Antibiotic activity and resistance of lactic acid bacteria and other antagonistic bacteriocin-producing microorganisms

Yong Yang ^a

Olga O. Babich ^b

Stanislav A. Sukhikh ^b

Maria I. Zimina ^b

Irina S. Milentyeva ^c

Affiliation

a Qiqihar University, Qiqihar, China

b Immanuel Kant Baltic Federal University, Kaliningrad, Russia

c Kemerovo State University, Kemerovo, Russia

Copyright ©Yang et al. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0. (http://creativecommons.org/licenses/by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.

Received 29 June, 2020 | Accepted in revised form 14 July, 2020 | Published 25 August, 2020

DOI: http://doi.org/10.21603/2308-4057-2020-2-377-384

Abstract

Introduction. Increased resistance of microorganisms to traditional antibiotics has created a practical need for isolating and synthesizing new antibiotics. We aimed to study the antibiotic activity and resistance of bacteriocins produced by lactic acid bacteria and other microorganisms.
Study objects and methods. We studied the isolates of the following microorganism strains: Bacillus subtilis, Penicillium glabrum, Penicillium lagena, Pseudomonas koreenis, Penicillium ochrochloron, Leuconostoc lactis, Lactobacillus plantarum, Leuconostoc mesenteroides, Pediococcus acidilactici, Leuconostoc mesenteroides, Pediococcus pentosaceus, Lactobacillus casei, Lactobacillus fermentum, Bacteroides hypermegas, Bacteroides ruminicola, Pediococcus damnosus, Bacteroides paurosaccharolyticus, Halobacillus profundi, Geobacillus stearothermophilus, and Bacillus caldotenax. Pathogenic test strains included Escherichia coli, Salmonella enterica, Staphylococcus aureus, Pseudomonas aeruginosa, Bacillus mycoides, Alcaligenes faecalis, and Proteus vulgaris. The titer of microorganisms was determined by optical density measurements at 595 nm.
Results and discussion. We found that eleven microorganisms out of twenty showed high antimicrobial activity against all test strains of pathogenic and opportunistic microorganisms. All the Bacteroides strains exhibited little antimicrobial activity against Gramnegative test strains, while Halobacillus profundi had an inhibitory effect on Gram-positive species only. The Penicillium strains also displayed a slight antimicrobial effect on pathogenic test strains.
Conclusion. The antibiotic resistance of the studied lactic acid bacteria and other bacteriocin-producing microorganisms allows for their use in the production of pharmaceutical antibiotic drugs.

Keywords

Lactic acid bacteria, bacteriocins, antibiotic properties, antibiotic resistance, natural sources, isolates

FUNDING

The study was part of the federal targeted program on “Obtaining Pharmaceutical Substances Based on Antagonist Microorganisms Isolated from Natural Sources” (Unique Project Identifier RFMEFI57418X0207) under Agreements No. 075-02- 2018-1934 of December 20, 2018 and No. 075-15-2019-1383 of June 18, 2019 of the Ministry of Science and Higher Education of the Russian Federation (Minobrnauka).

REFERENCES

Cavera VL, Arthur TD, Kashtanov D, Chikindas ML. Bacteriocins and their position in the next wave of conventional antibiotics. International Journal of Antimicrobial Agents. 2015;46(5):494–501. DOI: https://doi.org/10.1016/j.ijantimicag.2015.07.011.
Bindiya ES, Bhat SG. Marine bacteriocins: A review. Journal of Bacteriology and Mycology: Open Access. 2016;2(5):140–147. DOI: https://doi.org/10.15406/jbmoa.2016.02.00040.
Yongkiettrakul S, Maneerat K, Arechanajan B, Malila Y, Srimanote P, Gottschalk M, et al. Antimicrobial susceptibility of Streptococcus suis isolated from diseased pigs, asymptomatic pigs, and human patients in Thailand. BMC Veterinary Research. 2019;15(1). DOI: https://doi.org/10.1186/s12917-018-1732-5.
De Freire Bastos MC, Coelho MLV, da Silva Santos OC. Resistance to bacteriocins produced by Gram-positive bacteria. Microbiology. 2015;161(4):683–700. DOI: https://doi.org/10.1099/mic.0.082289-0.
Noda M, Miyauchi R, Danshiitsoodol N, Matoba Y, Kumagai T, Sugiyama M. Expression of genes involved in bacteriocin production and self-resistance in Lactobacillus brevis 174A is mediated by two regulatory proteins. Applied and Environmental Microbiology. 2018;84(7). DOI: https://doi.org/10.1128/AEM.02707-17.
Kumariya R, Garsa AK, Rajput YS, Sood SK, Akhtar N, Patel S. Bacteriocins: Classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microbial Pathogenesis. 2019;128:171–177. DOI: https://doi.org/10.1016/j.micpath.2019.01.002.
Ahmad V, Khan MS, Jamal QMS, Alzohairy MA, Al Karaawi MA, Siddiqui MU. Antimicrobial potential of bacteriocins: in therapy, agriculture and food preservation. International Journal of Antimicrobial Agents. 2017;49(1):1–11. DOI: https://doi.org/10.1016/j.ijantimicag.2016.08.016.
Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics and Antimicrobial Proteins. 2014;6(3–4):177–185. DOI: https://doi.org/10.1007/s12602-014-9162-6.
Ghazaryan L, Tonoyan L, Ashhab AA, Soares MIM, Gillor O. The role of stress in colicin regulation. Archives of Microbiology. 2014;196(11):753–764. DOI: https://doi.org/10.1007/s00203-014-1017-8.
Cramer WA, Sharma O, Zakharov SD. On mechanisms of colicin import: the outer membrane quandary. Biochemical Journal. 2018;475(23):3903–3915. DOI: https://doi.org/10.1042/BCJ20180477.
Ghequire MGK, De Mot R. The tailocin tale: peeling off phage tails. Trends in Microbiology. 2015;23(10):587–590. DOI: https://doi.org/10.1016/j.tim.2015.07.011.
Gupta VG, Pandey A. New and future developments in microbial biotechnology and bioengineering. Microbial Secondary Metabolites Biochemistry and Applications. Netherlands: Elsevier; 2019. 213 p.
Zhao Z, Orfe LH, Liu J, Lu S-Y, Besser TE, Call DR. Microcin PDI regulation and proteolytic cleavage are unique among known microcins. Scientific Reports. 2017;7. DOI: https://doi.org/10.1038/srep42529.
Ge J, Kang J, Ping W. Effect of acetic acid on bacteriocin production by Gram-positive bacteria. Journal of Microbiology and Biotechnology. 2019;29(9):1341–1348. DOI: https://doi.org/10.4014/jmb.1905.05060.
Rebuffat S. Microcins and other bacteriocins: bridging the gaps between killing stategies, ecology and applications. In: Dorit RL, Roy SM, Riley MA, editors. The bacteriocins: current knowledge and future prospects. Wymondham: Caister Academic Press; 2016. pp. 11–34. DOI: https://doi.org/10.21775/9781910190371.02.
Wencewicz TA, Miller MJ. Sideromycins as pathogen-targeted antibiotics. In: Fisher JF, Mobashery S, Miller MJ, editors. Antibacterials. Volume 2. Cham: Springer; 2017. pp. 151–183. DOI: https://doi.org/10.1007/7355_2017_19.
Garcia-Gutierrez E, O’Connor PM, Colquhoun IJ, Vior NM, Rodriguez JM, Mayer MJ, et al. Production of multiple bacteriocins, including the novel bacteriocin gassericin M, by Lactobacillus gasseri LM19, a strain isolated from human milk. Applied Microbiology and Biotechnology. 2020;104(9):3869–3884. DOI: https://doi.org/10.1007/s00253-020-10493-3.
Egan K. Ross RP, Hill C. Bacteriocins: antibiotics in the age of the microbiome. Emerging Topics in Life Sciences. 2017;1(1):55–63. DOI: https://doi.org/10.1042/ETLS20160015.
Alvarez-Sieiro P, Montalbán-López M, Mu DD, Kuipers OP. Bacteriocins of lactic acid bacteria: extending the family. Applied Microbiology and Biotechnology. 2016;100(7):2939–2951. DOI: https://doi.org/10.1007/s00253-016-7343-9.
Sun Z, Wang X, Zhang X, Wu H, Zou Y, Li P, et al. Class III bacteriocin Helveticin-M causes sublethal damage on target cells through impairment of cell wall and membrane. Journal of Industrial Microbiology and Biotechnology. 2018;45(3):213–227. DOI: https://doi.org/10.1007/s10295-018-2008-6.
Tracanna V, De Jong A, Medema MH, Kuipers OP. Mining prokaryotes for antimicrobial compounds: from diversity to function. FEMS Microbiology Reviews. 2017;41(3):417–429. DOI: https://doi.org/10.1093/femsre/fux014.
Acedo JZ, Chiorean S, Vederas JC, van Belkum MJ. The expanding structural variety among bacteriocins from Grampositive bacteria. FEMS Microbiology Reviews. 2018;42(6):805–828. DOI: https://doi.org/10.1093/femsre/fuy033.
Ongey EL, Yassi H, Pflugmacher S, Neubauer P. Pharmacological and pharmacokinetic properties of lanthipeptides undergoing clinical studies. Biotechnology Letters. 2017;39(4):473–482. DOI: https://doi.org/10.1007/s10529-016-2279-9.
Wiebach V, Mainz A, Siegert MAJ, Jungmann NA, Lesquame G, Tirat S, et al. The anti-staphylococcal lipolanthines are ribosomally synthesized lipopeptides. Nature Chemical Biology. 2018;14(7):652–654. DOI: https://doi.org/10.1038/s41589-018-0068-6.
Bennallack PR, Griffitts JS. Elucidating and engineering thiopeptide biosynthesis. World Journal of Microbiology and Biotechnology. 2017;33(6). DOI: https://doi.org/10.1007/s11274-017-2283-9.
Lajis AFB. Biomanufacturing process for the production of bacteriocins from Bacillaceae family. Bioresources and Bioprocessing. 2020;7(1). DOI: https://doi.org/10.1186/s40643-020-0295-z.
Crone WJK, Vior NM, Santos-Aberturas J, Schmitz LG, Leeper FJ, Truman AW. Dissecting bottromycin biosynthesis using comparative untargeted metabolomics. Angewandte Chemie-International Edition. 2016;55(33):9639–9643. DOI: https://doi.org/10.1002/anie.201604304.
Hegemann JD, Zimmermann M, Xie X, Marahiel MA. Lasso peptides: an intriguing class of bacterial natural products. Accounts of Chemical Research. 2015;48(7):1909–1919. DOI: https://doi.org/10.1021/acs.accounts.5b00156.
Li Y, Ducasse R, Zirah S, Blond A, Goulard C, Lescop E, et al. Characterization of sviceucin from Streptomyces provides insight into enzyme exchangeability and disulfide bond formation in lasso peptides. ACS Chemical Biology. 2015;10(11):2641–2649. DOI: https://doi.org/10.1021/acschembio.5b00584.
Lear S, Munshi T, Hudson AS, Hatton C, Clardy J, Mosely JA, et al. Total chemical synthesis of lassomycin and lassomycin-amide. Organic and Biomolecular Chemistry. 2016;14(19):4534–4541. DOI: https://doi.org/10.1039/c6ob00631k.
Garvey M, Rowan NJ. Pulsed UV as a potential surface sanitizer in food production processes to ensure consumer safety. Current Opinion in Food Science. 2019;26:65–70. DOI: https://doi.org/10.1016/j.cofs.2019.03.003.
Metelev M, Tietz JI, Melby JO, Blair PM, Zhu LY, Livnat I, et al. Structure, bioactivity, and resistance mechanism of streptomonomicin, an unusual lasso peptide from an understudied halophilic actinomycete. Chemistry and Biology. 2015;22(2):241–250. DOI: https://doi.org/10.1016/j.chembiol.2014.11.017.
Chiorean S, Vederas JC, van Belkum MJ. Identification and heterologous expression of the sec-dependent bacteriocin faerocin MK from Enterococcus faecium M3K31. Probiotics and Antimicrobial Proteins. 2018;10(2):142–147. DOI: https://doi.org/10.1007/s12602-017-9374-7.
Sukhikh SA, Krumlikov VYu, Evsukova AO, Asyakina LK. Formation and study of symbiotic consortium of lactobacilli to receive a direct application starter. Foods and Raw Materials. 2017;5(1):51–62. DOI: https://doi.org/10.21179/2308-4057-2017-1-51-62.

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Yang Y, Babich OO, Sukhikh SA, Zimina MI, Milentyeva IS. Identification of total aromas of plant protein sources. Foods and Raw Materials. 2020;8(2):377–384. DOI: http://doi.org/10.21603/2308-4057-2020-2-377-384

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