Skip to main content

Advertisement

SpringerLink
Log in

Gassericin A: a circular bacteriocin produced by Lactic acid bacteria Lactobacillus gasseri

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

During the recent years extensive efforts have been made to find out bacteriocins from lactic acid bacteria (LAB) active against various food spoilage and pathogenic bacteria, and superior stabilities against heat treatments and pH variations. Bacteriocins isolated from LAB have been grouped into four classes. Circular bacteriocins which were earlier grouped among the four groups of bacteriocins, have recently been proposed to be classified into a different class, making it class V bacteriocins. Circular bacteriocins are special molecules, whose precursors must be post translationally modified to join the N to C termini with a head-to-tail peptide bond. Cyclization appears to make them less susceptible to proteolytic cleavage, high temperature and pH, and, therefore, provides enhanced stability as compared to linear bacteriocins. The advantages of circularization are also reflected by the fact that a significant number of macrocyclic natural products have found pharmaceutical applications. Circular bacteriocins were unknown two decades ago, and even to date, only a few circular bacteriocins from a diverse group of Gram positive organisms have been reported. The first example of a circular bacteriocin was enterocin AS-48, produced by Enterococcus faecalis AS-48. Gassereccin A, produced by Lactobacillus gasseri LA39, Reutericin 6 produced by Lactobacillus reuteri LA6 and Circularin A, produced by Clostridium beijerinickii ATCC 25,752, are further examples of this group of antimicrobial peptides. In the present scenario, Gassericin A can be an important tool in the food preservation owing to its properties of high pH and temperature tolerance and the fact that it is produced by LAB L. gasseri, whose many strains are proven probiotic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abriouel H, Valdivia E, Martinez-Bueno M, Maqueda M, Galvez A (2003) A simple method for semi-preparative scale production and recovery of enterocin AS-48 derived from Enterococcus faecalis subsp. liquefaciens A-48–32. J Microbiol Meth 55:599–605

    Article  CAS  Google Scholar 

  • Arakawa K, Kawai Y, Iioka H, Tanioka M, Nishimura J, Kitazawa J, Tsurumi K, Saito T (2009) Effects of gassericins A and T, bacteriocins produced by Lactobacillus gasseri, with glycine on custard cream preservation. J Dairy Sci 92:2365–2372

    Article  CAS  Google Scholar 

  • Arakawa K, Kawai Y, Ito Y, Nakamura K, Chujo T, Nishimura J, Kitazawa H, Saito T (2010) HPLC purification and re-evaluation of chemical identity of two circular bacteriocins, gassericin A and reutericin 6. Lett Appl Microbiol 50(4):406–411

    Article  CAS  Google Scholar 

  • Blond A, Péduzzi J, Goulard C, Chiuchiolo MJ, Barthélémy M, Prigent Y, Salomón RA, Farías RN, Blond A, Moreno F, Rebuffat S (1999) The cyclic structure of microcin J25, a 21-residue peptide antibiotic from Escherichia coli. Eur J Biochem 259:747–755

    Article  CAS  Google Scholar 

  • Blond A, Cheminant M, Cheminant M, Ségalas-Milazzo I, Péduzzi J, Barthélémy M, Goulard C, Salomón R, Moreno F, Farías R, Rebuffat S (2001) Solution structure of microcin J25, the single macrocyclic antimicrobial peptide from Escherichia coli. Eur J Biochem 268:2124–2133

    Article  CAS  Google Scholar 

  • Braun V, Pilsl H, Gross P (1994) Colicins: structures, modes of action, transfer through membranes, and evolution. Arch Microbiol 161:199–206

    Article  CAS  Google Scholar 

  • Calne RY, White DJG, Thiru S, Evans DB, McMaster P, Dunn DC (1978) Cyclosporin A in patients receiving renal allografts from cadaver donors. Lancet 2:1323–1327

    Article  CAS  Google Scholar 

  • Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229

    Article  CAS  Google Scholar 

  • Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788

    Article  CAS  Google Scholar 

  • Craik DJ, Daly NL, Saska I, Trabi M, Rosengren KJ (2003) Structures of naturally occurring circular proteins from Bacteria. J Bacteriol 185(14):4011–4021

    Article  CAS  Google Scholar 

  • Craik DJ, Cemazar M, Wang CK, Daly NL (2006) The cyclotide family of circular miniproteins: nature’s combinatorial peptide template. Biopolymers 84:250–266

    Article  CAS  Google Scholar 

  • Danders W, Marahiel MA, Krause M, Kosui N, Kato T, Izumiya N, Kleinkauf H (1982) Antibacterial action of gramicidin S and tyrocidines in relation to active transport, in vitro transcription, and spore outgrowth. Antimicrob Agents Chemother 22(5):785–790

    Article  CAS  Google Scholar 

  • Davidson PM, Hoover DG (1993) Antimicrobial components from lactic acid bacteria. In: Salminen S, Wright A (ed). Lactic acid bacteria 127–159

  • de Vugst L, Vandamme EJ (1994) Bacteriocins of lactic acid bacteria. Microbiol, Genet Appl. London : blackie Acad and professional. ISBND 75:140174–140179

    Google Scholar 

  • Drider D, Fimland G, Héhard Y, McMullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582

    Article  CAS  Google Scholar 

  • Eijsink VH, Axelsson L, Diep DB, Havarstein LS, Holo H, Nes IF (2002) Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek 81:639–654

    Article  CAS  Google Scholar 

  • Ennahar S, Aoude-Werner D, Sorokine O, Van Dorsselaer A, Bringel F, Hubert JC, Hasselmann C (1996) Production of pediocin AcH by Lactobacillus plantarum WHE 92 isolated from cheese. Appl Environ Microbiol 62:4381–4387

    CAS  Google Scholar 

  • Gálvez A, Maqueda M, Valdivia E, Quesada A, Montoya E (1986) Characterization and partial purification of a broad spectrum antibiotic AS-48 produced by Streptococcus faecalis. Can J Microbiol 32:765–771

    Article  Google Scholar 

  • Gaillard-Gendron S, Vignon D, Cottenceau G, Graber M, Zorn N, van Dorsselaer A, Pons AM (2000) Isolation, purification and partial amino acid sequence of a highly hydrophobic new microcin named microcin L produced by Escherichia coli. FEMS Microbiol Lett 193:95–98

    Article  CAS  Google Scholar 

  • Göransson U, Svangård E, Claeson P, Bohlin L (2004) Novel strategies for isolation and characterisation of cyclotides: the discovery of bioactive macrocyclic plant polypeptides in the Violaceae. Curr Protein Pept Sci 5(5):317–330

    Article  Google Scholar 

  • Gustafson KR, Sowder RC II, Henderson LE, Parsons IC, Kashman Y, Cardellina JH II, McMahon JB, Buckheit RW Jr, Pannell LK, Boyd MR (1994) Circulins A and B. Novel human immunodeficiency virus (HIV)-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J Am Chem Soc 116(20):9337–9338

    Article  CAS  Google Scholar 

  • Heng NCK, Tagg JR (2006) What’s in a name? Class distinction for bacteriocins Nat Rev Microbiol 4, doi:10.1038/nrmicro1273-c1

  • Ito Y, Kawai Y, Arakawa K, Honme Y, Sasaki T, Saito T (2001) Conjugative plasmid from Lactobacillus gasseri LA 39 that carried for production of and immunity to the circular bacteriocin gassericin A. Appl Environ Microbiol 75(19):6340–6351

    Article  Google Scholar 

  • Itoh T, Fujimoto Y, Kawai Y, Toba Y, Saito T (1995) Inhibition of food-borne pathogenic bacteria by bacteriocins from Lactobacillus gasseri. Lett Appl Microbiol 21:137–141

    Article  CAS  Google Scholar 

  • Jacob F, Lwoff A, Siminovitch A, Wollman E (1953) De′finition de quelques termes relatifs a` la lysoge′nie. Ann Inst Pasteur (Paris) 84:222–224

    CAS  Google Scholar 

  • Joerger RD, Hoover DG, Barefood SF, Harmon KM, Grinstead DA, Nettlescutte CG (2000) Bacteriocins. In: Lederberg (ed) Encyclopedia of Microbiology. San Diego, Academic Press, Inc. 1(2):383–97

  • Kalmokoff ML, Cyr TD, Hefford MA, Whitford MF, Teather RM (2003) Butyrivibriocin AR10, a new cyclic bacteriocin produced by the ruminal anaerobe Butyrivibrio fibrisolvens AR10: characterization of the gene and peptide. Can J Microbiol 49(12):763–773

    Article  CAS  Google Scholar 

  • Kawai Y, Saito T, Kitazawa H, Itoh T (1998a) Gasserisin A; an uncommon cyclic bacteriocin produced by Lactobacillus gasseri LA39 at N- and C-terminal ends. Biosci Biotechnol Biochem 62:2438–2440

    Article  CAS  Google Scholar 

  • Kawai Y, Saito T, Suzuki M, Itoh T (1998b) Sequence analysis by cloning of the structural gene of gassericin A, a hydrophobic bacteriocins produced by Lactobacillus gasseri LA39. Biosci Biotechnol Biochem 62:887–892

    Article  CAS  Google Scholar 

  • Kawai Y, Saitoh B, Takahashi O, Kitazawa H, Saito T, Nakajima H, Itoh T (2000) Primary amino acid and DNA sequence of gassericin T, a lactacin F family bacteriocin produced by Lactobacillus gasseri SBT2055. Biosci Biotechnol Biochem 64(10):2201–2208

    Article  CAS  Google Scholar 

  • Kawai Y, Ishii Y, Uemura J, Kitazawa H, Saito T, Itoh T (2001) Lactobacillus reuteri LA6 and Lactobacillus gasseri LA39 isolated from faeces of the same human infant produce identical cyclic bacteriocin. Food Microbiol 18:407–415

    Article  CAS  Google Scholar 

  • Kawai Y, Arakawa K, Itoh A, Saitoh B, Ishii Y, Nishimura J, Kitazawa H, Itoh T, Saito T (2003) Heterologous expression of gassericin A, a bacteriocin produced by Lactobacillus gasseri LA39. Anim Sci J 74:45–51

    Article  CAS  Google Scholar 

  • Kawai Y, Kemperman R, Kok J, Saito T (2004a) The circular bacteriocins gassericin A and circularin A. Curr Protein Pept Sci 5(5):393–398

    Article  CAS  Google Scholar 

  • Kawai Y, Ishii Y, Arakawa K, Uemura K, Saitoh B, Nishimura J, Kitazawa H, Yamazaki Y, Tateno Y, Itoh T, Saito T (2004b) Structural and functional differences in two cyclic bacteriocins with the same sequences produced by lactobacilli. Appl Environ Microbiol 70(5):2906–2911

    Article  CAS  Google Scholar 

  • KawaiY Saito T, Toba T, Samant SK, Itoh T (1994) Isolation and characterization of a highly hydrophobic new bacteriocin (Gassericin A) from Lactobacillus gasseri LA39. Biosci Biotech Biochem 58(7):1218–1221

    Article  Google Scholar 

  • Kawulka KE, Sprules T, Diaper CM, Whittal RM, McKay RT, Mercier P, Zuber P, Vederas JC (2004) Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry 43(12):3385–3395

    Article  CAS  Google Scholar 

  • Kemperman R, Kuipers A, Karsens H, Nauta A, Kuipers O, Kok J (2003) Identification and characterization of two novel clostridial bacteriocins, circularin A and closticin 574. Appl Environ Microbiol 69(3):1589–1597

    Article  CAS  Google Scholar 

  • Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–85

    CAS  Google Scholar 

  • Kohli RM, Walsh CT (2003) Enzymology of acyl chain macrocyclization in natural product biosynthesis. Chem Commun (Camb) 7:297–307

    Google Scholar 

  • Kolter R, Moreno F (1992) Genetics of ribosomally synthesized peptide antibiotics. Annu Rev Microbiol 46:141–163

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Leah AM, van Belkum MJ, Garneau-Tsodikova S, Whittal RM, Zheng J, McMullen LM, Vederas JC (2008) Isolation and characterization of Carnocyclin A, a novel circular bacteriocin produced by Carnobacterium maltaromaticum UAL307. Appl Environ Microbiol 74(15):4756–4763

    Google Scholar 

  • Leer RJ, vander Vossen JM, van Giezen M, van Noort JM, Pouwels PH (1995) Genetic analysis of acidocin B, a novel bacteriocin produced by Lactobacillus acidophilus. Microbiology 141:1629–1635

    Article  CAS  Google Scholar 

  • Leuders T, Birkemo GA, Nissen-Meyer J, Andersen Q, Nes IF (2005) Proline Conformation-Dependent Antimicrobial Activity of a Proline-Rich Histone H1 N-Terminal Peptide Fragment Isolated from the Skin Mucus of Atlantic Salmon. Antimicrob Agents Chemother 49(6):2399–2406

    Article  Google Scholar 

  • Luckett S, García RS, Barker JJ, Konarev AV, Shewry PR, Clarke AR, Brady RL (1999) High-resolution structure of a potent, cyclic proteinase inhibitor from sunflowerseeds. J Mol Biol 290(2):525–533

    Article  CAS  Google Scholar 

  • Maqueda M, Gálvez A, Sánchez-Barrena MJ, González C, Albert A, Rico M, Valdivia E E (2004) Peptide AS-48: prototype of a new class of cyclic bacteriocins. Curr Prot Pept Sci 5:399–416

    Article  CAS  Google Scholar 

  • Motlagh AM, Bhunia AK, Szostek F, Hansen TR, Johnson MC, Ray B (1992) Nucleotide and amino acid sequence of pap-gene (pediocin AcH production) in Pediococcus acidilactici H. Lett Appl Microbiol 15:45–48

    Article  CAS  Google Scholar 

  • Nakamura K, Arakawa K, Kawai Y, Yasuta N, Chujo T, Watanabe M, Iioka H, Tanioka M, Nishimura J, Kitazawa H, Tsurumi K, Saito T (2013) Food preservative potential of gassericin A-containing concentrate prepared from cheese whey culture supernatant of Lactobacillus gasseri LA39. Anim Sci J 84(2):144–149

    Article  CAS  Google Scholar 

  • Nes IF, Bao Diep D, Havarstein LS, Brurberg MB, Eijsink V, Holo H (1996) Biosynthesis of bacteriocins of lactic aci bacteria. Antonie Van Leeuwenhoek 70:113–128

    Article  CAS  Google Scholar 

  • Nes IF, Diep DB, Holo H (2007) Bacteriocin diversity in Streptococcus and Enterococcus. J Bacteriol 189:1189–1198

    Article  CAS  Google Scholar 

  • O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotech 28:23–31

    Google Scholar 

  • Pillardy J, Czaplewski C, Liwo A, Lee J, Ripoll DR, Kazmierkiewicz R, Oldziej S, Wedemeyer WJ, Gibson KD, Arnautova YA, Saunders J, Ye YJ, Scheraga HA (2001) Recent improvements in prediction of protein structure by global optimization of a potential energy function. Proc Natl Acad Sci USA 98:2329–2333

    Article  CAS  Google Scholar 

  • Pons AM, Lanneluc I, Cottenceau G, Sable S (2002) New developments in non-post translationally modified microcins. Biochimie 84:531–537

    Article  CAS  Google Scholar 

  • Riley MA, Gordon DM (1992) A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol 138:1345–1352

    Article  CAS  Google Scholar 

  • Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56:117–137

    Article  CAS  Google Scholar 

  • Rivas L, Andreu D (2003) Eukaryotic antibiotic peptides: a new alternative in clinics? Enferm Infecc Microbiol Clin 21(7):358–365

    Google Scholar 

  • Ross RP, Morgan S, Hill C (2002) Preservation and fermentation: past, present and future. Int J Food Microbiol 79:3–16

    Article  CAS  Google Scholar 

  • Salomo′n RA, Farías RN (1992) Microcin 25, a novel antimicrobial peptide produced by Escherichia coli. J Bacteriol 174:7428–7435

    Google Scholar 

  • Sánchez-Hidalgo M, Montalbán-López M, Martínez-Bueno M, Valdivia E, Maqueda M (2007) Natural ribosomally synthesized circular proteins. Communicating current research and educational topics and trends in applied microbiology. In: Méndez-Vilas A (ed)

  • Schillinger U, Kaya M, Lucke FK (1991) Behaviour of Listeria monocytogenes in meat and its control by a bacteriocin producing strain of Lactobacillus sake. J Appl Bacteriol 70:473–478

    Article  CAS  Google Scholar 

  • Selsted ME (2004) Theta-defensins: cyclic antimicrobial peptides produced by binary ligation of truncated alpha-defensins. Curr Protein Pept Sci 5(5):365–371

    Article  CAS  Google Scholar 

  • Smarda J, Smajs D (1998) Colicins–exocellular lethal proteins of Escherichia coli. Folia Microbiol (Praha) 43:563–582

    Article  CAS  Google Scholar 

  • Starzl TE, Klintmalm GB, Porter KA, Iwatsuki S, Schröter GP (1981) Liver transplantation with use of cyclosporin a and prednisone. N Engl J Med 305(5):266–269

    Article  CAS  Google Scholar 

  • Suzuki T, Hayashi K, Fujikawa K, Tsukamoto K (1963) Contribution to the elucidation of the structure of polymyxin B1. J Biochem 54:555–556

    CAS  Google Scholar 

  • Tang YQ, Yuan J, Osapay G, Osapay K, Tran D, Miller CJ, Ouellette AJ, Selsted ME (1999) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 286(5439):498–502

    Article  CAS  Google Scholar 

  • Toba T, Samant SK, Yoshioka E, Itoh T (1991) Reutericin 6, a new bacteriocin produced by Lactobacillus reuteri LA6. Lett Appl Microbiol 13:281–286

    Article  CAS  Google Scholar 

  • Trabi M, Craik DJ (2002) Circular proteins—no end in sight. Trends Biochem Sci 27:132–138

    Article  CAS  Google Scholar 

  • Tsutsumi M, Ohotaka F (1985) Antimicrobial action of glycine on Salmonella typhimurium in pickle. Jpn J Zootech Sci 56:571–576

    CAS  Google Scholar 

  • Wirawan RE, Swanson KM, Kleffmann T, Jack RW, Tagg JR (2007) Uberolysin: a novel cyclic bacteriocin produced by Streptococcus uberis. Microbiology 153(5):1619–1630

    Article  CAS  Google Scholar 

  • Witherup KM, Bogusky MJ, Anderson PS, Ramjit H, Ransom RW, Wood T, Sardana M (1994) Cyclopsychotride A, a Biologically Active, 31-Residue Cyclic Peptide Isolated from Psychotria longipes. J Nat Prod 57(12):1619–1625

    Article  CAS  Google Scholar 

  • Zheng G, Yan LZ, Vederas JC, Zuber P (1999) Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin. J Bacteriol 181:7346–7355

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dairy Microbiology Division, National Dairy Research Institute, Karnal, 132001, India

    Neha Pandey, R. K. Malik & Garima Singroha

  2. Animal Biotechnology Division, National Dairy Research Institute, Karnal, 132001, India

    J. K. Kaushik

Authors
  1. Neha Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. K. Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. K. Kaushik
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Garima Singroha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neha Pandey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pandey, N., Malik, R.K., Kaushik, J.K. et al. Gassericin A: a circular bacteriocin produced by Lactic acid bacteria Lactobacillus gasseri . World J Microbiol Biotechnol 29, 1977–1987 (2013). https://doi.org/10.1007/s11274-013-1368-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-013-1368-3

Keywords

Search

Navigation