Variable Characteristics of Bacteriocin-Producing Streptococcus salivarius Strains Isolated from Malaysian Subjects

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Abstract

Background

Salivaricins are bacteriocins produced by Streptococcus salivarius, some strains of which can have significant probiotic effects. S. salivarius strains were isolated from Malaysian subjects showing variable antimicrobial activity, metabolic profile, antibiotic susceptibility and lantibiotic production.

Methodology/Principal Findings

In this study we report new S. salivarius strains isolated from Malaysian subjects with potential as probiotics. Safety assessment of these strains included their antibiotic susceptibility and metabolic profiles. Genome sequencing using Illumina’s MiSeq system was performed for both strains NU10 and YU10 and demonstrating the absence of any known streptococcal virulence determinants indicating that these strains are safe for subsequent use as probiotics. Strain NU10 was found to harbour genes encoding salivaricins A and 9 while strain YU10 was shown to harbour genes encoding salivaricins A3, G32, streptin and slnA1 lantibiotic-like protein. Strain GT2 was shown to harbour genes encoding a large non-lantibiotic bacteriocin (salivaricin-MPS). A new medium for maximum biomass production buffered with 2-(N-morpholino)ethanesulfonic acid (MES) was developed and showed better biomass accumulation compared with other commercial media. Furthermore, we extracted and purified salivaricin 9 (by strain NU10) and salivaricin G32 (by strain YU10) from S. salivarius cells grown aerobically in this medium. In addition to bacteriocin production, S. salivarius strains produced levan-sucrase which was detected by a specific ESI-LC-MS/MS method which indicates additional health benefits from the developed strains.

Conclusion

The current study established the bacteriocin, levan-sucrase production and basic safety features of S. salivarius strains isolated from healthy Malaysian subjects demonstrating their potential for use as probiotics. A new bacteriocin-production medium was developed with potential scale up application for pharmaceuticals and probiotics from S. salivarius generating different lantibiotics. This is relevant for the clinical management of oral cavity and upper respiratory tract in the human population.

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Most cited references 37

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Bacteriocins: developing innate immunity for food.

Paul D. Cotter, Colin Hill, R. Paul Ross (2005)

Bacteriocins are bacterially produced antimicrobial peptides with narrow or broad host ranges. Many bacteriocins are produced by food-grade lactic acid bacteria, a phenomenon which offers food scientists the possibility of directing or preventing the development of specific bacterial species in food. This can be particularly useful in preservation or food safety applications, but also has implications for the development of desirable flora in fermented food. In this sense, bacteriocins can be used to confer a rudimentary form of innate immunity to foodstuffs, helping processors extend their control over the food flora long after manufacture.

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Bacteriocins of gram-positive bacteria.

J R Tagg, Brian Jack, Ratna B. Ray (1995)

In recent years, a group of antibacterial proteins produced by gram-positive bacteria have attracted great interest in their potential use as food preservatives and as antibacterial agents to combat certain infections due to gram-positive pathogenic bacteria. They are ribosomally synthesized peptides of 30 to less than 60 amino acids, with a narrow to wide antibacterial spectrum against gram-positive bacteria; the antibacterial property is heat stable, and a producer strain displays a degree of specific self-protection against its own antibacterial peptide. In many respects, these proteins are quite different from the colicins and other bacteriocins produced by gram-negative bacteria, yet customarily they also are grouped as bacteriocins. Although a large number of these bacteriocins (or bacteriocin-like inhibitory substances) have been reported, only a few have been studied in detail for their mode of action, amino acid sequence, genetic characteristics, and biosynthesis mechanisms. Nevertheless, in general, they appear to be translated as inactive prepeptides containing an N-terminal leader sequence and a C-terminal propeptide component. During posttranslational modifications, the leader peptide is removed. In addition, depending on the particular type, some amino acids in the propeptide components may undergo either dehydration and thioether ring formation to produce lanthionine and beta-methyl lanthionine (as in lantibiotics) or thio ester ring formation to form cystine (as in thiolbiotics). Some of these steps, as well as the translocation of the molecules through the cytoplasmic membrane and producer self-protection against the homologous bacteriocin, are mediated through specific proteins (enzymes). Limited genetic studies have shown that the structural gene for such a bacteriocin and the genes encoding proteins associated with immunity, translocation, and processing are present in a cluster in either a plasmid, the chromosome, or a transposon. Following posttranslational modification and depending on the pH, the molecules may either be released into the environment or remain bound to the cell wall. The antibacterial action against a sensitive cell of a gram-positive strain is produced principally by destabilization of membrane functions. Under certain conditions, gram-negative bacterial cells can also be sensitive to some of these molecules. By application of site-specific mutagenesis, bacteriocin variants which may differ in their antimicrobial spectrum and physicochemical characteristics can be produced. Research activity in this field has grown remarkably but sometimes with an undisciplined regard for conformity in the definition, naming, and categorization of these molecules and their genetic effectors. Some suggestions for improved standardization of nomenclature are offered.

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Bacteriocins: modes of action and potentials in food preservation and control of food poisoning.

Tjakko Abee, Lothar Krockel, Colin Hill (1995)

Lactic acid bacteria (LAB) play an essential role in the majority of food fermentations, and a wide variety of strains are routinely employed as starter cultures in the manufacture of dairy, meat, vegetable and bakery products. One of the most important contributions of these microorganisms is the extended shelf life of the fermented product by comparison to that of the raw substrate. Growth of spoilage and pathogenic bacteria in these foods is inhibited due to competition for nutrients and the presence of starter-derived inhibitors such as lactic acid, hydrogen peroxide and bacteriocins (Ray and Daeschel, 1992). Bacteriocins, are a heterogenous group of anti-bacterial proteins that vary in spectrum of activity, mode of action, molecular weight, genetic origin and biochemical properties. Currently, artificial chemical preservatives are employed to limit the number of microorganisms capable of growing within foods, but increasing consumer awareness of potential health risks associated with some of these substances has led researchers to examine the possibility of using bacteriocins produced by LAB as biopreservatives. The major classes of bacteriocins produced by LAB include: (I) lantibiotics, (II) small heat stable peptides, (III) large heat labile proteins, and (IV) complex proteins whose activity requires the association of carbohydrate or lipid moieties (Klaenhammer, 1993). Significantly however, the inhibitory activity of these substances is confined to Gram-positive bacteria and inhibition of Gram-negatives by these bacteriocins has not been demonstrated, an observation which can be explained by a detailed analysis and comparison of the composition of Gram-positive and Gram-negative bacterial cell walls (Fig. 1). In both types the cytoplasmic membrane which forms the border between the cytoplasm and the external environment, is surrounded by a layer of peptidoglycan which is significantly thinner in Gram-negative bacteria than in Gram-positive bacteria. Gram-negative bacteria possess an additional layer, the so-called outer membrane which is composed of phospholipids, proteins and lipopolysaccharides (LPS), and this membrane is impermeable to most molecules. Nevertheless, the presence of porins in this layer will allow the free diffusion of molecules with a molecular mass below 600 Da. The smallest bacteriocins produced by lactic acid bacteria are approximately 3 kDa and are thus too large to reach their target, the cytoplasmic membrane (Klaenhammer, 1993; Stiles and Hastings, 1991). However, Stevens et al. (1991) and Ray (1993) have demonstrated that Salmonella species and other Gram-negative bacteria become sensitive to nisin after exposure to treatments that change the permeability barrier properties of the outer membrane (see below). This review will focus on the mode of action of lantibiotics (class I) and class II LAB bacteriocins and their potentials in food preservation and control of food poisoning.

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Author and article information

Contributors

Paul D. Cotter: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2014

Publication date (Electronic): 18 June 2014

Volume: 9

Issue: 6

Electronic Location Identifier: e100541

Affiliations

[1]Institute of Biological Sciences, Microbiology Division, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia

Teagasc Food Research Centre, Ireland

Author notes

* E-mail: kphil@ 123456um.edu.my

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: AB KP. Performed the experiments: AB KP. Analyzed the data: AB KP. Contributed reagents/materials/analysis tools: KP. Wrote the paper: AB KP.

Article

Publisher ID: PONE-D-14-03627

DOI: 10.1371/journal.pone.0100541

PMC ID: 4062538

PubMed ID: 24941127

SO-VID: 62aa9a45-59cc-46b7-9f97-50b3c9eee711

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 27 January 2014

Date accepted : 28 May 2014

Page count

Pages: 16

Funding

The authors wish to acknowledge the support by way of facilities from University of Malaya and the High Impact Research – Malaysian Ministry of Higher Education grant designated as UM.C/625/1/HIR/MOHE/SC/08 with account F000008-21001 under the Principal Investigator Koshy Philip for the study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Variable Characteristics of Bacteriocin-Producing Streptococcus salivarius Strains Isolated from Malaysian Subjects

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Abstract

Background

Methodology/Principal Findings

Conclusion

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Malaysian Management Journal

Most cited references 37

Bacteriocins: developing innate immunity for food.

Bacteriocins of gram-positive bacteria.

Bacteriocins: modes of action and potentials in food preservation and control of food poisoning.

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