Abstract
The production of natural antimicrobial peptides (AMPs) is an innate immunity trait of all life forms including eukaryotes and prokaryotes. While these AMPs are usually called as defensins in eukaryotes, they are known as bacteriocins in prokaryotes. Bacteriocins are more diverse AMPs considering their varied composition and posttranslational modifications. Accordingly, this review is focused on cysteine-rich AMPs resembling eukaryotic defensins such as laterosporulin from Brevibacillus spp. and associated peptides secreted by the members of related genera. In fact, structural studies of laterosporulin showed the pattern typically observed in human defensins and therefore, should be considered as bacterial defensin. Although the biosynthesis mechanism of bacterial defensins displayed high similarities, variations in amino acid composition and structure provided the molecular basis for a better understanding of their properties. They are reported to inhibit Gram-positive, Gram-negative, non-multiplying and human pathogenic bacteria. The extreme stability is due to the presence of intra-molecular disulfide bonds in prokaryotic defensins and reveals their potential clinical and food preservation applications. Notably, they are also reported to have potential anticancer properties. Therefore, this review is focused on multitude of diverse applications of bacterial defensins, exploring the possible correlations between their structural, functional and possible biotechnological applications.
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Ahern M, Verschueren S, van Sinderen D (2003) Isolation and characterization of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol Lett 220:127–131
Altena K, Guder A, Cramer C, Bierbaum G (2000) Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl Environ Microbiol 66:2565–2571
Appleyard AN, Choi S, Read DM et al (2009) Dissecting structural and functional diversity of the lantibiotic mersacidin. Chem Biol 16:490–498
Arnison PG, Bibb MJ, Bierbaum G et al (2013) Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30:108–160
Baindara P, Chaudhry V, Mittal G, Liao LM, Matos CO, Khatri N, Franco OL, Patil PB, Korpole S (2016a) Characterization of the antimicrobial peptide penisin, a class Ia novel lantibiotic from Paenibacillus sp. strain A3. Antimicrob Agents Chemother 60:580–591
Baindara P, Singh N, Ranjan M, Nallabelli N, Chaudhry V et al (2016b) Laterosporulin10: a novel defensin like class IId bacteriocin from Brevibacillus sp. strain SKDU10 with inhibitory activity against microbial pathogens. Microbiology 162:1286–1299
Baindara P, Gautam A, Raghava GPS, Korpole S (2017). Anticancer properties of a defensin like class IId bacteriocin Laterosporulin10. Sci Rep 7:46541
Bastos, MCF, Ceotto H (2011) Bacterial antimicrobial peptides and food preservation. In: Ray M, Chikindas M (eds) Natural antimicrobials in food safety and quality. CAB International, Wallingford, pp 62–76
Bernbom N, Licht TR, Brogren CH, Jelle B, Johansen AH, Badiola I et al (2006) Effects of Lactococcus lactis on composition of intestinal microbiota: role of nisin. Appl Environ Microbiol 72:239–244
Brotz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG (1998) The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 42:154–160
Bruhn H (2005) A short guided tour through functional and structural features of saposin-like proteins. Biochem J 389:249–257
Chatterjee S, Chatterjee S, Lad SJ, Phansalkar MS, Rupp RH, Ganguli BN et al (1992) Mersacidin, a new antibiotic from Bacillus. Fermentation, isolation, purification and chemical characterization. J Antibiot (Tokyo) 45:832–838
Chatterjee C, Paul M, Xie L, van der Donk WA (2005) Biosynthesis and mode of action of lantibiotics. Chem Rev 105:633–684
Chehimi S, Pons AM, Sablé S, Hajlaoui MR, Limam F (2010) Mode of action of thuricin S, a new class IId bacteriocin from Bacillus thuringiensis. Can J Microbiol 56:162–167
Chen XH, Koumoutsi A, Scholz R et al (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014
Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20
Cotter PD, Ross RP, Hill C (2013) Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11:95–105
Daniels R, Mellroth P, Bernsel A, Neiers F, Normark S, von Heijne G, Henriques-Normark B (2010) Disulfide bond formation and cysteine exclusion in gram-positive bacteria. J Biol Chem 285:3300–3309
Dimarcq JL, Bulet P, Hetru C, Hoffmann J (1998) Cysteine-rich antimicrobial peptides in invertebrates. Biolpolymers 47:465–477
Duc LH, Honz HA, Barbosa, Henriques AO, Cutting SM (2004) Characterization of bacillus probiotics available for human use. Appl Environ Microbiol 70:2161–2171
Eijsink VGH, Skeie M, Middelhoven PH, BrurbergMB, Nes IF (1998) Comparative Studies Of Class IIa bacteriocins of lactic acid bacteria. Appl Environ Microbiol 64:3275–3281
Fimland G, Johnsen L, Axelsson L, Brurberg MB, Nes IF, Eijsink VGH, Nissen-Meyer J (2000) C-terminal disulfide bridge in pediocin-like bacteriocins renders bacteriocin activity less temperature dependent and is a major determinant of the antimicrobial spectrum. J Bacteriol 182:2643–2648
Flühe L et al (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 8:350–357
Fuller R (1989) Probiotics in man and animals. Experientia 35:406–407
Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3:710–720
Gao B, Rodriguez MC, Lanz-Mendoza H, Zhu S (2009) AdDLP, a bacterial defensin-like peptide, exhibits anti-Plasmodium activity. Biochem Biophys Res Commun 387:393–398
Garg N, Tang W, Goto Y, Nair SK, van der Donk WA (2012) Lantibiotics from Geobacillus thermodenitrificans. Proc Natl Acad Sci USA 109:5241–5246
Giuliani A, Pirri G, Rinaldi AC (2010) Antimicrobial peptides: the LPS connection. Methods Mol Biol 618:137–154
Gong W, Wang J, Chen Z et al (2011) Solution structure of LCI, a novel antimicrobial peptide from Bacillus subtilis. BioChemistry 50:3621–3627
Gross E, Morell JL (1971) The structure of nisin. J Am Chem Soc 93:4634–4635
Gross E, Kiltz HH, Nebelin E (1973) Subtilin, VI: the structure of subtilin. Hoppe-Seyler’s Z Physiol Chem 354:810–812
Gunasekera S, Daly NL, Anderson MA, Craik Dj (2006) Chemical synthesis and biosynthesis of the cyclotide family of circular proteins. IUBMB Life 58:515–524
Hatahet F, Boyd D, Beckwith J (2014) Disulfide bond formation in prokaryotes: history, diversity and design. Biochim Biophys Acta 1844:1402–1414
Hong HA, Huang J-M, Khaneja R, Hiep LV, Urdaci MC, Cutting SM (2008) The safety of Bacillus subtilis and Bacillus indicus as food probiotics. J Appl Microbiol 105:510–520
Inaba K (2009) Disulfide bond formation system in Escherichia coli. J Biochem 146:591–597
Jansen EF, Hirschmann DJ (1944) Subtilin, an antibacterial product of Bacillus subtilis: culturing conditions and properties. Arch Biochem 4:297–304.
Kagan BL, Selsted ME, Ganz T, Lehrer RI (1990) Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc Natl Acad Sci 87:210–214.
Karlyshev AV, Melnikov VG, Chikindas ML (2014) Draft genome sequence of Bacillus subtilis strain KATMIRA1933. Genome Announc 2:e00619–14.
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 43:3385–3395
Kellner R et al (1988) Gallidermin: a new lanthionine-containing polypeptide antibiotic. Eur J Biochem 177:53–59
Kruszewska D, Sahl HG, Bierbaum G, Pag U, Hynes SO, Ljungh A (2004) Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J Antimicrob Chemother 54:648–653
Lawton EM, Cotter PD, Hill C, Ross RP (2007) Identification of a novel two-peptide lantibiotic, Haloduracin, produced by the alkaliphile Bacillus halodurans C-125. FEMS Microbiol Lett 267:64–67
Lee H, Churey J, Worobo RW (2009) Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiol Lett 299:205–213
Lohans CT, Vederas JC (2014) Structural characterization of thioether-bridged bacteriocins. J Antibiotics 67:23–30
Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot 62:1677–1686
Nagy K, Mikuláss KR, Végh AG, Kereszt A, Kondorosi E, Váró G, Szegletes Z (2015) Interaction of cysteine-rich cationic antimicrobial peptides with intact bacteria and model membranes. Gen Physiol Biophys 34:135–144
Navarre WW, Schneewind O (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 61(3):174–229
Nguyen LT, Haney EF, Vogel HJ (2011) The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol 29:464–472
Noll S, Sinko PJ, Chikindas ML (2011) Elucidation of the molecular mechanisms of action of the natural antimicrobial peptide subtilosin against the bacterial vaginosis-associated pathogen Gardnerella vaginalis.. Probiotics Antimicrob Proteins 3:41–47
Oman TJ, Boettcher JM, Wang H, Okalibe XN, van der Donk WA (2011) Sublancin is not a lantibiotic but an S-linked glycopeptide. Nat Chem Biol 7:78–80
Paiva AD, Breukink E, Mantovani HC (2011) Role of lipid II and membrane thickness in the mechanism of action of the lantibiotic bovicin HC5. Antimicrob Agents Chemother 55:5284–5293
Parison J, Carey S, Breukink E, Chan WC, Narbad A, Bonev B (2008) Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrob Agents Chemother 52:612–618
Patil NA, Tailhades J, Hughes RA, Separovic F, John DW, Hossain MA (2015) Cellular disulfide bond formation in bioactive peptides and proteins. Int J Mol Sci 16:1791–1805
Prasch T, Naumann T, Markert RL, Sattler M, Schubert W, Schaal S, Bauch M, Kogler H, Griesinger C (1997) Constitution and solution conformation of the antibiotic mersacidin determined by NMR and molecular dynamics. Eur J Biochem 244:501–512
Rea MC, Sit CS, Clayton E, O’Connor PM, Whittal RM, Zheng J, Vederas JC, Ross RP, Hill C (2010) Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci 107: 9352–9357.
Ross AC, John C Vederas (2011) Fundamental functionality: recent developments in understanding the structure–activity relationships of lantibiotic peptides. J Antibiotics 64:27–34
Schneider TR, Karcher J, Pohl E, Lubini P, Sheldrick GM (2000) Ab initio structure determination of the lantibiotic mersacidin. Acta Cryst D Biol Crystallogr 56:705–713.
Silverstein KAT, Moskal WA, Wu HC et al (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51:262–280
Singh PK, Chittpurna, Ashish, Sharma V, Patil PB, Korpole S (2012) Identification, purification and characterization of laterosporulin, a novel bacteriocin produced by Brevibacillus sp. strain GI-9. PLoS ONE 7:e31498
Singh PK, Solanki V, Sharma S, Thakur KG, Krishanan B, Korpole S (2015) The intramolecular disulfide-stapled structure of laterosporulin, a class IId bacteriocin, conceals a human defensin-like structural module. FEBS J 282:203–214
Sirtori LR, Cladera-Olivera F, Lorenzini DM, Tsai SM, Brandelli A (2006) Purification and partial characterization of an antimicrobial peptide produced by Bacillus sp. strain P45, a bacterium from the Amazon basin fish Piaractus mesopotamicus. J Gen Appl Microbiol 52:357–363
Sit CS, van Belkum MJ, McKay RT, Worobo RW, Vederas JC (2011) The 3D solution structure of thurincin H, a bacteriocin with four sulfur to α-Carbon crosslinks. Angew Chem Int Ed 50:8718–8721
Sutyak KE, Wirawan RE, Aroutcheva AA, Chikindas ML (2008) Isolation of the Bacillus subtilis antimicrobial peptide from the dairy product-derived Bacillus amyloliquefaciens. J Appl Microbiol 104:1067–1074
Takami H, Nakasone K, Takaki Y, Maeno G, Sasaki R, Masui N, Fuji F, Hirama C, Nakamura Y, Ogasawara N, Kuhara S, Horikoshi K (2000) Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis. Nucleic Acids Res 28:4317–4331
Teng Y, Zhao W, Qian C, Li Q, Zhu L, Wu X (2012) Gene cluster analysis for the biosynthesis of elgicins, novel lantibiotics produced by Paenibacillus elgii B69. BMC Microbiol 12:45
Wiedmann I et al (2001) Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J Biol Chem 276:1772–1779
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Baindara, P., Kapoor, A., Korpole, S. et al. Cysteine-rich low molecular weight antimicrobial peptides from Brevibacillus and related genera for biotechnological applications. World J Microbiol Biotechnol 33, 124 (2017). https://doi.org/10.1007/s11274-017-2291-9
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DOI: https://doi.org/10.1007/s11274-017-2291-9