechnol 44:573–588.  https://doi.org/10.1007/s10295-016-1815-x CrossRefPubMedGoogle Scholar
  6. Barbosa J, Caetano T, Mendo S (2015) Class I and Class II lanthipeptides produced by Bacillus spp. J Nat Prod 78:2850–2866.  https://doi.org/10.1021/np500424y CrossRefPubMedGoogle Scholar
  7. Chakraborty K, Thilakan B, Kizhakkekalam VK (2017a) Antibacterial aryl-crowned polyketide from Bacillus subtilis associated with seaweed Anthophycus longifolius. ARPN J Eng Appl Sci 12:3218–3221.  https://doi.org/10.1111/ijlh.12426 CrossRefGoogle Scholar
  8. Chakraborty K, Thilakan B, Raola VK (2017b) Previously undescribed antibacterial polyketides from heterotrophic Bacillus amyloliquefaciens associated with seaweed Padina gymnospora. Appl Biochem Biotechnol 184:1–17.  https://doi.org/10.1007/s12010-017-2562-9 CrossRefGoogle Scholar
  9. Chen Y, Li J, Xiao P, Li GY, Yue S, Huang J, Zhu WY, Mo ZL (2016) Isolation and characterization of Bacillus spp. M001 for potential application in turbot (Scophthalmus maximus L.) against Vibrio anguillarum. Aquac Nutr 22:374–381.  https://doi.org/10.1111/anu.12259 CrossRefGoogle Scholar
  10. Chen YL, Liu SA, Mou HJ, Ma YX, Li M, Hu XK (2017) Characterization of lipopeptide biosurfactants produced by Bacillus licheniformis MB01 from marine sediments. Front Microbiol 8:1–11.  https://doi.org/10.3389/fmicb.2017.00871 CrossRefGoogle Scholar
  11. Cheng AC, Lin HL, Shiu YL, Tyan YC, Liu CH (2017) Isolation and characterization of antimicrobial peptides derived from Bacillus subtilis E20-fermented soybean meal and its use for preventing Vibrio infection in shrimp aquaculture. Fish Shellfish Immunol 67:270–279.  https://doi.org/10.1016/j.fsi.2017.06.006 CrossRefPubMedGoogle Scholar
  12. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clement C, Barka EA, Jacquard C, Dorey S (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:177–187.  https://doi.org/10.1111/mpp.12170 CrossRefPubMedGoogle Scholar
  13. Franco R, Martín L, Arenal A, Santiesteban D, Sotolongo J, Cabrera H, Mejías J, Rodríguez G, Moreno AG, Pimentel E, Castillo NM (2017) Evaluation of two probiotics used during farm production of white shrimp Litopenaeus vannamei (Crustacea: Decapoda). Aquac Res 48:1936–1950.  https://doi.org/10.1111/are.13031 CrossRefGoogle Scholar
  14. Guo L, Guo J, Xu F (2017) Optimized extraction process and identification of antibacterial substances from Rhubarb against aquatic pathogenic Vibrio harveyi. 3 Biotech 7:377.  https://doi.org/10.1007/s13205-017-1012-2 CrossRefPubMedGoogle Scholar
  15. Gupta A, Geetika V, Gupta P (2016) Growth performance, feed utilization, digestive enzyme activity, innate immunity and protection against Vibrio harveyi of freshwater prawn, Macrobrachium rosenbergii fed diets supplemented with Bacillus coagulans. Aquac Int 24:1379–1392.  https://doi.org/10.1007/s10499-016-9996-x CrossRefGoogle Scholar
  16. Jasim B, Sreelakshmi KS, Mathew J, Radhakrishnan EK (2016) Surfactin, iturin, and fengycin biosynthesis by endophytic Bacillus sp. from Bacopa monnieri. Microb Ecol 72:106–119.  https://doi.org/10.1007/s00248-016-0753-5 CrossRefPubMedGoogle Scholar
  17. Jauregi P, Coutte F, Catiau L, Lecouturier D, Jacques P (2013) Micelle size characterization of lipopeptides produced by B. subtilis and their recovery by the two-step ultrafiltration process. Sep Purif Technol 104:175–182.  https://doi.org/10.1016/j.seppur.2012.11.017 CrossRefGoogle Scholar
  18. Kim YO, Park IS, Kim DJ, Nam BH, Kim DG, Jee YJ, An CM (2014) Identification and characterization of a bacteriocin produced by an isolated Bacillus sp. SW1-1 that exhibits antibacterial activity against fish pathogens. J Korean Soc Appl Biol Chem 57:605–612.  https://doi.org/10.1007/s13765-014-4174-1 CrossRefGoogle Scholar
  19. Kim K, Lee Y, Ha A, Kim JI, Park AR, Yu NH, Son H, Choi GJ, Park HW, Lee CW, Lee T, Lee YW, Kim JC (2017) Chemosensitization of Fusarium graminearum to chemical fungicides using cyclic lipopeptides produced by Bacillus amyloliquefaciens strain JCK-12. Front Plant Sci 8:1–16.  https://doi.org/10.3389/fpls.2017.02010 CrossRefGoogle Scholar
  20. Lee MH, Lee J, Nam YD, Lee JS, Seo MJ, Yi SH (2016) Characterization of antimicrobial lipopeptides produced by Bacillus sp. LM7 isolated from chungkookjang, a Korean traditional fermented soybean food. Int J Food Microbiol 221:12–18.  https://doi.org/10.1016/j.ijfoodmicro.2015.12.010 CrossRefPubMedGoogle Scholar
  21. Lim JH, Jeong HY, Kim SD (2011) Characterization of the bacteriocin J4 produced by Bacillus amyloliquefaciens j4 isolated from Korean traditional fermented soybean paste. J Appl Biol Chem 54:468–474.  https://doi.org/10.3839/jksabc.2011.072 CrossRefGoogle Scholar
  22. Liu XF, Li Y, Li JR, Cai LY, Li XX, Chen JR, Lyu SX (2015) Isolation and characterisation of Bacillus spp. antagonistic to Vibrio parahaemolyticus for use as probiotics in aquaculture. World J Microbiol Biotechnol 31:795–803.  https://doi.org/10.1007/s11274-015-1833-2 CrossRefPubMedGoogle Scholar
  23. Meidong R, Doolgindachbaporn S, Jamjan W, Sakai K, Tashiro Y, Okugawa Y, Tongpim S (2017) A novel probiotic Bacillus siamensis B44v isolated from Thai pickled vegetables (Phak-dong) for potential use as a feed supplement in aquaculture. J Gen Appl Microbiol 63:246–253.  https://doi.org/10.2323/jgam.2016.12.002 CrossRefPubMedGoogle Scholar
  24. Moyne AL, Shelby R, Cleveland TE, Tuzun S (2001) Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J Appl Microbiol 90:622–629.  https://doi.org/10.1046/j.1365-2672.2001.01290.x CrossRefPubMedGoogle Scholar
  25. Niazi A, Manzoor S, Asari S, Bejai S, Meijer J, Bongcam-rudloff E (2014) Genome analysis of Bacillus amyloliquefaciens subsp. plantarum UCMB5113: a rhizobacterium that improves plant growth and stress management. PLoS One 9:e104651.  https://doi.org/10.1371/journal.pone.0104651 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Pathak KV, Keharia H (2014) Identification of surfactins and iturins produced by potent fungal antagonist, Bacillus subtilis K1 isolated from aerial roots of banyan (Ficus benghalensis) tree using mass spectrometry. 3 Biotech 4:283–295.  https://doi.org/10.1007/s13205-013-0151-3 CrossRefPubMedGoogle Scholar
  27. Perez-Sanchez T, Ruiz-Zarzuela I, Blas ID, Balcazar JL (2014) Probiotics in aquaculture: a current assessment. Rev Aquac 6:133–146.  https://doi.org/10.1111/raq.12033 CrossRefGoogle Scholar
  28. Ramarathnam R, Bo S, Chen Y, Dilantha Fernando WG, Gao XW, Kievit TD (2007) Molecular and biochemical detection of fengycin- and bacillomycin D-producing Bacillus spp., antagonistic to fungal pathogens of canola and wheat. Can J Microbiol 53:901–911.  https://doi.org/10.1139/W07-049 CrossRefPubMedGoogle Scholar
  29. Ravindran C, Varatharajan GR, Rajasabapathy R (2016) Antibacterial activity of marine Bacillus substances against Vibrio cholerae and Staphylococcus aureus and in vivo evaluation using embryonic zebrafish test system. 78:417–422Google Scholar
  30. Shi BH, Zheng H, Huang JZ, Luo XZ, Luo XL (2015) Purification and partial characterization of a thermostable antimicrobial protein from Bacillus subtilis FB123. World J Microbiol Biotechnol 31:1285–1290.  https://doi.org/10.1007/s11274-015-1871-9 CrossRefPubMedGoogle Scholar
  31. Silva EF, Soares MA, Calazans NF, Vogeley JL, Valle BC, Soares R, Peixoto S (2012) Effect of probiotic (Bacillus spp.) addition during larvae and postlarvae culture of the white shrimp Litopenaeus vannamei. Aquac Res 44:13–21.  https://doi.org/10.1111/j.1365-2109.2011.03001.x CrossRefGoogle Scholar
  32. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857.  https://doi.org/10.1111/j.1365-2958.2005.04587.x CrossRefPubMedGoogle Scholar
  33. Sumi CD, Yang BW, Yeo I-C, Hahm YT (2015) 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 CrossRefPubMedGoogle Scholar
  34. Tanaka K, Amaki Y, Ishihara A, Nakajima H (2015) Synergistic effects of [Ile7]surfactin homologues with bacillomycin D in suppression of gray mold disease by Bacillus amyloliquefaciens biocontrol strain SD-32. J Agric Food Chem 63:5344–5353.  https://doi.org/10.1021/acs.jafc.5b01198 CrossRefPubMedGoogle Scholar
  35. Touraki M, Frydas I, Karamanlidou G, Mamara A (2012) Partial purification and characterization of a bacteriocin produced by Bacillus subtilis NCIMB 3610 that exhibits antimicrobial activity against fish pathogens. J Biol Res 18:310–319Google Scholar
  36. Xiu PY, Liu R, Zhang DC, Sun CM (2017) Pumilacidin-like lipopeptides derived from marine bacterium Bacillus sp. strain 176 suppress the motility of Vibrio alginolyticus. Appl Environ Microbiol 83:e00450–e00417CrossRefGoogle Scholar
  37. Xu DF, Wang YL, Sun LJ, Liu HM, Li JR (2013) Inhibitory activity of a novel antibacterial peptide AMPNT-6 from Bacillus subtilis against Vibrio parahaemolyticus in shrimp. Food Control 30:58–61.  https://doi.org/10.1016/j.foodcont.2012.07.025 CrossRefGoogle Scholar
  38. Xu HM, Rong YJ, Zhao MX, Song B, Chi ZM (2014) Antibacterial activity of the lipopetides produced by Bacillus amyloliquefaciens M1 against multidrug-resistant Vibrio spp. isolated from diseased marine animals. Appl Microbiol Biotechnol 98:127–136.  https://doi.org/10.1007/s00253-013-5291-1 CrossRefPubMedGoogle Scholar
  39. Yang H, Li X, Li X, Yu HM, Shen ZY (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 CrossRefPubMedGoogle Scholar
  40. Zhang B, Dong CJ, Shang QM, Cong Y, Kong WJ, Li PL (2013) Purification and partial characterization of bacillomycin L produced by Bacillus amyloliquefaciens K103 from lemon. Appl Biochem Biotechnol 171:2262–2272.  https://doi.org/10.1007/s12010-013-0424-7 CrossRefPubMedGoogle Scholar
  41. Zhang Q, Yu HR, Tong T, Tong WP, Dong LF, Xu MZ, Wang ZC (2014) Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish Shellfish Immunol 38:7–14.  https://doi.org/10.1016/j.fsi.2014.02.008 CrossRefPubMedGoogle Scholar
  42. Zhao J, Wu YX, Ho HH, Chen ZJ, Li XY, He YQ (2016) PBT1, a novel antimicrobial protein from the biocontrol agent Bacillus subtilis XF-1 against Plasmodiophora brassicae. Eur J Plant Pathol 145:583–590.  https://doi.org/10.1007/s10658-016-0905-y CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Food Science and Institute of Food BiotechnologySouth China Agricultural UniversityGuangzhouChina
  2. 2.Research Center for Micro-Ecological Agent Engineering and Technology of Guangdong ProvinceGuangzhouChina

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