1,112
Views
0
CrossRef citations to date
0
Altmetric
Review Articles

Nisin resistance in Gram-positive bacteria and approaches to circumvent resistance for successful therapeutic use

, , , &
Pages 376-385 | Received 03 Nov 2020, Accepted 11 Feb 2021, Published online: 09 Mar 2021

References

  • Alves FCB, Albano M, Andrade BFMT, Chechi JL, Pereira AFM, Furlanetto A, Rall VLM, Fernandes AAH, dos Santos LD, Barbosa LN, et al. 2020. Comparative proteomics of methicillin-resistant staphylococcus aureus subjected to synergistic effects of the Lantibiotic Nisin and Oxacillin. Microb Drug Resist. 26(3):179–189.
  • Angelopoulou A, Field D, Pérez-Ibarreche M, Warda AK, Hill C, Ross RP. 2020. Vancomycin and nisin A are effective against biofilms of multi-drug resistant Staphylococcus aureus isolates from human milk. PLoS One. 15(5):e0233284.
  • Arii K, Kawada-Matsuo M, Oogai Y, Noguchi K, Komatsuzawa H. 2019. Single mutations in BraRS confer high resistance against nisin A in Staphylococcus aureus. Microbiologyopen e791. 8(11):791.
  • Arnusch CJ, Bonvin AMJJ, Verel AM, Jansen WTM, Liskamp RMJ, de Kruijff B, Pieters RJ, Breukink E. 2008. The vancomycin-nisin(1-12) hybrid restores activity against vancomycin resistant enterococci. Biochemistry. 47(48):12661–12663.
  • Begley M, Cotter PD, Hill C, Ross RP. 2010. Glutamate decarboxylase-mediated nisin resistance in listeria monocytogenes. Appl Environ Microbiol. 76(19):6541–6546.
  • Begley M, Hill C, Ross RP. 2006. Tolerance of Listeria monocytogenes to cell envelope-acting antimicrobial agents is dependent on SigB. Appl Environ Microbiol. 72(3):2231–2234.
  • Bergholz TM, Tang S, Wiedmann M, Boor KJ. 2013. Nisin resistance of Listeria monocytogenes is increased by exposure to salt stress and is mediated via LiaR. Appl Environ Microbiol. 79(18):5682–5688.
  • Blake KL, Randall CP, O’Neill AJ. 2011. In vitro studies indicate a high resistance potential for the lantibiotic nisin in Staphylococcus aureus and define a genetic basis for nisin resistance. Antimicrob Agents Chemother. 55(5):2362–2368.
  • Bonnet M, Rafi MM, Chikindas ML, Montville TJ. 2006. Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes. Appl Environ Microbiol. 72(4):2556–2563.
  • Breukink E, Wiedemann I, van Kraaij C, Kuipers OP, Sahl HG, de Kruijff B. 1999. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science. 286(5448):2361–2364.
  • Chi H, Holo H. 2018. Synergistic antimicrobial activity between the broad spectrum Bacteriocin Garvicin KS and nisin, farnesol and polymyxin b against gram-positive and gram-negative bacteria. Curr Microbiol. 75(3):272–277.
  • Clemens R, Zaschke-Kriesche J, Khosa S, Smits SHJ. 2017. Insight into two ABC transporter families involved in lantibiotic resistance. Front Mol Biosci. 4:91.
  • Cleveland J, Montville TJ, Nes IF, Chikindas ML. 2001. Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol. 71(1):1–20.
  • Collins B, Guinane CM, Cotter PD, Hill C, Ross RP. 2012. Assessing the contributions of the lias histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. Appl Environ Microbiol. 78(8):2923–2929.
  • Cotter PD, Ross RP, Hill C. 2013. Bacteriocins–a viable alternative to antibiotics? Nat Rev Microbiol. 11(2):95–105.
  • Crandall AD, Montville TJ. 1998. Nisin Resistance in Listeria monocytogenes ATCC 700302 Is a Complex Phenotype. Appl Environ Microbiol. 64(1):231–237.
  • de Abreu LCL, Todaro V, Sathler PC, da Silva LCRP, do Carmo FA, Costa CM, Toma HK, Castro HC, Rodrigues CR, de Sousa VP, et al. 2016. Development and characterization of nisin nanoparticles as potential alternative for the recurrent vaginal candidiasis treatment. AAPS PharmSciTech. 17(6):1421–1427.
  • de Freire Bastos MDC, Varella Coelho ML, da Silva Santos OC. 2015. Resistance to bacteriocins produced by gram-positive bacteria. Microbiology. 161(Pt 4):683–700.
  • De Martinis ECP, Crandall AD, Mazzotta AS, Montville TJ. 1997. Influence of pH, salt, and temperature on nisin resistance in Listeria monocytogenes†. J Food Prot. 60(4):420–423.
  • de Vos WM,  Mulders JW, Siezen RJ, Hugenholtz J, Kuipers OP. 1993. Properties of nisin Z and distribution of its gene, nisZ, in Lactococcus lactis. Appl Environ Microbiol. 59(1):213–218.
  • Dobson A, Cotter PD, Paul Ross R, Hill C. 2012. Bacteriocin production: a probiotic trait? Appl Environ Microbiol. 78(1):1–6.
  • Dosler S, Gerceker AA. 2011. In vitro activities of nisin alone or in combination with vancomycin and ciprofloxacin against methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. Chemotherapy. 57(6):511–516.
  • Draper LA, Cotter PD, Hill C, Ross RP. 2015. Lantibiotic resistance. Microbiol Mol Biol Rev. 79(2):171–191.
  • El-Kazzaz SS, Abou E-KN. 2020. The effect of lantibiotic nisin on the inhibitory and bactericidal activities of antibiotics used against vancomycin resistant enterococci. J Glob Antimicrob Resist. 2020:263–269.
  • Fabretti F, Theilacker C, Baldassarri L, Kaczynski Z, Kropec A, Holst O, Huebner J. 2006. Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect Immun. 74(7):4164–4171.
  • Field D, Begley M, O’Connor PM, Daly KM, Hugenholtz F, Cotter PD, Hill C, Ross RP. 2012. Bioengineered nisin a derivatives with enhanced activity against both gram positive and gram negative pathogens. PLoS One. 7(10):e46884.
  • Field D, Blake T, Mathur H, O’Connor PM, Cotter PD, Paul Ross R, Hill C. 2019. Bioengineering nisin to overcome the nisin resistance protein. Mol Microbiol. 111(3):717–731.
  • Field D, Cotter PD, Hill C, Ross RP. 2015a. Bioengineering lantibiotics for therapeutic success. Front Microbiol. 6:1363.
  • Field D, Gaudin N, Lyons F, O’Connor PM, Cotter PD, Hill C, Ross R. 2015b. A bioengineered nisin derivative to control biofilms of Staphylococcus pseudintermedius. PLOS ONE. 10(3):e0119684.
  • Field D, O’Connor R, Cotter PD, Ross RP, Hill C. 2016. In vitro activities of nisin and nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Front Microbiol. 7:e00508.
  • Garde S, Avila M, Medina M, Nuñez M. 2004. Fast induction of nisin resistance in Streptococcus thermophilus INIA 463 during growth in milk. Int J Food Microbiol. 96(2):165–172.
  • Geitani R, Ayoub Moubareck C, Touqui L, Karam Sarkis D. 2019. Cationic antimicrobial peptides: alternatives and/or adjuvants to antibiotics active against methicillin-resistant Staphylococcus aureus and multidrug-resistant Pseudomonas aeruginosa. BMC Microbiol. 19(1):54.
  • Gomes D, Santos R, S. Soares R, Reis S, Carvalho S, Rego P, C. Peleteiro M, Tavares L, Oliveira M. 2020. Pexiganan in combination with nisin to control polymicrobial diabetic foot infections. Antibiotics. 9(3):128–115.
  • Gravesen A, Jydegaard Axelsen A-M, Mendes da Silva J, Hansen TB, Knøchel S. 2002. Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl Environ Microbiol. 68(2):756–764.
  • Hayes K, Field D, Hill C, O’Halloran F, Cotter L. 2019. A novel bioengineered derivative of nisin displays enhanced antimicrobial activity against clinical Streptococcus agalactiae isolates. J Glob Antimicrob Resist. 19:14–21.
  • Henderson LO, Flores BJE, Skeens J, Kent D, Murphy SI, Wiedmann M, Guariglia-Oropeza V. Nevertheless. 2020.  Nevertheless, she resisted–role of the environment on listeria monocytogenes sensitivity to nisin treatment in a. Laboratory Cheese Model. 11:1–15.
  • Hiron A, Falord M, Valle J, Débarbouillé M, Msadek T. 2011. Bacitracin and nisin resistance in Staphylococcus aureus: a novel pathway involving the BraS/BraR two-component system (SA2417/SA2418) and both the BraD/BraE and VraD/VraE ABC transporters. Mol Microbiol. 81(3):602–622.
  • Jiang X, Geng Y, Ren S, Yu T, Li Y, Liu G, Wang H, Meng H, Shi L. 2019. The  VirAB-VirSR-AnrAB multicomponent system is involved in. resistance of listeria monocytogenes EGD-e to Cephalosporins, Bacitracin, Nisin, Benzalkonium chloride, and ethidium bromide. Appl Environ Microbiol. 85(20):e01470-19.
  • Kang J, Wiedmann M, Boor KJ, Bergholz TM. 2015. VirR-mediated resistance of listeria monocytogenes against food antimicrobials and cross-protection induced by exposure to organic acid salts. Appl Environ Microbiol. 81(13):4553–4562.
  • Kaur S, Kaur S. 2015. Bacteriocins as potential anticancer agents. Front Pharmacol. 6:272–211. to
  • Kawada-Matsuo M, Watanabe A, Arii K, Oogai Y, Noguchi K, Miyawaki S, Hayashi T, Komatsuzawa H. 2020. Staphylococcus aureus virulence affected by an alternative nisin a resistance mechanism. Appl Environ Microbiol. 86(8):1–14.
  • Kawada-Matsuo M, Yoshida Y, Zendo T, Nagao J, Oogai Y, Nakamura Y, Sonomoto K, Nakamura N, Komatsuzawa H. 2013. Three distinct two-component systems are involved in resistance to the class I bacteriocins, nukacin isk-1 and nisin a, in Staphylococcus aureus. PLoS One. 8(7):e69455.
  • Khosa S, AlKhatib Z, Smits SHJ. 2013. NSR from Streptococcus agalactiae confers resistance against nisin and is encoded by a conserved nsr operon. Biol Chem. 394(11):1543–1549.
  • Kovács M, Halfmann A, Fedtke I, Heintz M, Peschel A, Vollmer W, Hakenbeck R, Brückner R. 2006. A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J Bacteriol. 188(16):5797–5805.
  • Kramer NE, Hasper HE, van den Bogaard PTC, Morath S, de Kruijff B, Hartung T, Smid EJ, Breukink E, Kok J, Kuipers OP, et al. 2008. Increased D-alanylation of lipoteichoic acid and a thickened septum are main determinants in the nisin resistance mechanism of Lactococcus lactis. Microbiology. 154(Pt 6):1755–1762.
  • Kramer NE, van Hijum SAFT, Knol J, Kok J, Kuipers OP. 2006. Transcriptome analysis reveals mechanisms by which Lactococcus lactis acquires nisin resistance. Antimicrob Agents Chemother. 50(5):1753–1761.
  • Kumariya R, Garsa AK, Rajput YS, Sood SK, Akhtar N, Patel S. 2019. Bacteriocins: classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microb Pathog. 128:171–177.
  • Lubelski J, Rink R, Khusainov R, Moll GN, Kuipers OP. 2008. Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci. 65(3):455–476.
  • Maisnier-Patin S, Richard J. 1996. Cell wall changes in nisin-resistant variants of Listeria innocua grown in the presence of high nisin concentrations. FEMS Microbiol Lett. 140(1):29–35.
  • Malekmohammadi S, Kodjovi KK, Sherwood J, Bergholz TM. 2017. Genetic and environmental factors influence Listeria monocytogenes nisin resistance. J Appl Microbiol. 123(1):262–270.
  • Mantovani HC, Russell JB. 2001. Nisin resistance of Streptococcus bovis. Appl Environ Microbiol. 67(2):808–813.
  • Martínez B, Obeso JM, Rodríguez A, García P. 2008. Nisin-bacteriophage crossresistance in Staphylococcus aureus. Int J Food Microbiol. 122(3):253–258.
  • Mataraci E, Dosler S. 2012. In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin-resistant Staphylococcus aureus biofilms. Antimicrob Agents Chemother. 56(12):6366–6371.
  • Mathur H, Field D, Rea MC, Cotter PD, Hill C, Ross RP. 2017. B acteriocin-antimicrobial synergy: a medical and food perspective. Front Microbiol. 8:1–18.
  • Mazzotta AS, Crandall AD, Montville TJ. 1997. Nisin resistance in clostridium botulinum spores and vegetative cells. Appl Environ Microbiol. 63(7):2654–2659.
  • McBride SM, Sonenshein AL. 2011. The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile. Microbiology. 157(Pt 5):1457–1465.
  • Molloy EM, Ross RP, Hill C. 2012. Bac’ to the future: bioengineering lantibiotics for designer purposes. Biochem Soc Trans. 40(6):1492–1497.
  • Narimisa N, Sadeghi Kalani B, Mohammadzadeh R, Masjedian JF. 2020. Combination of antibiotics—Nisin reduces the formation of Persister Cell in Listeria monocytogenes. Microb Drug Resist. 0:1–8.
  • Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem. 274(13):8405–8410.
  • Piper C, Hill C, Cotter PD, Ross RP. 2011. Bioengineering of a Nisin A-producing Lactococcus lactis to create isogenic strains producing the natural variants Nisin F, Q and Z. Microb Biotechnol. 4(3):375–382.
  • Porta N, Zaschke-Kriesche J, Frieg B, Gopalswamy M, Zivkovic A, Etzkorn M, Stark H, Smits SHJ, Gohlke H. 2019. Small-molecule inhibitors of nisin resistance protein NSR from the human pathogen Streptococcus agalactiae. Bioorg Med Chem. 27(20):115079.
  • Rana K, Sharma R, Preet S. 2019. Augmented therapeutic efficacy of 5-fluorouracil in conjunction with lantibiotic nisin against skin cancer. Biochem Biophys Res Commun. 520(3):551–559.
  • Randall CP, Gupta A, Utley-Drew B, Lee SY, Morrison-Williams G, O’Neill AJ. 2018. Acquired nisin resistance in staphylococcus aureus involves constitutive activation of an intrinsic peptide antibiotic detoxification module. mSphere. 3(6):e00633.
  • Reiners J, Lagedroste M, Ehlen K, Leusch S, Zaschke-Kriesche J, Smits SHJ. 2017. The  N-terminal region of nisin is important for the BceAB-type ABC transporter NsrFP from streptococcus agalactiae COH1. Front Microbiol. 8:e01643.
  • Rishi P, Bhagat NR, Thakur R, Pathania P. 2018. Tackling salmonella persister cells by antibiotic-nisin combination via mannitol. Indian J Microbiol. 58(2):239–243.
  • Rouse S, Field D, Daly KM, O’Connor PM, Cotter PD, Hill C, Ross RP. 2012. Bioengineered nisin derivatives with enhanced activity in complex matrices. Microb Biotechnol. 5(4):501–508.
  • Santos R, Ruza D, Cunha E, Tavares L, Oliveira M. 2019. Diabetic foot infections: application of a nisin-biogel to complement the activity of conventional antibiotics and antiseptics against Staphylococcus aureus biofilms. PLoS One. 14(7):e0220000.
  • Smith MK, Draper LA, Hazelhoff PJ, Cotter PD, Ross RP, Hill C. 2016. A  bioengineered nisin derivative, M21A, in combination with food grade additives eradicates biofilms of Listeria monocytogenes. Front Microbiol. 7:1–11.
  • Snyder AB, Worobo RW. 2014. Chemical and genetic characterization of bacteriocins: antimicrobial peptides for food safety. J Sci Food Agric. 94(1):28–44.
  • Suárez JM, Edwards AN, McBride SM. 2013. The Clostridium difficile cpr locus is regulated by a noncontiguous two-component system in response to type A and B lantibiotics. J Bacteriol. 195(11):2621–2631.
  • Szendy M, Kalkhof S, Bittrich S, Kaiser F, Leberecht C, Labudde D, Noll M. 2019. Structural change in GadD2 of Listeria monocytogenes field isolates supports nisin resistance. Int J Food Microbiol. 305:108240.
  • Tong Z, Zhang Y, Ling J, Ma J, Huang L, Zhang L. 2014. An in vitro study on the effects of nisin on the antibacterial activities of 18 antibiotics against Enterococcus faecalis. PLoS One. 9(2):e89209.
  • Verheul A, Russell NJ, Van’T Hof R, Rombouts FM, Abee T. 1997. Modifications of membrane phospholipid composition in nisin-resistant Listeria monocytogenes Scott A. Appl Environ Microbiol. 63(9):3451–3457.
  • Walker GV, Heng NCK, Carne A, Tagg JR, Wescombe PA. 2016. Salivaricin E and abundant dextranase activity may contribute to the anti-cariogenic potential of the probiotic candidate Streptococcus salivarius JH. Microbiology. 162(3):476–486.
  • Xuanyuan Z, Wu Z, Li R, Jiang D, Su J, Xu H, Bai Y, Zhang X, Saris PEJ, Qiao M, et al. 2010. Loss of IrpT function in Lactococcus lactis subsp. lactis N8 results in increased nisin resistance. Curr Microbiol. 61(4):329–334.
  • Yoshida Y, Matsuo M, Oogai Y, Kato F, Nakamura N, Sugai M, Komatsuzawa H. 2011. Bacitracin sensing and resistance in Staphylococcus aureus. FEMS Microbiol Lett. 320(1):33–39.
  • Zaschke-Kriesche J, Reiners J, Lagedroste M, Smits SHJ. 2019. Influence of nisin hinge-region variants on lantibiotic immunity and resistance proteins. Bioorg Med Chem. 27(17):3947–3953.
  • Zhao X, Zhen Z, Wang X, Guo N. 2017. Synergy of a combination of nisin and citric acid against Staphylococcus aureus and Listeria monocytogenes. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 34(12):2058–2068.
  • Zhu D, Li R, Liu F, Xu H, Li B, Yuan Y, Saris PE, Qiao M. 2016. Mu insertion in feuD triggers the increase in nisin immunity in Lactococcus lactis subsp. lactis N8. J Appl Microbiol. 120(2):402–412.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.