Bacteriocins and Their Applications in Food Preser

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Bacteriocins and Their Applications in Food Preservation

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Bacteriocins and Their Applications in Food


Preservation
a a a b a
Ramith Ramu , Prithvi S Shirahatti , Aishwarya T Devi , Ashwini Prasad , Kumuda J. ,
a c d a
Lochana M. S. , Zameer F. , Dhananjaya B. L. & Nagendra Prasad M. N.
a
Department of Biotechnology, Sri Jayachamarajendra College of Engineering, Mysore 570
006, India
b
Department of Microbiology, Faculty of Life Sciences, JSS University, Mysore, India
c
Mahajana Life Science Research Laboratory, Department of Biotechnology, Microbiology
and Biochemistry, Pooja Bhagavat Memorial Mahajana Post Graduate Centre, Metagalli,
Mysore - 570 016, Karnataka, India.
d
Click for updates Toxinology/Toxicology and Drug Discovery Unit, Center for Emerging Technologies, Jain
Global Campus, JainUniversity, Kanakapura Taluk, Ramanagara-562112, Karnataka, India.
Accepted author version posted online: 20 Jul 2015.

To cite this article: Ramith Ramu, Prithvi S Shirahatti, Aishwarya T Devi, Ashwini Prasad, Kumuda J., Lochana M. S., Zameer
F., Dhananjaya B. L. & Nagendra Prasad M. N. (2015): Bacteriocins and Their Applications in Food Preservation, Critical
Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2015.1020918

To link to this article: http://dx.doi.org/10.1080/10408398.2015.1020918

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Bacteriocins applications

Bacteriocins and their applications in food preservation

Ramith Ramu1, Prithvi S Shirahatti1, Aishwarya T Devi1, Ashwini Prasad2, Kumuda J1, Lochana

MS1, Zameer F3, Dhananjaya BL4, Nagendra Prasad MN1,*

1
Department of Biotechnology, Sri Jayachamarajendra College of Engineering, Mysore 570 006,

India
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2
Department of Microbiology, Faculty of Life Sciences, JSS University, Mysore, India
3
Mahajana Life Science Research Laboratory, Department of Biotechnology, Microbiology and

Biochemistry, Pooja Bhagavat Memorial Mahajana Post Graduate Centre, Metagalli, Mysore -

570 016, Karnataka, India.


4
Toxinology/Toxicology and Drug Discovery Unit, Center for Emerging Technologies, Jain

Global Campus, JainUniversity, Kanakapura Taluk, Ramanagara-562112, Karnataka, India.


*
Corresponding Authors Dr. M.N. Nagendra Prasad, Sri Jayachamarajendra College of

Engineering&JainUniversity, Karnataka, India, Phone: +91 9886480528

Fax: +91821 2548290, Email: [email protected], [email protected]

ABSTRACT

Bacteriocins are ribosomally-synthesized antimicrobial peptides or proteinaceous compounds

produced by bacterial strains. They are generally effective in inhibiting the growth of similar or

closely related bacterial strains. A high diversity of various bacteriocins is produced by many

lactic acid bacteria (LAB) and is found in numerous fermented and non-fermented foods. Several

bacteriocins from LAB extend potential applications in food preservation, thus help foods to be

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naturally preserved and richer in organoleptic and nutritional properties. Though chemical

preservatives for the preservation of food are successful to some extent, their quality is not as

satisfying as fresh food. Hence, an alternative is required and bacteriocins serve the purpose.

Nisin is currently the only bacteriocin widely used as a food preservative. Numerous bacteriocins

have been characterized chemically, biochemically, genetically and also at the molecular level to

understand their basic mode of action. This article gives an overview of classification of

bacteriocins, isolation & characterization, and mode of action. Besides, article highlights the
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optimized parameters for growth of bacteria in the production of bacteriocins and various

bioassays for their determination. Special emphasis has been provided on explaining the

beneficial aspects of nisin.

Keywords

Bacteriocin; Nisin; Lactic acid bacteria (LAB); Lantibiotics; Bio-preservation.

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INTRODUCTION

All organisms produce organic compounds that are not directly involved in their normal growth,

development, or reproduction and are termed as secondary metabolites (Fraenkel 1959). They are

generally low-molecular-mass products that include antibiotics, pigments, toxins, effectors of

ecological competition and symbiosis, pheromones, enzyme inhibitors, immunomodulating

agents, receptor antagonists, agonists and so on (Demain 1992).

Likewise, bacteriocins are produced by bacterial ribosomes as secondary metabolites. Antibiotics


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are also produced by some bacteria and, hence, along with bacteriocins they should be

considered as different antimicrobial compounds (Davidson and Hoover 1993). A large group of

functionally diverse antimicrobial compounds found in all major lineages of bacteria and archaea

constitute the bacteriocin family (Riley and Wertz 2002). While some possess a narrow

bactericidal spectrum, many others exhibit a broader activity against some of the distantly related

species (Klaenhammer 1993; Adam and Moss 1995). Over-all, specific immunity proteins

responsible for this are encoded in the bacteriocin operon (McAuliffe et al., 2000; Cintas et al.,

2001). Majority of them exert their action through the formation of transitory poration complexes

or ionic channels which cause reduction or dissipation of the proton motive force leading to the

formation of pores in the cytoplasmic membrane of sensitive cells (Cintas et al., 1998; Herranz et

al., 1999). They also employ other killing mechanisms like cell wall interference and nuclease

activity (Braun et al., 1994; Smarda and Smajs, 1998).

Considering the antibacterial property of bacteriocins, some researchers speculate on considering

them and antibiotics under the same class but since bacteriocins are bactericidal peptides, while

antibiotics are produced by multi-enzyme complexes, there remains a demarcation between the

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two bactericidal agents. Most bacteriocins kill a narrow spectrum of bacteria, as compared to the

traditional antibiotics (Tu et al., 2002). Some bacteriocins produced by lactic acid bacteria (LAB)

are called lantibiotics and they have potential applications in the food industry. Currently

existing synthetic food preservatives raise some concern with regard to the quality of food and

are associated to several health hazards. In this view, bacteriocins prove safer alternatives and

constitute a revolutionary breakthrough in the food preservation. Hence, bacteriocins are

efficiently produced from isolated and purified bacteria. Bacteriocins are categorized and
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discussed in detail as shown in Figure 1. They are characterized based on different principles

viz., chemical, biochemical, molecular, and genetic characteristics (Mian et al., 2012).

Classification

Bacteriocins are an important part of the defence system of bacteria and are produced by both

Gram-positive and Gram-negative species. Bacteriocins from Gram-positive bacteria are broadly

classified into 4 groups. The presence of sulfide (such as lanthionine) and disulfide bonds has

been taken as the major distinguishing factor since it also entails their spectrum of activity (Jack

et al., 1995). However, the molecular mass, thermo-stability, enzymatic sensitivity, presence of

post translational modified amino acids, and mode of action also play a role, especially in the

classification into sub-groups (Klaenhammer 1993). The groups may be stated as:

i. Class I-Bacteriocins

ii. Class II-Bacteriocins

iii. Class III-Bacteriocins

iv. Class IV-Bacteriocins

Class I-Bacteriocins

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Class I bacteriocins are post-translationally modified peptides containing unusual amino acids,

such as lanthionine or methyl lanthionine residues and are called lantibiotics (Nissen and Nes

1997). They are produced by LAB to attack other Gram-positive bacteria and are smaller than 5

kDa (Boman 1995). Nisin, subtilin, cytolysin and variacin 8 are a few examples (Gross and

Morell, 1971; Gross and Kitz, 1973; Gilmore et al., 1994).

Class II-Bacteriocins

Class II bacteriocins are heat-stable, unmodified peptides, and do not contain the unusual amino
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acid and hence they are called non-lantibiotics. They are small peptide molecules which are

smaller than 10 kDa and produced by LAB (Bierbaum and Sahl 2009). Class II bacteriocins are

further divided into 3 sub-classes, namely IIa, IIb, and IIc (Ennahar et al., 2000). Pediocin-like

bacteriocins, two-component bacteriocins, and thiol-activated bacteriocins are grouped under the

IIa, IIb, and IIc sub-classes, respectively. Some of the examples are pediocin PA-1, lactacin F,

enterocin AS-48 (Nissen et al., 2009). The major difference between Class I and Class II

bacteriocins is that Class I bacteriocins undergo post-translational modifications and thus give

rise to the unusual amino acid lanthionine, whereas Class II bacteriocins do not undergo any such

modifications.

Class III-Bacteriocins

Class III bacteriocins are heat-labile and larger (>10 kDa) protein molecules (Savadogo et al.,

2006). They are sub-classified into 2 sub-classes: Class IIIa or bacteriolysins and Class IIIb or

non-lytic bacteriocins. Lysostaphin, a 27-kDa peptide that is produced from Gram-positive

Staphylococcus species, is the best-studied bacteriolysin (Bastos et al., 2010).

Class IV-Bacteriocins

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Class IV bacteriocins are complex proteins that contain lipid or carbohydrate moieties (Oman et

al., 2011; Upreti and Hinsdill 1975). This group was added after the observation that bacteriocin

activities obtained in a cell free supernatant were abolished not only by protease treatments, but

also by glycolytic and lipolytic enzymes (Jimenez et al., 1993; Tagg et al., 1976; Nes et al.,

2000; Garneau et al., 2002). Plantaricin S and leuconocin S are major examples of Class IV

bacteriocins (Vijay and John 2002).

Further, according to the scheme of Cotter et al., (2005), bacteriocins are classified into 2 major
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groups, namely lantibiotics and unmodified peptides. The authors eliminated classes IIa, III, and

IV and restructured class II. Thus, the class of unmodified peptides includes pediocin-like

peptides, two-component peptides, cyclic peptides, and miscellaneous bacteriocins. Considering

both the schemes, a universal bacteriocin classification was established, as shown in Figure 1.

While Gram-positive bacteria are classified as detailed in the above section, Gram-negative

bacteriocins are categorized based on their size. These bacteriocins are produced from Gram-

negative bacteria (arise mainly from enterobacteriaceae) and are heat-stable molecules. They are

mainly classified into 2 classes based on their molecular mass:

i. High-molecular-mass peptides (30 kDa-80 kDa) named colicins

ii. Low-molecular-mass peptides (1 kDa-10 kDa) called microcins (Drider and Ribuffat

2011).

Since the beginning of 21 stcentury, bacteriocins have been classified in several other ways, based

on their specific adsorption and immunity patterns (Frederic 1957). Reeves named and grouped

bacteriocins into 16 classes based on the species of the producing strain, like the colicins which

are bacteriocins produced by E. coli, pyocins by Pseudomonas aeruginosa, arizonacins by

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Paracolobactrum arizonae, cloacins by Enterobacter cloacae, pneumocins by Klebsiella

pneumoniae, pesticin by Yersinia pestis, monocin by Listeria monocytogenes, cerecin by

Bacillus cereus, and staphylococcin by Staphylococcus aureus (Reeves 1965).

Mode of action of bacteriocins

Bacteriocins affect different essential functions of the living cell viz., transcription, translation,

replication, and cell wall biosynthesis due to great variety of chemical structures, but most of

them destroy the energy potential of sensitive cells by forming membrane channels or pores
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(Juan et al., 2000; Ganzle 2004). The best-described mechanism is pore formation. The presence

of molecular receptors in the membrane of the target cell is suggested by the relatively small

action spectrum of some bacteriocins, although this has not been demonstrated (Van and Stiles

2000).

A model demonstrated using nisin suggests that, using C-terminal, nisin primarily binds to

phosphatidylglycerol, a universal receptor, present on the cytoplasmic membrane of target

bacteria (Breukink and Kruijff 2006). Hence a complete loss of activity could be observed if the

C-terminal is removed (Giffard et al., 1997). Binding of nisin is followed by insertion and

penetration of a part of peptide into the cytoplasmic membrane. Fluorescence studies indicate a

parallel orientation of nisin molecule with respect to the membrane surface having N-terminal

inserted slightly deeper than C-terminal (Breukink et al., 1998). This initiates the process of

membrane insertion and pore formation, leading to rapid cell death (Cotter et al., 2005; Breukink

and Kruijff 2006).

In general, the helical amphiphilic structure of class II peptides allows them to get inserted into

the membrane of the target cell, leading to depolarization and death (Cotter et al., 2005; Drider et

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al., 2006). At the hydrophilic N-terminus of the peptides, the initial interaction takes place with

the heads of the anionic membrane phospholipids. The C-terminus of the peptide is thought to be

involved in hydrophobic interactions with the membrane as it is more hydrophobic than the N-

terminal (Alonso et al., 2000).Class II bacteriocins allow the insertion of the peptide into the

membrane of sensitive microorganism, using its amphiphilic structure, and causes depolarization

and death (Brashears et al., 1998).

On the contrary, the large bacteriolytic proteins, such as lysostaphin (Class III bacteriocins), lead
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to death and cell lysis by directly acting on the cell wall of Gram-positive target cells (Cotter et

al., 2005). Under the influence of various mechanisms, bacteriocins cause microbial cell killing

either in an isolated or most consorted manner (Paker et al., 1989; Daw and Falkiner 1996).

Unbalanced cytoplasmic membrane function, inhibition of nucleic acid synthesis, interference

with protein synthesis and changing the cell translator mechanism lead to bacteriocins killing a

microbial cell (Nes and Tagg 1996). Due to the development of specific immunity mediated by a

protein, bacteriocin-producing cells are not affected by the action of their own bacteriocin

(Hancock and Chapple 1999). Bacteriocins have been noteworthy in detections and causing

fatality to competitor bacteria, with little or no damage to their producing cell (Tadashi and

Schnneewind 1998).

Microorganisms have competitive superiority when they dispute ecological niches in the

environment where they are developing their metabolic activities (Stockewell et al., 1993).

Based on this narrow action, bacteriocins play a role as intra-specific mediators or promoters of

interactions among microbial populations (Jennifer et al., 2001). When 2 or more

microorganisms are present in an environment and adversely interfere with growth and survival

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of other ones, antibiosis occurs. It is the antagonistic action exerted by bacteriocin-producing

bacteria on the other bacteria in the same environment (Schillinger 1990; Ray 1996).

Isolation of bacteriocinogenic strains from food systems

The majority of bacteriocin producers are natural food isolates and hence they are suited for food

applications (Raja et al., 2010). An increased health-conscious public now tries to avoid foods

with chemical preservatives or which have undergone extensive processing. The most powerful

means for obtaining useful cultures for scientific and commercial purposes are isolation and
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screening of microorganisms from natural sources (Vanden et al., 1993). Isolation procedures

employed by different researchers were relatively similar, but for the culture conditions and the

growth media required they differed between different food sources. The principle involved in

their purification remained the same.

Isolation of LAB from milk products

According to the procedure employed by Arokiyamary and Shivakumar (2011) on milk products,

isolation of bacteriocins from LAB was standardized. The bacterial count was performed to

make appropriate dilutions on the most accepted medium, MRS agar, to maintain optimal

growth. The LAB grown in an aerobic environment, utilizing the nutrients from MRS agar, were

isolated using bacteriological techniques.

Isolation of bacteriocins from appam batter

Vijai et al., (2005) standardized a procedure for the extraction of bacteriocins from South Indian

special dosa (commonly known as appam) batter. Saline dilutions of appam batter, cultured on

MRS agar anaerobically, was transferred to MRS broth and checked for purity. For the purpose

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of upgrading purity, sterilization of centrifuged supernatant using a filter membrane of 0.22 µm

was utilized.

Isolation of bacteriocins from chicken intestine

Apart from food products, isolation of bacteriocins has been reported in marine environments,

rock sediments, and chicken intestine. Narayanapillai et al., (2012) have designed an isolation

method from chicken intestine. Briefly, pure cultures obtained from inoculation of crushed

pieces of chicken intestine were grown on MRS agar at optimum temperature to test the
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bacteriocin production. The strains from the pure culture were Gram-stained to examine

bacteriocin-producing bacteria and further grown at optimum temperature.

Bacteriocins, being an extremely heterogeneous group of substances, their purification to

homogeneity become a very complex task. Although bacteriocins are generally extracted after

centrifugation using the ammonium sulfate precipitation method, there are 3 other major

methods of purification which have been widely accepted. The first is a conventional method and

includes ammonium sulfate precipitation, ion exchange, hydrophobic interaction, gel filtration,

and reverse phase high-pressure liquid chromatography (RP-HPLC). A second method is much

simpler and generally used for the production of bacteriocins at laboratory-scale. The steps

involve ammonium sulphate precipitation, solvent precipitation using chloroform/methanol and

then RP-HPLC. The third bacteriocin purification method requires maximization of the

bioavailability of bacteriocins by varying the pH of the fermentation medium. Further, a standard

unit operation protocol, namely hydrophobic interaction gel or expanded bed adsorption, can be

employed. This method is used for the production of bacteriocins at bulk scale (Eduardo et al.,

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2013). Isolation of bacteriocins has also been done from a variety of food systems like dhokla,

khaman, murabba, chyawanprash, kalakand, and rasgulla.

Characterization principles of common bacteriocins

By definition, bacteriocins can also be designated as antibiotics due to their bactericidal mode of

action against closely related species (De Man et al., 1960; Klement et al., 1990; Kuryolowcz

1991; Davis 1999). The most abundant and diversified molecules with antibiotic activity

produced by different bacteria including Gram-positive and Gram -negative species are
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bacteriocins (Riley 1998). A major difference between bacteriocins and antibiotics is found in

their activity of inhibiting specific microorganisms. Bacteriocins restrict their activity to strains

of related species whereas antibiotics have a wider activity spectrum and do not show any

preferential effect on closely related strains (Jennifer et al., 2001).

Based on their molecular size, antibacterial spectrum, stability, physical and chemical properties,

and action mode, bacteriocins are formed into heterogeneous groups (Davidson and Hoover

1993; De Vuyst and Vandamme 1994, b). Most bacteriocins of low molecular weight are

cationic and have greater antimicrobial activity at low pH (Sinell 1989; Bendjeddou et al., 2012).

Adsorption of bacteriocins to Gram-positive cell surfaces is dependent on pH and shows

maximum adsorption at or above pH 6. The mode of action, effect of heat, pH, proteolytic

enzymes, salt, and detergents on bacteriocin activity, determination of molecular mass, amino

acid composition and sequence, and determination of the genetic organization, production, and

secretion are included in the characterization of bacteriocins (Svetoslav 2009).

Biochemical characterization of bacteriocin BacUB9

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According to the experiments conducted by Maja et al., (2010) bacteriocin BacUB9 is a heat-

stable molecule. It is produced from a Gram-positive bacterium, Lactobacillus paracasei subsp.

paracasei BGUB9.Among the 2 bacteriocins characterized from this bacterium, BacUB9 is the

one which has a very narrow anti-microbial spectrum. Its molecular mass is 4 kDa and it is

susceptible to the activity of proteolytic enzymes. Its activity decreases at 100ºC for 60 min and

its activity is completely abolished at 100ºC for 120 min. Bacteriocin BacUB9 retains its activity

in the pH range of 1-10 when it is present in a cell-free supernatant of the producer strain.
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Antimicrobial activity is lost at pH 11. Treatment of bacteriocin UB9 with various proteolytic

enzymes (pepsin, trypsin, α-chymotrypsin, pronase E, and proteinase K) results in the loss of its

antibacterial activity. Bacteriocin UB9 shows that it is of a proteinaceous nature and it is strongly

suggested that it belongs to the class II bacteriocins.

Molecular characterization of bacteriocin Carocin D

Carotovoricin and carocin S1 are 2 different bacteriocins which are found in the Gram-negative

bacterium Pectobacterium carotovorum subsp. carotovorum, causing soft-rot disease in various

plants (Eunjung et al., 2010). Carocin D is the third bacteriocin found in the same producing

species. An antibacterial activity of carocin D against the indicator strain Pcc3 is carried by a

particular strain Pcc21 (Chan et al., 2009). Carocin D is encoded by the caroDK gene located in

the genomic DNA, which is an immunity protein providing protection. The Edman degradation

process determined the N-terminal amino acid sequences of purified carocin D. In a comparison

with the amino acid sequence of caroDK, it was found that 8 amino acids are missing at the N

terminus. Mora et al., (2008) and Bendjeddou et al., (2012) proved that 8 amino acids are

removed from the N terminus of carocin D during maturation and that it is synthesized as a

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precursor peptide. Bacteria became resistant to carocin D, when caroDK and caroDI genes were

transformed into carocin D-sensitive bacteria such as Pcc3. This bacteriocin is slight resistant to

heat but not to proteases. CarocinD sensitive, non-pathogenic bacteria readily express this

bacteriocin, which has great potential as a biological control agent.

Chemical and genetic characterization of bacteriocins Carnobacteriocins BM1 and B2

According to observations made by Quadri (1994), the Gram-positive bacterium

Carnobacterium piscicola LV17B produces carnobacteriocins BM1 and B2, which are thermo
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stable class II bacteriocins. The purification of these bacteriocins includes hydrophobic

interaction, size exclusion, and reversed-phase high-performance liquid chromatography (Pillet

et al., 1995). Using the information from the N-terminal amino acid sequences for the purified

bacteriocins, probes were synthesized to locate structural genes for the carnobacteriocins

(Saucier et al., 1995). A HindIII fragment of 1.9-kilobase (kb) from a plasmid (pCP40) of 61-kb

contains the carnobacteriocin B2 structural gene. Presence of the 61-kb plasmid is necessary for

the expression of chromosomal bacteriocin and its immunity function. These bacteriocins are

synthesized as pre-bacteriocins (Jack et al., 1995). Mature 43-amino acid carnobacteriocin BM1

(4524.6 kDa) and the mature 48-amino acid carnobacteriocin B2 (4969.9 kDa) are obtained by

the post-translational cleavage of an 18-amino acid N-terminal extension at a Gly-Gly (positions

-2 and -1). These 2 peptides show significant amino acid homology to each other and with those

class II bacteriocins containing the YGNGV amino acid motif near the N terminus.

Biochemical and genetic characterization of bacteriocin Nisin Z

Nisin is the first lantibiotic (Class I - Bacteriocins) mentioned in the scientific literature; it is

produced by certain strains of Lactococcus lactis (Jung 1991; Murugesh 2003). It has a

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molecular weight of 3354 and is composed of 34 amino acids and displays a bactericidal mode of

activity and is said to be nontoxic to animals and humans (Hurst 1983). Rogers and Whittier

observed its activity for the first time in 1928, and it was studied as a discrete antimicrobial

substance in 1944 (Mattick and Hirsch 1947). Nisin is the best-studied bacteriocin produced by

some Lactococcus lactis strains and has been used for food preservation in over 50 countries.

The corresponding study describes characterization of nisin Z-producing L. lactis strain isolated

from Boza traditional cereal-based fermented food from Turkey. In this study, bacteriocin by
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Lactococcus lactis subsp. lactis GYL32 strain inhibited not only related strains but also Gram-

positive bacteria, such as Listeria monocytogenes, Staphylococcus aureus, and Bacillus cereus.

Treatment with proteinase K and α-chymotrypsin inactivates the antimicrobial substance. It is

heat-stable when treated at 100 ºC for 20 min. Different pH, enzyme, and heat treatments

concluded that the bacteriocin produced by GYL32 is nisin Z. The sequence analysis result

showed that it is nisin Z, and its genetic determinants are encoded on genomic DNA. The

molecular weight of nisin Z was determined as 6,700 Da by Tricine-SDS-PAGE analysis. The

results of this study suggested that nisin Z producer L. lactis subsp. lactis GYL32 strain may be

used as a starter culture for improving the safety of fermented products (Gozde and Yasin 2012).

Optimization

Different ecological niches from which strains of bacteriocin have been isolated, including meat,

fish, fruits, vegetables, milk, and cereal products (Ammor et al., 2006). Factors affecting the

bacteriocin production include type of medium used, glucose concentration, temperature, pH,

and agitation (De Vuyst and Vandamme 1994, b); Sanchez et al., 2002). These bacteriocins

differ widely in molecular weight, pH, presence and number of particular groups of amino-acids.

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However, the differences in antimicrobial activity cannot be solely attributed to the amino acids

or its sequences present (Svetoslav 2009).

Some of the widely used bacteriocins have been well researched and their production has been

well optimized. For example, in the production of nisin and pediocin PA-1 from P. acidilactici,

Yang and Ray (1994) identified that high cell density, optimal pH, and specific nutrients in the

media resulted in an increased yield. Specifically for nisin, the pH optimum was identified to be

pH 4 – 6 and temperature optimum at 150C. Also, Coventry et al., (1996) established that
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significant protein-free production of bacteriocins was obtained using food-grade diatomite

calcium silicate and several desorbing agents in comparison to ammonium sulfate precipitation.

Universally, Class I and Class II bacteriocins are stable at acidic pH. Rodriguez et al., (2002) and

Jack et al., (1996) effectively demonstrated this for pediocin PA-1 and piscicolin 126 which

remained stable at pH range between pH 4-6 and pH 2-3, respectively. According to Usmiati

(2009), the optimum conditions for bacteriocin production on S. typhimurium, E. Coli, and L.

monocytogenes (Holo et al., 1991; Sullivan 2002) are at 330 C and pH 5. The trials involved 2

steps:

i. Lactobacillus isolates are selected based on their potential in producing bacteriocins.

ii. Bacteriocin production process is optimized (Bromberg et al., 2004).

The parameters to be observed are turbidity of bacterial culture in nutrient broth and the number

of activated colonies of the isolate (Vaughan et al., 2001). Svetoslav et al.(2012) observed that,

bacteriocin ST22Ch belonging to Class II group, had a narrow spectrum of activity, was heat-

resistant and stable at pH 2-10. He also observed that different levels of bacteriocin ST22Ch are

produced during the stationary phase of fermentation in the presence of 2% (w/v) glucose and a

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combination of tryptone, meat extract, and yeast extract. These findings determined the varying

requirements for an optimal production of bacteriocins.

Assays for the detection of bacteriocins and their activity

For the detection of bacteriocin production and its activity, many methods have been described.

It is a fact that bacteriocins can diffuse in solid or semisolid culture media, which can be

subsequently inoculated with a suitable indicator strain. Making use of this fact, authors Kekessy

and Piguet (1970) conducted experiments on the detection of bacteriocins using agar. Indicator
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and producing strains of bacteria were used for the screening purpose (Nicolle and Prunet 1964).

Micro-titration method for bacteriocin activity assay

Using the micro-titration method involving polystyrene micro-plate wells containing MRS broth,

Daba et al., (1994) made serial 2-fold dilutions of bacteriocin preparations. The diluted culture

was incubated at optimum temperature and the activity was further detected. For the experiment,

P. acidilactic bacteria were utilized.

The ELISA test

Bouksaim et al., (1999) utilized ELISA for the detection of bacteriocins. They mainly used

affinity-purified anti-nisin immunoglobulin for the binding of nisin and anti-nisin peroxidise

which was linked with the substrate. A carbonate-bicarbonate buffer of basic pH was used for

incubation. To reduce the nonspecific binding, the microtiter wells were coated with a blocking

reagent, Tween-20. The bound enzyme was determined which implied the amount of

bacteriocins. ELISA and agar diffusion assays, even though were more sensitive for pure nisin,

they failed to differentiate nisin from subtilin and also the closest structural analogue of nisin

(Fowler et al., 1975; Falahee et al., 1990). Later, competitive direct ELISA assays were

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published by Suarez et al., (1996) where the detection limit for nisin was based on polyclonal

mouse antibodies, and the above limit for nisin was measured utilizing the monoclonal mouse

antibodies.

Turbidimetric assay for nisin

It was used for detection of nisin by Simone et al., (2003) by the use of a special media

containing meat extract, yeast extract, tryptone, glucose, NaCl, Na 2HPO4 with neutral pH. At

specific time intervals, samples were collected, their optical densities were measured
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spectrophotometrically and the growth curve of the test microorganism was obtained. To stop the

further growth of microorganism, the samples were injected with thiomersalate solution.

Electrophoretic method

The only electrophoretic method for nisin quantification has been published by Rossano et al.,

(1998). Their capillary zonal electrophoretic assay was used to analyze nisin from milk. The

bioluminescence genes from Xenorhabdus luminescens species were placed under the nisin

inducible promoter in the same plasmid and were transformed into the non-nisin producer L.

lactis. This led to the extra cellular nisin stimulation and a subsequent addition of substrate for

the luciferase, resulted in bioluminescence by the indicator strain (Wahlstrom and Saris 1999).

Very recently Immonen and Karp (2007) introduced an improved luciferase assay.

Chemiluminescence-assisted Immunodot assay for nisin

It was described by Bouksaim et al., (1999) in which serum from rabbit immunized with nisin Z

was used to detect nisin. Dadoudi et al., (2001) developed the first method to distinguish between

nisin A and nisin Z. The monoclonal antibodies raised against nisin Z could be used to quantify

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nisin Z with detection limits in pure solution, in fermentation broth, in milk and in whey and the

antibodies developed this way did not cross-react with nisin A.

Detection using agar

It is a fact that bacteriocins can diffuse in solid or semi-solid culture media, which can be

subsequently inoculated with suitable indicator strain like phage (FredericQ 1957). Before

proceeding to any steps of assay, chloroform vapour was used to ensure the sterility of agar

surface. As chloroform vapours attack plastic, the assay does not allow the use of plastic Petri-
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dishes (Nicolle and Prunet 1964). Kekessy and Piguet (1970) described a new technique based

on the tri-dimensional diffusion of bacteriocins. The detection of bacteriocins was done on the

reverse side of agar plate which serves as culture surface for the indicator strain. There is no

direct contact between producer and indicator strains of bacteria. As in the case of other

methods, where it is not easy to decide whether a zone of inhibition is due to either producing

strain or indicator strain, in this method, no inhibition area due to indicator strain are formed.

Beneficial aspects of bacteriocins

In context to food, it isn’t enough to only improve production but it is also necessary to store the

produce for distribution and later use. But there are many criteria considered, in order to safely

store food products (Brul and Coote 1999). The currently existing preservatives are not entirely

satisfactory to the consumers, food laws or the producers. Food preservation basically requires

the maintenance of the functional properties of the product, and also other physico-chemical

properties so that it remains appealing to the consumer. However, higher the preservative

treatment, higher is the damage caused to the food product (Ray 1992). Thus, continued

treatment with the preservatives could effectively nullify their use.

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Bacteriocins as biopreservatives

In recent times, there is a continuous raise of awareness in the public regarding the amount of

chemical intake, which curbs the amount of chemical preservatives that may be used in food

(Harris et al., 1997). Thus, barely any variety exists without controversies of the multifarious

health problems associated with them. In view of the above problems, bio-preservatives are in

very high commercial demand at present, in the form of protective cultures or their metabolites

i.e. enzymes and bacteriocins (Holzapfel et al., 1995). Bio-preservation is defined as extension of
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shelf life and food safety by use of natural or controlled microbiota and/or their antimicrobial

compounds. The destruction of the pathogens depends on improved food safety by search of

more efficient chemical preservative and drastic physical treatment (high temperature treatment).

These have various drawbacks such as toxicity of chemicals used, nutritional alteration of food

and to overcome these disadvantages, LAB and their bacteriocins are being popularized.

Bacteriocins from LAB

Lactic acid bacteria have been widely used for thousands of years in the production of fermented

products. Since they are present in several consumed products, they have been deemed safe for

human consumption and been provided the GRAS (Generally Regarded As Safe) status

(Jeevaratnam et al., 2005). Due to this, most of the research on bacteriocins so far has been

concentrated exclusively from LAB. The bacteriocins from food grade Lactic Acid Bacteria

(LAB) qualify as an ideal food bio preservative primarily because:

i. It is proven non-toxic to humans

ii. Does not alter the nutritional properties of the food product

iii. Effective at low concentration

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iv. Active under refrigerated storage (Sinell 1989; Daeschel and Ray 1992; Gould 1995).

FDA approved bacteriocin–nisin

Most of the Gram-positive bacteria are especially susceptible to Nisin (Class I-Bacteriocin), but

have little or no effect on Gram-negative bacteria, yeast or fungi (De Vuyst and Vandamme

1994, a). In the year 1969, nisin was stated to be safe and natural food additive by FAO/WHO

expert committee on food additive (FAO/WHO 1969). Nearly 15 years later, nisin was used

commercially in around 39 countries (Hurst 1983). It was given the designation E234 in 1983
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after being incorporated to the EEC food additive list (EEC 1983). Nisin was GRAS (Generally

Recognized As Safe) certified in USA in 1988 (Federal Register 1988) and by Food and Drug

Administration in the year 2001 (FDA 2001). It was allowed as food additive in more than 50

countries including Europe, China and the US by the year 1996 (Delves-Broughtan et al., 1996).

Its potential application was first demonstrated in 1981 for food preservation and elaborated its

use since 1990 (Delves-Broughtan 1990). Nisin concentrate was commercialized as ‘Nisaplin’ by

Alpin and Barrett which is now used as a preservative in dairy products, cured meat, canned food

and other fermentation industry divisions. Nisin was first discovered in 1928 as a result of

difficulties faced in cheese making where storage of milk had supported the growth of

contaminant organisms to produce the inhibitor (Hirsch et al., 1951). A partially purified form of

nisin was commercially made (De Vuyst and Vandamme 1994 , a; Twomey et al., 2002) and a

saleable bacteriocin-containing fermented powder is available as a food additive (Rodríguez et

al., 1999).

Bacteriocins have been found to inhibit food spoilage by pathogenic bacteria such as

Staphylococcus aureus (Chang and Chang 2011), Escherichia coli (Foulds and Shemin 1969),

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Bacillus cereus (Kabore et al., 2013), Listeria monocytogenes (Pucci et al., 1988) and

Clostridium perfringens (Gamal 2006) which are recalcitrant to food preservation methods. The

production and application of bacteriocin could effectively combat nearly all of the problems of

the food industry apropos preservation. Bacteriocins are well suited for this purpose due to their

thermo-stability and pH tolerance.

Bacteriocins from traditional products

There are so many different types of food ranging from spicy ethnic food to down home
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favourites. The options are endless, even within a particular recipe or type of food. India being

the country of diversified geographical and cultural origin is also known for its many traditional

cuisines. Many of these products, apart from their cultural heritage also have been known to

possess many beneficial qualities. Few examples of such products are dosa (Mallesha et al.,

2010), idli (Vijayendra et al., 2010), kokum (Khurana and Kanawjia 2007) and lassi (Amit et al.,

2012). They are traditionally known for their effects such as cooling the body, aiding digestion,

probiotic effects, protection against certain microbial attacks and so on.

Indian traditional products provide a promising array of sources for obtaining bacteriocin

producing bacteria. Lactic acid bacteria isolates from appam batter, capable of producing good

amount of bacteriocins have been identified by Vijai et al., (2005). Isolates of bacteriocin

producing microorganisms were also isolated from curd, dosa batter and idli batter and the

bacteria were identified as a species of Lactobacillus while the effect of physical and cultural

parameters were tested on them (Sourav and Arijit 2010). Lactobacillus species was also recently

isolated from different milk products such as curd, milk peda, butter and ghee and the bacteriocin

from them were found effective against many common food pathogens (Arokiyamary and

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Shivakumar 2011). So it is sufficiently established that Indian traditional products are rich in

lactic acid bacteria that produce bacteriocins with the potential to be used as food preservatives.

However, most of the work was started only very recently and there are still many unexplored

traditional products that may provide invaluable bacteriocins.

CONCLUSION

Bacteriocins are a diverse group of antimicrobial proteins or peptides ribosomally encoded

covering a broad range of applications in the food and medical industry. They employ a variety
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of killing mechanisms that contain genes which are either chromosomally or plasmid encoded

with certain toxins. Bacteriocins possess relatively narrow killing spectrum that includes

cytoplasmic membrane pore formation, cell wall interference and nuclease activity that alters the

cell membrane permeability properties. Most of the bacteriocins were originally isolated from

organisms which are involved in food fermentation. Considering its wide applications,

optimization of the production of bacteriocins requires much attention. LAB produced

bacteriocins also known as Lantibiotics, were regarded as GRAS and hence is one of the most

researched types of bacteriocins. The most potent lantibiotic is nisin which is produced by

Lactococcus lactis and has been regarded as the only bacteriocin used as a food preservative that

has been approved by the FDA. Various bioassays are designed most of which are with regard to

Nisin which also finds applications in pharmaceuticals. Bacteriocins are potentially used in food,

human and animal health applications. The use of bacteriocins is of great interest in the food

system since they are recognized as safe and can also be used as bio-preservatives. Thus it is

desirable to expand the understanding of the activity of bacteriocins in order to determine their

efficacy more accurately for future applications in food model systems. Food safety is deemed as

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the paramount of international concern. Since bacteriocins are considered as natural products,

usage of bacteriocins in food systems will surely gain good acceptance from customers who

demand for more natural and safer food products that are free from chemicals.

Declaration of Interest

The authors declare there is no conflict of interest

ACKNOWLEDGEMENTS

Ramith Ramu thanks TEQIP New Delhi, India for awarding the Research fellowship. The
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authors are grateful to the Principal, Sri Jayachamarajendra College of Engineering, Mysore, and

the Head of the Department of Biotechnology for their encouragement and support. DBL thanks

Jain University for constant encouragement and support given to the progress in research.

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Table. 1: Various bacteriocins and their target bacteria in food systems

Producing Source References


Group Bacteriocin Target Bacteria
Strain

Camambert, Hirsch and


Clostridium
ricotta and others 1951;
Class I Nisin botulinum, Listeria
manchego Sulzer and
monocytogens
cheese. Busse 1991
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Enterocin
AS-48,
Listeria Ananou and
Class II Enterocin A, Meat
monocytogens others 2005
Pediocin
Gram
ACH
positive
Staphylococcus Wu and others
Pasteurized
Class III aureus and 2003; Maria
Lysostaphin milk, cheese,
Staphylococcus and others
sausages
epidermidis 2004
Carr and
L. paraplantarum Milk and others 2002;
Class IV Plantaricin S
and L. pentosus cheese Pepe and
others 2004
Brenda, 2007;
Obi and
Colicins Colicin E1 E.coli O157:H7 Meat
Campbell,
Gram
1978
negative
Probiotic Anke and
Microcins Microcin S E. coli E2348/69 drug others 2012
Symbioflor 2

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Fig 1: Classification of Bacteriocins

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Fig 2: Mechanism of Pore Formation by Nisin

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