Importance of microbial antagonisms about food attribution

Science against microbial pathogens: communicating current research and technological advances
______________________________________________________________________________
A. Méndez-Vilas (Ed.)
Importance of microbial antagonisms about food attribution
Zerrin Erginkaya1, Emel Ünal1 and Selin Kalkan1
1
University of Cukurova, Department of Food Engineering, Adana, Turkey
Some microorganisms can inhibit other microorganisms or reduce their growth in medium thanks to their metabolites,
indirect (by changing pH, osmotic pressure and surface tension) or direct (by producing toxic component, antimicrobial
component, bacteriocin, antibiotic etc.), this situation is called as antagonistic relation. These antagonistic interactions
among microorganisms have been used often in biologic attribution of food. In recent years, depending on use of
antimicrobial microorganisms and their metabolites in various food products, studies about stability and shelf life
extension have gained a special importance. Nowadays, the most extensive research and commercial practices are based
on lactic acid bacteria. In addition to lactic acid bacteria, it was reported that probiotics, yeast, fungus and bacteriophage
have antagonistic characteristics. In this chapter, antagonistic relation among some microorganisms gradually increased
importance about food attribution and often focused was explained
Key words: Antagonism, food attribution, microorganisms
1. Introduction
In recent years, consumers prefer natural foods without chemical preservatives about food attribution. As a result of this
situation, methods of natural protection begin to popular in food attribution and new preservation methods are focused
on the use of microorganisms or of their metabolites; thus it was focused on antagonistic relation among
microorganisms. In 1976 firstly by Antonie van Leeuwenhoek, antibiosis was mentioned as a biological interaction
between two or more organisms that is detrimental to at least one of them or an antagonistic association between an
organism and the metabolic substances produced by another. Also in 1877 Louis Pasteur and J.F. Joubert were reported
that urine bacteria have inhibitor effect on Bacillus anthracis. In addition to these, it was found bacteriocins, antibiotics,
lytic agents, bacteriolytic enzymes, bacteriophage and other metabolic products like hydrogen peroxide and diacetyl as
other inhibitors produced by bacteria. These antagonistic interactions among microorganisms have been used often in
biologic attribution of food. Lactic acid bacteria, yeast, fungus and bacteriophages have antagonistic characteristics and
these are used on food attribution. Especially in recent years, depending on use of microorganisms and their
antimicrobial metabolites in various food products, studies about stability and shelf life extension have gained a special
importance. Nowadays, the most extensive research and commercial practices are based on lactic acid bacteria [1-10].
In this chapter, it was explained antagonistic relation among these important microorganisms gradually increased
importance about food attribution.
2. Microbial Antagonisms
Some microorganisms can inhibit other microorganisms or reduce their growth in medium thanks to their metabolites,
indirect (by changing pH, osmotic pressure and surface tension) or direct (by producing toxic component, antimicrobial
component, bacteriocin, antibiotic etc.), this situation is called as antagonistic relation. For example, organic acids
produced by microorganisms have antimicrobial effect on sensitive microorganisms to acids. Also some bacteria
prevent growth of some other bacteria in media by producing metabolite called as bacteriocin. The most intensive
studies and commercial practices about microbial antagonisms have focused on lactic acid bacteria. In addition to lactic
acid bacteria, it was reported that probiotics, yeasts, fungus and bacteriophages have antagonistic characteristics [1120].
2.1 Antagonistic characteristics of Lactic Acid Bacteria
Lactic acid bacteria are well known as beneficial bacteria and include probiotic bacteria that help maintain a good
enteral environment and producers of biopreservatives in dairy products and fermented foods. It was determined in
some researches that lactic acid bacteria have antimicrobial effects on some bacteria, pathogens, fungus and yeasts and
also play an important role in detoxification of mchotoxins. Antagonistic effect of lactic acid bacteria is from their
metabolites like lactic acids and other organic acids, H2O2, bacteriocin or antimicrobial components similar to
bacteriocin, also diacetyl, ethanol and CO2 [5,6, 16, 23, 24, 26, 27, 40, 44, 55, 56, 73, 84, 85].
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Science against microbial pathogens: communicating current research and technological advances
_______________________________________________________________________________
A. Méndez-Vilas (Ed.)
2.1.1 Bacteriocins
Bacteriocins are bacterially produced antimicrobial peptides with narrow or broad host ranges. Antimicrobial effects of
bacteriocins against sensitive microorganisms change depending on environmental factors like pH, temperature,
composition and constitution of food [13, 14, 19].
Whereas bacteriocins are mostly synthesized by gram(+) bacteria, they are also produced by gram(-) bacteria.
Bacteriocin produced by gram(-) is called as “microcin”. The size of protein, effect spectrum and mechanisms of
microcins are diffrent from bacteriocin produced by gram(+) bacteria. Whereas bacteriocin are known as an important
biocontrol method in reduction of illness from food, some researcher was reported that bacteriocin can’t be used as first
process step in pathogen inhibition, but it was noted that bacteriocin can be used with adding hurdle methods in
preventing illness from food. Namely, it was determined that when bacteriocins are used with other protective
components or attribution methods in food protection, they were more effective. It was mostly used bacteriocins
synthesized by lactic acid bacteria in foods. Use of bacteriocin synthesized by lactic acid bacteria highly increased in
food, because it has antimicrobial effect on most pathogen like Listeria monocytogenes, Staphylococcus aureus,
Clostridium botulinum ve Salmonella spp. [25, 34, 35, 42, 47, 58, 69].
2.1.2 Organic Acids
Lactic acid bacteria especially some species like Lactobacillus, Lactococcus, Leuconostoc, Pediococcus and
Streptococcus have been used as protective in fermented foods for long years. While homofermentative lactic acid
bacteria produce lactic acid bacteria from hexose, heterofermentative lactic acid bacteria synthesized acetic acid beside
lactic acid. Lactic acid bacteria have secured food safety and quality by be reducing pH with these acids. Lactic acid are
sour taste and odorless. It can mix easily with water and polimere, alcohol and ether; it is good solvent, weak acid.
Lactobacillus species synthesized more lactic acid than Streptococcus species (51, 54).
Lactic acid bacteria have antimicrobial effect on pathogen bacteria like Escherichia. coli, Staphylococcus aureus,
Salmonella spp.and Listeria monocytogenes in especially meat and dairy products, also spoilage bacteria, yeast and
fungus in food product [68, 70, 71, 86, 80].
It was determined with several researches that both lactic acid and acetic acid synthesized by lactic acid bacteria have
antimicrobial effects with wide spectrum on fungus, yeast and bacteria and also when there is propionic acid in media,
antifungal effect of acetic acid increase [51, 54, 68, 70, 71].
2.1.3 Hydrogen Peroxide
Hydrogen peroxide (H2O2) is produced during aerobic growth of lactic acid bacteria and it is an oxidizing component.
Hydrogen peroxide has antimicrobial effect on vegetative cells and spores of most microorganisms. Antimicrobial
effect of H2O2 has occurred by changing chemical structure and biochemical characteristics of enzymes of target
microorganisms. H2O2 inhibit most pathogen bacteria like Staphylococcus, Escherichia coli O157:H7, Pseudomonas
and Clostridium, also spoilage. Most researches were shown that contents of H2O2 produced by lactic acid bacteria in
optimum conditions is enough for inhibition of psychrophile bacteria [66, 83].
2.1.4 Laktoperoxidase
Lactoperoxidase is an enzyme that is found in secretion like milk, colostrum, salivary and lacrima. But, this enzyme is
effective when there are H2O2 and thiocyanate (SCN–) in medium and thus it can show antimicrobial activity. In
general it is known as lactoperoxidase system (LPS). Quantity of laktoperoxidase enzyme in cow milk is 3mg/100 ml or
much more. Quantity in breast milk is less. On early days after birth, antimicrobial activity reaches to maximum level.
While it show bactericidal effect against some bacteria, it show bacteriostatic effect against some. In general, this
system is more effective on gr(-) bacteria than gr(+) bacteria. LPS show bactericidal effect on bacteria like C. jejuni, L.
monocytogenes, Pseudomonas aeruginosa, Salmonella, S. aureus, ve Yersinia enterocolitica, also Coliform bacteria. It
has been used as protective component in region that hygienic conditions is not good and during transport of raw milk
from fabrics as non-cooler [16, 21, 67].
2.1.5 Diacetyl
Diacetyl is a product synthesed from pruvat as a result of metabolism of hexoses by lactic acid bacteria. Diacetyl has
butter odor.
It was found in most fermented product, especially dairy products and products from lactic acid
fermentation. Homofermentative lactic acid bacteria are formed more diacetyl than heterofermentative lactic acid
bacteria. Diacetyl show more inhibitor effect on gram(-) bacteria, fungus and yeasts than gram(+) bacteria. Also lactic
acid bacteria are highly resistant to diacetyl [6, 16, 41, 50, 59, 63, 88].
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Science against microbial pathogens: communicating current research and technological advances
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A. Méndez-Vilas (Ed.)
2.1.6 Ethanol
Ethanol is an antimicrobial metabolite produced by heterofermentative lactic acid bacteria. But in general production of
ethanol is low during fermentation. Ethanol can’t be effective in food protection because it was inactivated by organic
components in media [6, 16, 41, 50, 59, 63, 88].
2.1.7 CO2
CO2 is formed by most microorgnisms via fermentation and has antimicrobial effect; also it is a fermentation product of
heterofermentative lactic acid bacteria. Synthesis of CO2 and antimicrobial effect occur in anaerobic conditions. In
today, commonly it was utilize from antimicrobial effect of CO2 in biocontrol of product packed in modified
atmosphere. Gram(-) bacteria is more sensitive to CO2 in modified atmosphere than gram(+) bacteria. Also lactic acid
bacteria are more resistant than obligate aerobic microorganisms [6, 16, 41, 50, 59, 63, 88].
2.1.8 Antimicrobial Compounds with Low Molecular Mass
It was reported that some species of lactic acid bacteria synthesized compounds with low molecular mass. These
compounds have antimicrobial activity and are active in low pH, thermostable, and can solve in acetone. Out of
reuterin, reutericiklin and 2-pyrolidone-5-carboxylic acid from these components, others are not identified and it hasn’t
been found detail information about antimicrobial effect mechanisms yet [6, 16, 41, 50, 59, 63, 88].
2.1.9 Exopolysaccharides and Biofilms
A biofilm is an aggregate of microorganisms in which cells adhere to each other on a surface. These adherent cells are
frequently embedded within a self-produced matrix of extracellular polymeric substance or exopolysaccharide (EPS).
Exopolysaccharides (EPS) play an important role on bacteria resistance and form much level of biofilm. Many lactic
acid bacteria are able to produce exopolysaccharides (EPSs). Most lactic acid bacteria that have probiotic
characteristics and produce biofilm form protective effect against pathogenic bacteria. In recent years, it has been noted
that biofilm produced lactic acid bacteria has antibacterial effect especcially on some pathogen formed regard food
safety in meat and dairy products. Researches were especcially focused on antilisterial effect of biofilm formed lactic
acid bacteria. Also, it was reported that biofilms produced by lactic acid bacteria are effective on fungus. But, it should
be studied more about biofilms and focused on use of lactic acid bacteria biofilms as biocontrol agents with new studies
in food industry [31, 46, 77].
2. 2 Probiotics
Probiotics are live microorganisms thought to be beneficial to the host organism. Probiotics are commonly consumed as
part of fermented foods with specially added active live cultures; such as in yogurt, soy yogurt, or as dietary
supplements. Consumption of probiotics has about benefits about healthy. Some these benefits include: enhancing
bowel function, prevention of colon cancer, cholesterol lowering, lowering of blood pressure, improving immune
function and reducing infections, reducing inflammation, improving mineral absorption, preventing growth of harmful
bacteria, fighting off diseases like candida and exzema, and many more. Benefit about preventing growth of harmful
bacteria show that probiotics have also antagonistic characteristics. Because of all these benefits of probiotics, it was
reported that use of probiotic in food products will be helpful on food attribution and microbial quality of food [29, 30,
36, 37, 39, 62, 64].
2.3 Antagonistic Characteristics of Yeasts
Some yeasts having antagonistic effect against some fruit pathogens have been reported in 1980-1990. This antagonistic
effect has shown by Debaromyces hansenii in citrus and some of the species belong to Cryptococcus in apples and other
fruit has been reported [38, 61, 75, 76].
The main advantages of the antagonistic features of yeasts are list in; they don’t produce allergy-causing spores and
mycotoxins and synthesize antimicrobial metabolites. In addition, nutrient requirements for growth of yeast are not very
complex and even can be colonizing on dry surface for a long time. Use of yeast is economic compared with the other
chemical antimicrobial because substrates used for growth are cheaper. In addition to the antagonistic effects of yeasts,
yeasts are recommended for usage about food and animal feed because yeast cells have high amounts vitamins,
minerals and essential amino acids [65, 78, 82, 87, 89].
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Science against microbial pathogens: communicating current research and technological advances
_______________________________________________________________________________
A. Méndez-Vilas (Ed.)
2.3.1 Killer yeast
Some yeast synthesize toxin that has protein and glycoprotein structure and thus thanks to structure of toxin these yeasts
inhibit other sensitive strains to toxin. This synthesized protein is named killer protein or killer toxin and so this yeast
called as killer yeast. For the first time, killer yeast was found in Saccharomyces cerevisiae species by Bevan and
Makower in 1963. This toxin is only effect on eukaryotic cell and has not an effect on human and prokaryotic cell. It is
inactive at body temperature or degrades enzymatically (38, 87).
As known that some strains of yeasts have killer activity such as Candida(C. valida,C. albicans), Cryptococcus(C.
laurentii), Hanseniaspora(H. uvarum), Hansenula(H. anomala, H. mrakii, H. subpelliculosa), Kluyveromyces(K.
marxianus, K. wickerhamii, K. phaffii), Pichia ( P. kluyveri, P. membrafaciens ), Saccharomyces ( S. cerevisiae, S.
chevalieri, S. bayanus, S. capansis, S. uvarum) [76, 78, 82, 87, 89].
Killer yeast, in particular, becomes the dominant at spontaneous fermentation of wine. Because of these properties,
when killer yeasts used as starter culture, controlled fermentation takes places. However, studies about selection as
starter culture of these yeasts should make both in vivo and in vitro, because killer yeasts show different characteristics
in different environments [82, 87, 89].
2.3.2 Some commercial yeasts used as bio-control products
Nowadays, commercial yeast is used as bio-control products especially in order to prevent to deterioration of fruits after
harvest. The product known as “Aspire” has been used in the U.S. since 1996 and this product includes Candida
oleophila. Aspire is used against deterioration during storage fruits such as citrus, apple and pear by spray or by
immersion solution containing a certain concentration of yeast. “Yield plus” since 1997 in South Africa, have been
used for bio-control of Botrytis, Penicillium and Mucor causing deteriorations on particularly varieties of apples and
the other fruits. Cryptococcus albidus is antagonistic yeast in Yield plus. “Shemer” is another bio-control product
based on Metschnikowia fructicola and has been described and approved in 2001 in Israel. It has broad use spectrum on
fruits such as grapes, strawberries and sweet potatoes [11, 12, 38, 61].
It was utilized from antifungal characteristics of some Debaryomyces species during storage of fruit and dairy
products. These yeasts have been used as commercial for inhibition of some fungus such as Aspergillus sp.,
Byssochlamys fulva, Byssochlamys nivea, Cladosporium sp., Penicillium candidum ve Penicillium roqueforti [75, 76,
78, 82, 87, 89].
2.4 Fungal Pigments
Many studies have been done about the antioxidant and vitamins properties of the pigments synthesized by
microorganism. Even today some of them are commercial production to be use in foods. The antimicrobial properties of
microbial pigments have been noticed in recent years [43, 49, 53].
“Monacus” is the most widely known and used as food coloring pigment synthesized by some microorganisms. This
pigment is from Monascus sp. and can pose ranging from yellow to orange colors. Especially, in the Far East, this
pigment has been used for many years as a colorant in several foods such as wine, fish, cheese, beverages and even
sausages. Antibacterial effect of a pigment synthesized by M. purpureus was determined against S. aureus with some
studies. The antimicrobial effect of Monacus pigment varies according to type of target microorganism and pigment
[43, 49].
On the other hand, for commercial purposes, carotenoid is obtained from Dunaliella spp., Phafia rhodozyma and
Rhodotorula species. In some studies it was reported that microbial carotenoids have different inhibition effects against
food borne pathogens such as Salmonella Typhimurium S. Enteritidis, Staphlococcus aureus, Escherichia coli and
Bacillus subtilis [43, 49, 53].
2.5 Bacteriophages
Firstly, the usage of bacteriophage as a bio-control factor proposed shortly after the discovery of bacteriophage
independently by Twort (1915) and d’Herelle (1917) and suggested to be used in foods by Strauch et. al. (2007). Today,
the studies of use of bacteriophages as a bio-control factor (phage therapy) revived because of increasing antibiotic
resistances. Usually, these studies are concentrated about food safety, especially food pathogens such as E. coli
O157:H7, Campylobacter, Salmonella and Listeria causing epidemics of disease. Recently, bacteriophages described
“new” antimicrobial agents in food industry and studies carried out in order to expend the use of food [28, 32, 48].
Some researchers have two major concerns about the use of bacteriophages on food products. Consumption of these
bacteriophages with food is whether harmful or not on human health and how to overcome phage resistance of bacteria
against bacteriophages. There are some conditions to provide an effective bio-control by bacteriophages. When a phage
and a host meet, there needs to be a match between structures on both, and this confers specificity on the interaction, i.e.
any given phage will only infect a specific group of hosts. One of the remarkable factors in many food studies
inactivation is only achieved by using a high phage to host ratio (the multiplicity of infection, or MOI) with food
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A. Méndez-Vilas (Ed.)
pathogens. In addition, inactivation has been reported to occur at temperatures beneath the growth minimum of the host.
These facts suggest that the inactivation reported may be due to lyses from without, whereby large numbers of attached
phages kill the cell via the ‘death of a thousand cuts’. An example which could be explained by this is the inactivation
of Salmonella on melon which was reported to occur at 5°C and at an MOI of 200 [57, 60].
In general, studies in the literature are examined pathogens inactivation has been successfully by the use of
bacteriophages. In a study published by Atterbury et al. (2003) was achieved rate of 95-99% success C. jejuni
inactivation from chicken skin by bacteriophages. In another study has been reduced numerical of Listeria
monocytogenes by phages in infected melon and soft cheeses. Similarly, in another study, Salmonella Enteritidis were
followed after the application of phage therapy in raw and pasteurized milk and cheeses and were encounted in cheeses
made form pasteurized milk after 89 days of storage. However, the presence of Salmonella Enteritidis is still determined
in the same processed cheese made from raw milk. Similarly, in different study in order to inhibit of S. aureus in dairy
products, researchers used lytic bacteriophage cocktail isolated from raw milk. The results have shown that
bacteriophages can be use as a bio-preservative in manufacture of dairy products [52, 57, 60, 72, 74, 79].
In order to ensure food security, the first phage preparation to be used commercially contained a mixture of phages
against Listeria monocytogenes. In the Federal Register of August 18, 2006, the US Food and Drug Administration
(FDA) announced that it had approved the use of List-ShieldTM, the LMP-102 phage preparation made from six purified
phages to be used on ready-to-eat meat and poultry products as an antimicrobial agent against L. monocytogenes. The
approval of the phage preparation, developed from a company in USA, followed studies in which the effectiveness of
the phage preparation against the pathogen on food was proven and a spray application in meat and poultry processing
plants was permitted. The approved phage cocktail has antimicrobial activity against 170 strains of L. monocytogenes.
Former studies had shown that the phage cocktail is also effective on fresh fruits, like apple and melon, especially in
combination with the bacteriocin nisin. Another phage, designated P100, was developed from a Netherlands company
against L. monocytogenes and has also a potential to be widely used in the food industry. Listex P100 bacteriophage
product received also approval from the FDA for use on cheese. The approval was granted under the FDA’s GRAS
(Generally Recognized as Safe) procedure for use on cheese P100 was shown to be effective against a wide range of
Listeria strains and a bio-informatic analysis of the total genomic sequence did not reveal any similarities of P100 genes
or gene products to any genes or proteins or other factors known or believed to play a role in the pathogenicity or
virulence of L. monocytogenes [28, 32, 48, 57, 60, 79].
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