ANTIMICROBIAL ACTIVITY OF SURFACTANTS OF MICROBIAL ORIGIN T. P. Pirog, D. A. Lutsay, L. V. Kliuchka, K. A. Beregova

Details: Hits: 2600

ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

1 2019

"Biotechnologia Acta" V. 12, No 1, 2019
Р. 39-57, Bibliography 39-57, English
Universal Decimal Classification: 759.873.088.5:661.185
https://doi.org/10.15407/biotech12.01.039

ANTIMICROBIAL ACTIVITY OF SURFACTANTS OF MICROBIAL ORIGIN

T. P. Pirog, D. A. Lutsay, L. V. Kliuchka, K. A. Beregova

National University of Food Technologies, Kyiv, Ukraine

The recent literature data about the antibacterial and antifungal activity of microbial surfactants (lipopeptides synthesized by representatives of genera Bacillus, Paenibacillus, Pseudomonas, Brevibacillus, rhamnolipids of bacteria Pseudomonas, Burkholderia, Lysinibacillus sp., sophorolipids of yeasts Candida (Starmerella) and Rhodotorula), and our own experiments data concerning antimicrobial activity of surfactants synthesized by Acinetobacter calcoaceticus IMB B-7241, Rhodococcus erythropolis IMB Aс-5017 and Nocardia vaccini IMV B-7405 were presented.

The analysis showed that lipopeptides were more effective antimicrobial agents compared to glycolipids. Thus, the minimum inhibitory concentrations (MIC) of lipopeptides, ramnolipids and sophorolipids are on average (?g/ml): 1–32, 50–500, and 10–200, respectively. The MIC of surfactants synthesized by the IMV B-7241, IMV Ac-5017 and IMV B-7405 strains are comparable to those of the known microbial lipopeptides and glycolipids. The advantages of glycolipids as antimicrobial agents compared with lipopeptides were the possibility of their synthesis on industrial

waste and the high concentration of synthesized surfactants. The literature data and our own results indicate the need to study the influence of microbes’ cultivation conditions on the antimicrobial activity of the final product.

Key words: microbial lipopeptides, rhamnolipids and sophorolipids, antibacterial and antifungal Activity.

{accordion title="References" open="false"}

1. Santos D. K., Rufino R. D., Luna J. M., Santos V. A., Sarubbo L. A. Biosurfactants: multifunctional biomolecules of the 21st century. Int. J. Mol. Sci. 2016, 17 (3), 401. https://doi.org/10.3390/ijms17030401

2. Mnif I., Ghribi D. Glycolipid biosurfactants: main properties and potential applications in agriculture and food industry. J. Sci. Food Agric. 2016, 96 (13), 4310?4320. https://doi.org/10.1002/jsfa.7759

3. De Almeida D. G., Soares Da Silva R. C., Luna J. M., Rufino R. D., Santos V. A., Banat I. M., Sarubbo L. A. Biosurfactants: promising molecules for petroleum biotechnology advances. Front. Microbiol. 2016, V. 7, Р. 1718. https://doi.org/10.3389/fmicb.2016.01718

4. Arima K., Kakinuma A., Tamura G. Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation. Biochem. Biophys. Res. Commun. 1968, 31 (3), 488–494. https://doi.org/10.1016/0006-291X(68)90503-2

5. Katz E., Demain A. L. The peptide antibiotics of Bacillus: chemistry, biogenesis, and possible functions. Bacteriol. Rev. 1977, 41 (2), 449–474.

6. Jarvis F. G., Johnson M. J. A glyco-lipide produced by Pseudomonas aeruginosa. J. Am. Chem. Soc. 1949, 71 (12), 4124–4126. https://doi.org/10.1021/ja01180a073

7. Ito S., Honda H., Tomita F., Suzuki T. Rhamnolipids produced by Pseudomonas aeruginosa grown on n-paraffin (mixture of C12, C13 and C14 fractions). J. Antibiot (Tokyo). 1971, 24 (12), 855–859. https://doi.org/10.7164/antibiotics.24.855

8. Vollenbroich D., Pauli G., Оzel M., Vater J. Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis. Appl. Environ. Microbiol. 1997, 63 (1), 44–49.

9. Abalos А., Pinazo А., Infante М. R., Casals М., Garcіa F., Manresa A. Physicochemical and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa AT10 from soybean oil refinery wastes. Langmuir. 2001, 17 (5), 1367–1371. https://doi.org/10.1021/la0011735

10. Haba E., Pinazo A., Jauregui O., Espuny M. J., Infante M. R., Manresa A. Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol. Bioeng. 2003, 81 (3), 316–322. https://doi.org/10.1002/bit.10474

11. Singh P., Cameotra S. S. Potential applications of microbial surfactants in biomedical sciences. Trends Biotechnol. 2004, 22 (3), 142–146. https://doi.org/10.1016/j.tibtech.2004.01.010

12. Yilmaz E. S., Sidal U. Investigation of antimicrobial effects of a Pseudomonas-originated biosurfactant. Biologia. 2005, 60 (6), 723–725.

13. Cameotra S. S., Makkar R. S. Recent applications of biosurfactants as biological and immunological molecules. Curr. Opin. Microbiol. 2006, 7 (3), 262–266. https://doi.org/10.1016/j.mib.2004.04.006

14. Cort?s-S?nchez Ade J., Hern?ndez-S?nchez H., Jaramillo-Flores M. E. Biological activity of glycolipids produced by microorganisms: new trends and possible therapeutic alternatives. Microbiol. Res. 2013, 168 (1), 22–32. https://doi.org/10.1016/j.micres.2012.07.002

15. Meena K. R., Kanwar S. S. Lipopeptides as the antifungal and antibacterial agents: applications in food safety and therapeutics. Biomed. Res. Int. 2015. https://doi.org/10.1155/2015/473050

16. Cochrane S. A., Vederas J. C. Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med. Res. Rev. 2016, 36 (1), 4–31. https://doi.org/10.1002/med.21321

17. Zhao H., Shao D., Jiang C., Shi J., Li Q., Huang Q., Rajoka M. S. R, Yang H., Jin M. Biological activity of lipopeptides from Bacillus. Appl. Microbiol. Biotechnol. 2017, 101 (15), 5951–5960. https://doi.org/10.1007/s00253-017-8396-0

18. Abdel-Mawgoud A. M., Stephanopoulos G. Simple glycolipids of microbes: Chemistry, biological activity and metabolic engineering. Synth. Syst. Biotechnol. 2018, 3 (1), 3–19. https://doi.org/10.1016/j.synbio.2017.12.001

19. Hajfarajollah H., Eslami P. Mokhtarani https://iubmb.onlinelibrary.wiley.com/action/doSearch?ContribAuthorStored=Eslami%2C+ParisaB., Akbari Noghabi K. Biosurfactants from probiotic bacteria: A review. Biotechnol. Appl. Biochem. 2018, V. 18, Р. 768–783. https://doi.org/10.1002/bab.1686. http://orcid.org/0000-0002-9717-7237

20. Torres M. J., Petroselli G., Daz M., Erra-Balsells R., Audisio M. C. Bacillus subtilis subsp. subtilis CBMDC3f with antimicrobial activity against gram-positive foodborne pathogenic bacteria: UV-MALDI-TOF MS analysis of its bioactive compounds. World. J. Microbiol. Biotechnol. 2015, 31 (6), 929–940. https://doi.org/10.1007/s11274-015-1847-9

21. Sharma D., Ansari M. J., Gupta S., Al Ghamdi A., Pruthi P., Pruthi V. Structural characterization and antimicrobial activity of a biosurfactant obtained from Bacillus pumilus DSVP18 grown on potato peels. Jundishapur. J. Microbiol. 2015, 8 (9), e21257. https://doi.org/10.5812/jjm.21257

22. Ndlovu T., Rautenbach M., Vosloo J. A., Khan S., Khan W. Characterisation and antimicrobial activity of biosurfactant extracts produced by Bacillus amyloliquefaciens and Pseudomonas aeruginosa isolated from a wastewater treatment plant. AMB Express. 2017, 7 (1), 108. https://doi.org/10.1186/s13568-017-0363-8

23. Chen Y., Liu S. A., Mou H., Ma Y., Li M., Hu X. Characterization of lipopeptide biosurfactants produced by Bacillus licheniformis MB01 from marine sediments. Front. Microbiol. 2017, V. 8, Р. 871. https://doi.org/10.3389/fmicb.2017.00871

24. Baindara P., Mandal S. M., Chawla N., Singh P. K., Pinnaka A. K., Korpole S. Characterization of two antimicrobial peptides produced by a halotolerant Bacillus subtilis strain SK.DU.4 isolated from a rhizosphere soil sample. AMB Express. 2013, 3 (1), 2. https://doi.org/10.1186/2191-0855-3-2

25. Zhou Z., Liu F., Zhang X., Zhou X., Zhong Z., Su H., Li J., Li H., Feng F., Lan J., Zhang Z., Fu H., Hu Y., Cao S., Chen W., Deng J., Yu J., Zhang W., Peng G. Cellulose-dependent expression and antibacterial characteristics of surfactin from Bacillus subtilis HH2 isolated from the giant panda. PLoS One. 2018, 13 (1), e0191991. https://doi.org/10.1371/journal.pone.0191991

26. Fan H., Zhang Z., Li Y., Zhang X., Duan Y., Wang Q. Biocontrol of bacterial fruit blotch by Bacillus subtilis 9407 via surfactin-mediated antibacterial aActivity and colonization. Front Microbiol. 2017, V. 8, Р. 1973. https://doi.org/10.3389/fmicb.2017.01973

27. Saggese A., Culurciello R., Casillo A., Corsaro M. M., Ricca E., Baccigalupi L. A Marine isolate of Bacillus pumilus secretes a pumilacidin active against Staphylococcus aureus. Mar. Drugs. 2018, 16 (6), E180. https://doi.org/10.3390/md16060180

28. Pirog T. P., Paliichuk O. I., Iutynska G. O., Shevchuk T. A. Prospects of using microbial surfactants in plant growing. Mikrobiol. Zh. 2018, 80 (3), 115–135. (In Ukrainian). https://doi.org/10.15407/microbiolj80.03.115

29. Ramachandran R. Shrivastava M., Narayanan N. N., Thakur R. L., Chakrabarti A., Roy U. Evaluation of antifungal efficacy of three new cyclic lipopeptides of the class Bacillomycin from Bacillus subtilis RLID 12.1. Antimicrob. Agents. Chemother. 2018, 62 (1), e01457-17. https://doi.org/10.1128/AAC.01457-17

30. Liu J., Hagberg I., Novitsky L., Hadj-Moussa H., Avis T. J. Interaction of antimicrobial cyclic lipopeptides from Bacillus subtilis influences their effect on spore germination and membrane permeability in fungal plant pathogens. Fungal Biol. 2014, 118 (11), 855–861. https://doi.org/10.1016/j.funbio.2014.07.004

31. Mnif I., Hammami I., Triki M. A., Azabou M. C., Ellouze-Chaabouni S., Ghribi D. Antifungal efficiency of a lipopeptide biosurfactant derived from Bacillus subtilis SPB1 versus the phytopathogenic fungus. Fusarium solani. Environ. Sci. Pollut. Res. Int. 2015, 22 (22), 18137–18147. https://doi.org/10.1007/s11356-015-5005-6

32. Mnif I., Grau-Campistany A., Coronel-Le?n J., Hammami I., Triki M. A., Manresa A., Ghribi D. Purification and identification of Bacillus subtilis SPB1 lipopeptide biosurfactant exhibiting antifungal activity against Rhizoctonia bataticola and Rhizoctonia solani. Environ. Sci. Pollut. Res. Int. 2016, 23 (7), 6690–6699. https://doi.org/10.1007/s11356-015-5826-3

33. Mihalache G., Balaes T., Gostin I., Stefan M., Coutte F., Krier F. Lipopeptides produced by Bacillus subtilis as new biocontrol products against fusariosis in ornamental plants. Environ. Sci. Pollut. Res. Int. 2018, 25 (30), 29784–29793. https://doi.org/10.1007/s11356-017-9162-7

34. Singh A. K., Rautela R., Cameotra S. S. Substrate dependent in vitro antifungal activity of Bacillus sp. strain AR2. Microb. Cell Fact. 2014, V. 13, Р. 67. https://doi.org/10.1186/1475-2859-13-67

35. Sarwar A., Brader G., Corretto E., Aleti G., Abaidullah M., Sessitsch A., Hafeez F. Y. Qualitative analysis of biosurfactants from Bacillus species exhibiting antifungal activity. PLoS One. 2018, 13 (6), e0198107. https://doi.org/10.1371/journal.pone.0198107

36. Toral L., Rodr?guez M., B?jar V., Sampedro I. Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Front. Microbiol. 2018, V. 9, Р. 13–15. https://doi.org/10.3389/fmicb.2018.01315

37. Zihalirwa Kulimushi P., Arg?elles Arias A., Franzil L., Steels S., Ongena M. Stimulation of fengycin-type antifungal lipopeptides in Bacillus amyloliquefaciens in the presence of the maize fungal pathogen Rhizomucor variabilis. Front. Microbiol. 2017, V. 8, Р. 850. https://doi.org/10.3389/fmicb.2017.00850

38. Asari S., Ongena M., Debois D., De Pauw E., Chen K., Bejai S., Meijer J. Insights into the molecular basis of biocontrol of Brassica pathogens by Bacillus amyloliquefaciens UCMB5113 lipopeptides. Ann Bot. 2017, 120 (4), 551–562. https://doi.org/10.1093/aob/mcx089

39. Aw Y. K., Ong K. S., Lee L. H., Cheow Y. L., Yule C. M., Lee S. M. Newly isolated Paenibacillus tyrfis sp. nov., from Malaysian tropical peat swamp soil with broad spectrum antimicrobial activity. Front. Microbiol. 2016, V. 7, Р. 219. https://doi.org/10.3389/fmicb.2016.00219

40. Huang E., Yousef A. E. Paenibacterin, a novel broad-spectrum lipopeptide antibiotic, neutralises endotoxins and promotes survival in a murine model of Pseudomonas aeruginosa-induced sepsis. Int. J. Antimicrob. Agents. 2014, 44 (1), 74–77. https://doi.org/10.1016/j.ijantimicag.2014.02.018

41. Huang E., Yang X., Zhang L., Moon S. H., Yousef A. E. New Paenibacillus strain produces a family of linear and cyclic antimicrobial lipopeptides: cyclization is not essential for their antimicrobial activity. FEMS Microbiol. Lett. 2017, 364 (8). https://doi.org/10.1093/femsle/fnx049

42. Hiramoto M., Okada K., Nagai S. The revised structure of viscosin, a peptide antibiotic. Tetrahedron Lett. 1970, V. 14, Р. 1087–1090. https://doi.org/10.1016/S0040-4039(01)97915-8

43. Saini H. S., Barrag?n-Huerta B. E., Lebr?n-Paler A., Pemberton J. E., V?zquez R. R., Burns A. M., Marron M. T., Seliga C. J., Gunatilaka A. A., Maier R. M. Efficient purification of the biosurfactant viscosin from Pseudomonas libanensis strain M9-3 and its physicochemical and biological properties. J. Nat. Prod. 2008, 71 (6), 1011–1015. https://doi.org/10.1021/np800069u

44. Geudens N., Martins J. C. Cyclic Lipodepsipeptides from Pseudomonas spp. – biological swiss-army knives. Front. Microbiol. 2018, V. 9, Р. 1867. https://doi.org/10.3389/fmicb.2018.01867

45. Ma Z., Geudens N., Kieu N. P., Sinnaeve D., Ongena M., Martins J. C., H?fte M. Biosynthesis, chemical structure, and structure-activity relationship of orfamide lipopeptides produced by Pseudomonas protegens and related species. Front. Microbiol. 2016, V. 7, Р. 382. https://doi.org/10.3389/fmicb.2016.00382

46. Tazda?t D., Salah R., Mouffok S., Kabouche F., Keddou I., Abdi N., Grib H., Mameri N. Preliminary evaluation of a new low-cost substrate (amurca) in production of biosurfactant by Pseudomonas aeruginosa isolated from fuel-contaminated soil. J. Mater. Environ. Sci. 2018, 9 (3), 964–970.

47. Yang X., Huang E., Yuan C., Zhang L., Yousef A. E. Isolation and structural elucidation of brevibacillin, an antimicrobial lipopeptide from Brevibacillus laterosporus that combats drug-resistant gram-positive bacteria. Appl. Environ. Microbiol. 2016, 82 (9), 2763–2772. https://doi.org/10.1128/AEM.00315-16

48. Dalili D., Amini M., Faramarzi M. A., Fazeli M. R., Khoshayand M. R., Samadi N. Isolation and structural characterization of Coryxin, a novel cyclic lipopeptide from Corynebacterium xerosis NS5 having emulsifying and anti-biofilm activity. Colloids Surf. B Biointerfaces. 2015, V. 135, Р. 425–432. https://doi.org/10.1016/j.colsurfb.2015.07.005

49. Balan S. S., Kumar C. G., Jayalakshmi S. Aneurinifactin, a new lipopeptide biosurfactant produced by a marine Aneurinibacillus aneurinilyticus SBP-11 isolated from Gulf of Mannar: Purification, characterization and its biological evaluation. Microbiol. Res. 2017, V. 194, Р. 1–9. https://doi.org/10.1016/j.micres.2016.10.005

50. Sharma D., Mandal S. M., Manhas R. K. Purification and characterization of a novel lipopeptide from Streptomyces amritsarensis sp. nov. active against methicillin-resistant Staphylococcus aureus. AMB Express. 2014, V. 4, Р. 50. https://doi.org/10.1186/s13568-014-0050-y

51. Hajfarajollah H., Mokhtarani B., Noghabi K. A. Newly antibacterial and antiadhesive lipopeptide biosurfactant secreted by a probiotic strain, Propionibacterium freudenreichii. Appl. Biochem. Biotechnol. 2014, 174 (8), 2725–2740. https://doi.org/10.1007/s12010-014-1221-7

52. Mandal S. M., Sharma S., Pinnaka A. K., Kumari A., Korpole S. Isolation and characterization of diverse antimicrobial lipopeptides produced by Citrobacter and Enterobacter. BMC Microbiol. 2013, V. 13, Р. 152. https://doi.org/10.1186/1471-2180-13-152

53. In?s M., Dhouha G. Glycolipid biosurfactants: Potential related biomedical and biotechnological applications. Carbohydr. Res. 2015, 416, Р. 59–69. https://doi.org/10.1016/j.carres.2015.07.016

54. Sekhon Randhawa K. K., Rahman P. K. Rhamnolipid biosurfactants - past, present, and future scenario of global market. Front. Microbiol. 2014, V. 5, Р. 454. https://doi.org/10.3389/fmicb.2014.00454

55. Kiran G. S., Ninawe A. S., Lipton A. N., Pandian V., Selvin J. Rhamnolipid biosurfactants: evolutionary implications, applications and future prospects from untapped marine resource. Crit. Rev. Biotechnol. 2016, 36 (3), 399–415. https://doi.org/10.3109/07388551.2014.979758

56. Chen J., Wu Q., Hua Y., Chen J., Zhang H., Wang H. Potential applications of biosurfactant rhamnolipids in agriculture and biomedicine. Appl. Microbiol. Biotechnol. 2017, 101 (23–24), 8309–8319. https://doi.org/10.1007/s00253-017-8554-4

57. Henkel M., Geissler M., Weggenmann F., Hausmann R. Production of microbial biosurfactants: Status quo of rhamnolipid and surfactin towards large-scale production. Biotechnol J. 2017, 12 (7). https://doi.org/10.1002/biot.201600561

58. Chong H., Li Q. Microbial production of rhamnolipids: opportunities, challenges and strategies. Microb. Cell Fact. 2017, 16 (1), 137. https://doi.org/10.1186/s12934-017-0753-2

59. Irorere V. U., Tripathi L., Marchant R., McClean S., Banat I. M. Microbial rhamnolipid production: a critical re-evaluation of published data and suggested future publication criteria. Appl. Microbiol. Biotechnol. 2017, 101 (10), 3941?3951. https://doi.org/10.1007/s00253-017-8262-0

60. Tan Y. N., Li Q. Microbial production of rhamnolipids using sugars as carbon sources. Microb. Cell Fact. 2018, 17 (1), 89. https://doi.org/10.1186/s12934-018-0938-3

61. Tedesco P., Maida I., Palma Esposito F., Tortorella E., Subko K., Ezeofor C. C., Zhang Y., Tabudravu J., Jaspars M., Fani R., de Pascale D. Antimicrobial activity of monoramnholipids produced by bacterial strains isolated from the Ross Sea (Antarctica). Mar. Drugs. 2016, 14 (5). E83. https://doi.org/10.3390/md14050083

62. Chebbi A., Elshikh M., Haque F., Ahmed S., Dobbin S., Marchant R., Sayadi S., Chamkha M., Banat I. M. Rhamnolipids from Pseudomonas aeruginosa strain W10; as antibiofilm/antibiofouling products for metal protection. J. Basic Microbiol. 2017, 57 (5), 364–375. https://doi.org/10.1002/jobm.201600658

63. Elshikh M., Funston S., Chebbi A., Ahmed S., Marchant R., Banat I. M. Rhamnolipids from non-pathogenic Burkholderia thailandensis E264: Physicochemical characterization, antimicrobial and antibiofilm efficacy against oral hygiene related pathogens. N. Biotechnol. 2017, V. 36, Р. 26–36. https://doi.org/10.1016/j.nbt.2016.12.009

64. Aleksic I., Petkovic M., Jovanovic M., Milivojevic D., Vasiljevic B., Nikodinovic-Runic J., Senerovic L. Anti-biofilm properties of bacterial di-rhamnolipids and their semi-synthetic amide derivatives. Front. Microbiol. 2017, V. 8, 24–54. https://doi.org/10.3389/fmicb.2017.02454

65. Das P., Yang X. P., Ma L. Z. Analysis of biosurfactants from industrially viable Pseudomonas strain isolated from crude oil suggests how rhamnolipids congeners affect emulsification property and antimicrobial activity. Front. Microbiol. 2014, V. 5, Р. 696. https://doi.org/10.3389/fmicb.2014.00696

66. Sana S., Datta S., Biswas D., Sengupta D. Assessment of synergistic antibacterial activity of combined biosurfactants revealed by bacterial cell envelop damage. Biochim. Biophys. Acta Biomembr. 2018, 1860 (2), 579–585. https://doi.org/10.1016/j.bbamem.2017.09.027

67. Leite G. G., Figueir?a J. V., Almeida T. C. Val?es J. L., Marques W. F., Duarte M. D., Gorlach-Lira K. Production of rhamnolipids and diesel oil degradation by bacteria isolated from soil contaminated by petroleum. Biotechnol. Prog. 2016, 32 (2), 262–270. https://doi.org/10.1002/btpr.2208 https://doi.org/10.1002/btpr.220868. Haba E., Bouhdid S., Torrego-Solana N., Marqu?s A. M., Espuny M. J., Garc?a-Celma M. J., Manresa A. Rhamnolipids as emulsifying agents for essential oil formulations: antimicrobial effect against Candida albicans and methicillin-resistant Staphylococcus aureus. Int. J. Pharm. 2014, 476 (1–2), 134–141. https://doi.org/10.1016/j.ijpharm.2014.09.039

69. Oluwaseun A. C., Kola O. J., Mishra P., Singh J. R., Singh A. K., Cameotra S. S., Micheal B. O. Characterization and optimization of a rhamnolipid from Pseudomonas aeruginosa C1501 with novel biosurfactant activities. Sustainable Chem. Pharm. 2017, V. 6, Р. 26–36. https://doi.org/10.1016/j.scp.2017.07.001

70. Yan F., Xu S., Guo J., Chen Q., Meng Q., Zheng X. Biocontrol of post-harvest Alternaria alternata decay of cherry tomatoes with rhamnolipids and possible mechanisms of action. J. Sci. Food. Agric. 2015, 95 (7), 1469–1474. https://doi.org/10.1002/jsfa.6845

71. Deepika K. V., Sridhar P. R., Bramhachari P. V. Characterization and antifungal properties of rhamnolipids produced by mangrove sediment bacterium Pseudomonas aeruginosa strain KVD-HM52. Biocatal. Agric. Biotechnol. 2015, 4 (4), 608–615. https://doi.org/10.1016/j.bcab.2015.09.009

72. Rodrigues A. I., Gudi?a E. J., Teixeira J. A., Rodrigues L. R. Sodium chloride effect on the aggregation behaviour of rhamnolipids and their antifungal activity. Sci. Rep. 2017, 7 (1). https://doi.org/10.1038/s41598-017-13424-x

73. Oliveira M. R., Magri A., Baldo C., Camilios-Neto D., Minucelli T., Celligoi M. A. P. C. Sophorolipids a promising biosurfactant and its applications. Int. J. Adv. Biotechnol. Res. 2015, V. 6, Р. 161–174.

74. Dengle-Pulate V., Chandorkar P., Bhagwat S., Prabhune A. A. Antimicrobial and SEM studies of sophorolipids synthesized using lauryl alcohol. J. Surfactant Deterg. 2014, 17 (3), 543–552. https://doi.org/10.1007/s11743-013-1495-8

75. Zhang X., Ashby R., Solaiman D. K., Uknalis J., Fan X. Inactivation of Salmonella spp. and Listeria spp. by palmitic, stearic, and oleic acid sophorolipids and thiamine dilauryl sulfate. Front. Microbiol. 2016, V. 7, Р. 2076. https://doi.org/10.3389/fmicb.2016.02076

76. Morya V. K., Park J. H., Kim T. J., Jeon S., Kim E. K. Production and characterization of low molecular weight sophorolipid under fed-batch culture. Bioresour. Technol. 2013, V. 143, Р. 282–288. https://doi.org/10.1016/j.biortech.2013.05.094

77. Elshikh M., Moya-Ram?rez I., Moens H., Roelants S., Soetaert W., Marchant R., Banat I. M. Rhamnolipids and lactonic sophorolipids: natural antimicrobial surfactants for oral hygiene. J. Appl. Microbiol. 2017, 123 (5), 1111–1123. https://doi.org/10.1111/jam.13550

78. Solaiman D. K. Y., Ashby R. D., Birbir M., Caglayan P. Antibacterial activity of sophorolipids produced by Candida bombicola on gram-positive and gram-negative bacteria isolated from salted hides. JALCA. 2016, V. 111, Р. 358–364.

79. Solaiman D. K., Ashby R. D., Uknalis J. Characterization of growth inhibition of oral bacteria by sophorolipid using a microplate-format assay. J. Microbiol. Meth. 2017, V. 136, Р. 21–29. https://doi.org/10.1016/j.mimet.2017.02.012

80. Sen S., Borah S. N., Bora A., Deka S. Production, characterization, and antifungal activity of a biosurfactant produced by Rhodotorula babjevae YS3. Microb. Cell. Fact. 2017, 16 (1), 95. https://doi.org/10.1186/s12934-017-0711-z

81. Pirog T. P., Konon A. D., Sofilkanich A. P., Iutinskaia G. A. Effect of surface-active substances of Acinetobacter calcoaceticus IMV B-7241, Rhodococcus erythropolis IMV Ac-5017, and Nocardia vaccinii K-8 on phytopathogenic bacteria. Appl. Biochem. Microbiol. 2013, 49 (4), 360–367. https://doi.org/10.1134/S000368381304011X

82. Aleksic I., Petkovic M., Jovanovic M., Milivojevic D., Vasiljevic B., Nikodinovic-Runic J., Senerovic L. Anti-biofilm properties of bacterial di-rhamnolipids and their semi-synthetic amide derivatives. Front. Microbiol. 2017, V. 8, Р. 2454. https://doi.org/10.3389/fmicb.2017.02454

83. Ribeiro I. A., Bronze M. R., Castro M. F., Ribeiro M. H. Selective recovery of acidic and lactonic sophorolipids from culture broths towards the improvement of their therapeutic potential. Bioprocess. Biosyst. Eng. 2016, 39 (12), 1825?1837. https://doi.org/10.1007/s00449-016-1657-y

84. Wittgens A., Santiago-Schuebel B., Henkel M., Tiso T., Blank L. M., Hausmann R., Hofmann D., Wilhelm S., Jaeger K. E., Rosenau F. Heterologous production of long-chain rhamnolipids from Burkholderia glumae in Pseudomonas putida ? a step forward to tailor-made rhamnolipids. Appl. Microbiol. Biotechnol. 2017. https://doi.org/10.1007/s00253-017-8702-x

85. Zhihui X., Jiahui S., Bing L., Xin Y., Qirong S., Ruifu Z. Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl. Environ. Microbiol. 2013, 79 (3), 808?815. https://doi.org/10.1128/AEM.02645-12

86. Tiso T., Zauter R., Tulke H., Leuchtle B., Li W. J., Behrens B., Wittgens A., Rosenau F., Hayen H., Blank L. M. Designer rhamnolipids by reduction of congener diversity: production and characterization. Microb. Cell. Fact. 2017, 16 (1), 225. https://doi.org/10.1186/s12934-017-0838-y

87. Roelants S. L., Ciesielska K., De Maeseneire S. L., Moens H., Everaert B., Verweire S., Denon Q., Vanlerberghe B., Van Bogaert I. N., Van der Meeren P., Devreese B., Soetaert W. Towards the industrialization of new biosurfactants: Biotechnological opportunities for the lactone esterase gene from Starmerella bombicola. Biotechnol. Bioeng. 2016, 113 (3), 550?559. https://doi.org/10.1002/bit.25815

88. Pirog T. P., Sidor I. V., Lutsai D. A. Calcium and magnesium cations influence on antimicrobial and antiadhesive activity of Acinetobacter сalcoaceticus ІMV B-7241 surfactants. Biotechnol. acta. 2016, 9 (6), 50–57. https://doi.org/10.15407/biotech9.06.050

89. Pirog T. P., Nikituk L. V., Shevchuk T. A. Influence of divalent cations on synthesis of Nocardia vaccinii ІMV B-7405 surfactants with high antimicrobial and anti-Adhesion activity. Mikrobiol. Zh. 2017, 79 (5), 13–22. (In Ukrainian). https://doi.org/10.15407/microbiolj79.05.013

90. Pirog T. P., Shevchuk T. A., Petrenko N. M., Paliichuk O. I., Iutynska G. O. Influence of cultivation conditions of Rhodococcus erythropolis IMV Ac-5017 on the properties of synthesized surfactants. Mikrobiol. Zh. 2018, 80 (4), 13–27. (In Ukrainian). https://doi.org/10.15407/microbiolj80.04.013

{/accordions}