Fig. 1.
Structure-based classification of Gram-positive bacteriocins.
Fig. 2.
Structural-based classification of Gram-negative bacteriocins.
Fig. 3.
Bacteriocin mechanism of action on a) Gram-positive and b) Gram-negative bacteria.
Table I
Bacteriocins with potential application as therapeutic and food preservatives.
| Bacteriocin | Producer bacteria | Target microorganism | Use | Reference |
|---|---|---|---|---|
| 1. Food preservation | ||||
| AMA-K, Leucocin K7 | L. plantarum AMA-K | Enterococcus spp., E. coli, K. pneumoniae, Listeria spp. | Amasi, fermented milk product | (Todorov 2008) |
| Aureocin A70 | S. aureus A70 | L. monocytogenes | Dairy product | (Carlin Fagundes et al. 2016) |
| Bacteriocin 32Y | L.curvatus | L. monocytogenes | Pork and beef | (Gálvez et al. 2007) |
| Bacteriocin GP1 | L. rhamnosus GP1 | Staphylococcus sp., Aeromonas sp., Lactobacillus sp., Pseudomonas sp., Vibrio sp. | Fish | (Sarika et al. 2019) |
| Bovicin HC5 + Nisin | Streptococcus bovis HC5 | L. monocytogenes, S. aureus | Fresh cheese | (Pimentel-Filho et al. 2014) |
| Divergicin M35 | Carnobacteriumdivergens M35 | L. monocytogenes | Smoked fish | (Benabbou et al. 2020) |
| Enterocin | E.faecium FAIR-E 198 | Listeria spp. | Feta cheese | (Sarantinopoulos et al. 2002) |
| Enterocin 416K1 | E.casseliflavus IM 416K1 | L. monocytogenes NCTC 10888 | Cottage cheese | (Iseppi et al. 2008) |
| Enterocin AS-48 | Enterococcus sp. | L. monocytogenes, B. cereus | Cheese, vegetable, purees, and soups | (Gálvez et al. 2007) |
| H1, H2, H3, H4 | Bacillus sp. | V. alginolyticus, Aeromonas hydrophilla, P. stutzeri | Antimicrobial used in fish | (Feliatra et al. 2018) |
| Lacticin 3147 | L.lactis | L. monocytogenes | Matured and cottage cheese | (Mills et al. 2017) |
| Lacticin NK24 | L. lactis | Leuconostoc mesenteroides KCCM 11324 | Seafood | (Lee and Paik 2001) |
| Leucocin K7 | L. mesenteroides K7 | L. monocytogenes | Dairy product | (Shi et al. 2016) |
| Mecedocin | S.macedonicus ACA-DC 198 | C. tyrobutyricum LMG 1285T | Kasseri cheese | (Anastasiou et al. 2009) |
| NE | L.gasseri K7 (Rifr), L. gasseri LF221(Rifr) | C. tyrobutyricum | Semi-mature cheese | (Bogovič Matijašić et al. 2007) |
| Nisin | Lactococcus spp., Streptococcus spp. | L. monocytogenes, Clostridium botulinum, S. mutans, L. innocua, S. aureus, S. pneumoniae, B. cereus | Dairy products, meat, seafood | (Juturu and Wu 2018) |
| Pediocin PA1 | P.acidilactici | L. monocytogenes | Dairy products, meat | (Liu et al. 2008) |
| Plant-made salmocins | Salmonella spp. | S. enterica | Red meat | (Schneider et al. 2018) |
| Plant-made colicins (GRN 676, GRN 593) | E.coli | E. coli, P. aeruginosa, Salmonella spp. | Meat, fruits, or vegetables | (Hahn-Löbmann et al. 2019) |
| Psicolin 126, carnocyclin A | C. maltoaromaticum | L. monocytogenes | Ready-to-eat meat products | (Liu et al. 2014) |
| Reuterin | L. reuteri | E.coli, S. aureus, Candida albicans | Food preservation | (Helal et al. 2016) |
| Sakacin P | L.sakei | L.monocytogenes | Beef and Salmon | (Teneva-Angelova et al. 2018) |
| Thuricin BtCspB | B. thuringiensis | B.cereus | Food preservation and disease associate to B. cereus | (Huang et al. 2016) |
| 2. Bacterial infections | ||||
| ABP118 | L.salivarius subsp. salivarius UCC118 | Bacteroides | Antimicrobial agent | (Riboulet-Bisson et al. 2012) |
| Colicins Js and Z | E.coli | Enteroinvasive, E. coli (EIEC) and Shigella | Gastrointestinal infections | Bosák et al. 2021 |
| Divercin V41 | C.divergens | L. monocytogenes | Antimicrobial agent | (Rihakova et al. 2010) |
| Duramycin | Streptomyces cinnamoneus | B. subtilis | Antimicrobial, anti-viral, immunomodulation, ion channel modulation, treatment of atherosclerosis and cystic fibrosis | (Huo et al. 2017) |
| Enterocin CRL35 | E.mundtii | L. monocytogenes | Gastrointestinal infections | (Salvucci et al. 2012) |
| Epidermin and mersacidin-like peptides | S.epidermidis | P. acnes | Acne, folliculitis. | (Gillor et al. 2008) |
| Gallidermin/epidermin | S.gallinarum | S. epidermidis, S. aureus | Skin infections or associated with implants and prostheses | (Bengtsson et al. 2018; Bonelli et al. 2006) |
| Gassericin E | L.gasseri EV1461 | Pathogens associated with vaginosis | Vaginal infections | (Maldonado-Barragán et al. 2016) |
| Haemocin type B | Haemophilus haemolyticus | H. influenza | Respiratory infections | (Latham et al. 2017) |
| Lactocin 160 | L.rhamnosus | G. vaginalis | Urogenital tract infections, bacterial vaginosis | (Turovskiy et al. 2009) |
| Laterosporulin10 | Brevibacillus sp. strain SKDU10 | S. aureus, Mycobacterium tuberculosis (Mtb H37Rv), M. smegmatis MC2 155 | Human microbial pathogens | (Baindara et al. 2016) |
| Mersacidin | B.amyloliquefaciens | Methicillin-resistant S. aureus (MRSA) | Skin infection | (Kruszewska et al. 2004) |
| Microcin J25 (lasso-peptide) | E.coli | S.enterica, E.coli, S.flexnerii | Gastrointestinal infections | (Dobson et al. 2012) |
| Nisin A, Nisin Z, Nisaplin | L.lactis | S.mutans, S.aureus, E.faecalis, S.mastitis, C.albicans | Gastrointestinal, respiratory, and skin infections, oral health | (Shin et al. 2016) |
| Oralpeace TM (encapsulated nisin) | L.lactis | S. mutans, P. gingivalis | Dental caries, gingivitis | (Perez et al. 2014) |
| Piscicolin 126 | Carnobacterium spp. | Listeria spp. | Antimicrobial agent | (Miller and McMullen 2014) |
| Plantaricin 423 | L.plantarum | Listeria spp. | Antimicrobial agent | (Guralp et al. 2013) |
| PLNC8 αβ | L.plantarum | Staphylococcus sp., Porphyromonas gingivalis | Antimicrobial agent | (Bengtsson et al. 2020) |
| R-pyocins | P.aeruginosa | P. aeruginosa | Antimicrobial agent | (Redero et al. 2018) |
| TOMM Streptolysin S (SLS) | S.pyogenes | Clostridium sp., Listeria sp. | Hemolytic and cytotoxic activity against macrophages and neutrophils | (Molloy et al. 2015) |
| 3. Anticancer drugs | ||||
| Cancer cell lines | ||||
| Azurin | P.aeruginosa | MCF-7, UISO-Mel-2, osteosarcoma (U2OS) | (Nguyen and Nguyen 2016) | |
| Bovicin HC5 | S.bovis HC5 | MCF-7, HepG2 | (Rodrigues et al. 2019) | |
| Colicin E3 | E.coli | P388, HeLa, HS913T | (Kohoutova et al. 2014 | |
| Duramycin | S.cinnamoneus | AsPC-1, Caco-2, Colo320, CT116, JJN3, Lovo, MCF-7, MDA-B-231, MIA PaCa-2 | (Rodrigues et al. 2019) | |
| Enterocin LNS18 | E.thailandicus | HepG2 | (Al-Madboly et al. 2020) | |
| Laterosporulin LS10 | Brevibacillus latero– | HeLa, MCF-7, H1299, HEK293T, HT1080 | (Baindara et al. 2016) | |
| sporus SKDU10 | ||||
| M2163, M2386 | L.casei ATCC 334 | SW480 | (Rodrigues et al. 2019) | |
| Microcin E492 | K.pneumoniae | HeLa, Burkitt lymphoma variant (RJ2.25) | (Kaur and Kaur 2015) | |
| Nisin A | L.lactis | Head and neck squamous cell carcinoma (HNSCC) | (Shin et al. 2016) | |
| Pediocin K2a2-3 | P.acidilactici K2a2-3 | HT2a, HeLa | (Villarante et al. 2011) | |
| Pediocin CP2 | P.acidilactici CP2 MTCC501 | HeLa, MCF-7, HepG2, murine myeloma (Sp2/0-Ag 14) | (Kumar et al. 2012) | |
| Pep27anal2 | S.pneumoniae | Jurkat, HL-60, AML-2, MCF-7, SNU-601 | (Rodrigues et al. 2019) | |
| Plantaricin A | L.plantarum C11 | GH4, Reh, Jurkat, PC12, N2A | (Sand et al. 2013) | |
| Plantaricin P1053 | L.plantarum PBS067 | E705 | (De Giani et al. 2019) | |
| Pyocin S2 | P.aeruginosa 42A | HepG2, Im9, murine tumor (mKS-A TU-7), human fetal foreskin fibroblast (HFFF) | (Abdi-Ali et al. 2004) | |
| Sungsanpin | Streptomyces spp. | A549 | (Um et al. 2013) | |
| Smegmatocin | M.smegmatis 14468 | HeLa, AS-II, HGC-27, mKS-A TU-7 | (Kaur and Kaur 2015) | |
Table II
Biocontrol potential of bacteriocin-producing microorganisms in agriculture.
| Bacteriocin | Producer bacterium | Phytopathogen | Reference |
|---|---|---|---|
| Amylocyclin | B. amyloliquefaciens | Ralstonia solanacearum and X. campestris | (Scholz et al. 2014) |
| Bacteriocin 32Y | P. aeruginosa RsB29 | Fusarium sp. | (Sindhu et al. 2016) |
| Carocin D | P. carotovorum subsp. carotovorum | P. carotovorum subsp. Carotovorum | (Grinter et al. 2012; Roh et al. 2010) |
| Enterocin UNAD 046 | E. faecalis | B. theobromae, A. niger, P. expansum, P. ultimum. | (David and Onifade, 2018) |
| Fluoricin BC8 | P. fluorescens BC8 | P. solanacearum | (Sindhu et al. 2016) |
| Gluconacin | G. diazotrophicus PAL5 | X. albilineans and X. vasicola pv. vasculorum. | (Oliveira et al. 2018) |
| LlpA | P. putida BW11M1 | P. syringae | (Parret et al. 2005) |
| Morricin 269, Kurstacin 287, Kenyacin 404, Entomocin 420, Tolworthcin 524 | B. thurigiensis | Trichoderma spp., A. nodulans, F. graminis, F. oxysporum, Rhizopus sp., Mucor rouxii | (De La Fuente-Salcido et al. 2008; Salazar-Marroquín et al. 2016) |
| NE | P. syringae pv. ciccaronei | P. syringae subsp. savastanoi | (Lavermicocca et al. 2002) |
| BLIS RC-2 | B. amyloliquefaciens RC-2 | R. necatrix, P. oryzae, A. tumefaciens, Xanthomonascampestris pv. campestris, C. dematium | (Abriouel et al. 2011) |
| NE | B. gladioli | Tatumella ptyseos | (Marín-Cevada et al. 2012) |
| BL8 | B. thuringiensis subsp. tochigiensis HD868 | A. niger, A. fumigatus, A. flavus, Cryphonectria parasitica, F. oxysporum, Penicillium digitatum. | (Subramanian and Smith 2015) |
| Plantazolicin | B. velezensis FZB42 (B. amyloliquefaciens subsp. plantarum) | B. anthracis and nematodes. | (Chowdhury et al. 2015) |
| Putidacin L1 | P. protegens, P. putida | P. syringae | (Rooney et al. 2020) |
| Rhizobiocin | Rhizobium spp. | P. savastanoi | (Kaur Maan and Garcha 2018) |
| SF4c tailocins | P. fluorescens SF4c | X. vesicatoria | (Príncipe et al. 2018) |
| Syringacin M | P. syringae pv. tomato DC3000 | P. syringae | (Li et al. 2020) |
Fig. 4.
Timeline of bacteriocin patents reported worldwide from January 1, 2000 to August 7, 2020. Countries with the highest number of reported patents per year are shown. The figure was generated with the Patent Inspiration search engine (https://www.patentinspiration.com).
CN – China, US – United States, KR – Korea, RU – Russian Federation, UA – Ukraine, CA – Canada, JP – Japan, AU – Australia, NZ – New Zealand, GE – Germany, FR – France, TW – Taiwan, AT – Austria, PL – Poland, ES – Spain, AR – Argentina, MX – Mexico, BR – Brazil, DK – Denmark, CZ – Czech Republic, HU – Hungary, ZA – South Africa, SE – Sweden, IL – Israel, GB – United Kingdom.