Bacteriocins Lactobacillus — an alternative to antimicrobial drugs

✅ 全文

乳酸菌细菌素——抗菌药物的替代品

作者 I. M. Voloshyna; K. I. Soloshenko; V. Krasinko; Іnna Lych; Л. В. Шкотова 期刊 Biopolymers and Cell 发表日期 2021 ISSN 0233-7657 DOI 10.7124/bc.000a4e 类型 原创研究 (Original Research)

📄 英文摘要 English Abstract

EN

The review presents the characteristics of bacteria of the Lactobacillus family and their abi lity to synthesize various bacteriocins. The classification of bacteriocins of lactobacilli is given, which includes three classes: class I -lantibiotics (peptides with a molecular weight of less than 5 kDa, which contain lanthionine), class II -unmodified bacteriocins, also called nonlantibiotics (heat-resistant peptides , which do not contain lanthionine and have a molecular weight less than 10 kDa), and class III -a poorly studied group of thermolabile proteins with a molecular weight of more than 30 kDa. Lactobacilli are shown to synthesize a wide spectrum of bacteriocins, which demonstrate a variety of actions and are able to inhibit the growth of numerous species of opportunistic gram-positive microflora. The article also provides the examples of bacteriocins produced by Lactobacillus isolated from food products (fermented meat, fish, kombucha, goat milk, koumiss, etc.) and various human biotopes (microbiota of breast milk, intestinal tract and vaginal secretions). Additionally, the review shows the prospects of wide application of bacteriocins synthesized by Lactobacillus in the food and pharmaceutical industries.

📄 中文摘要 Chinese Abstract

中文
目前医药市场上存在多种药物,但由于各种外源性和内源性因素对人体主要系统的正常功能产生负面影响,疾病发病率呈上升趋势。首先,不利的环境因素、不均衡的营养、维生素和微量元素的缺乏、压力性情境的增加以及化学治疗药物和抗生素的大规模无控制使用,均构成了重要影响。上述因素的共同作用导致病原微生物对抗生素产生耐药性,因此有必要开发新型有效的抗菌药物。当前寻找具有抗菌活性药物的一个现代趋势是利用细菌素。细菌素是由细菌核糖体合成的肽或蛋白质,对通常与产生菌株密切相关的其他细菌具有抗菌活性。细菌素由多种微生物合成,已在医学、兽医学和食品技术中作为治疗剂以及食品防腐剂得到广泛应用,用于对抗各种感染性和食源性病原体。某些抗生素对人体健康具有有害的副作用,而细菌素不具有或仅具有很小的细胞毒性,这主要是因为所测试的细菌素由乳酸菌产生。乳酸菌长期以来在发酵和乳制品生产中作为生物防腐剂使用,同时也是健康人体消化道中正常菌群过度定植的因素之一。

📋 英文结构化总结 English Structured Summary

全文整理

EN

Background:

There are many different medicines on the pharmaceutical market, but the trend towards an increase of morbidity is observed due to the influence of various exo- and endogenous factors that negatively affect the normal functioning of the main systems of human body. First of all, this is the influence of unfavorable environmental factors, unbalanced nutrition, deficiency of vitamins and microelements, increased number of stressful situations, as well as the massive uncontrolled use of chemotherapeutic drugs and antibiotics. As a result, the combination of factors listed above leads to the resistance of pathogenic microorganisms to antibiotics, which causes necessity of the development of new effective antimicrobial drugs. One of the modern trends in the search for medicines with antimicrobial activity is the use of bacteriocins. Bacteriocins are ribosomally synthesized peptides or proteins produced by bacteria. These compounds have antibacterial activity against other bacteria, which are usually closely associated with the producent strain. Bacteriocins are synthesized by various microorganisms and have already found wide application in medicine, veterinary medicine and food technologies as a therapeutic agent, as well as a food preservative to combat various infectious and food pathogens. Some antibiotics have harmful side effects on human health whereas bacteriocins do not have any or have little cytotoxicity. It is mainly because the tested bacteriocins were produced by the lactic acid bacteria. The latter have been used in fermentation and milk production as bio-preservatives for a long time, and are also one of the factors of hypercolonization of the digestive tract of a healthy person with a normal microbiota.

Methods:

N/A - Review article

Results:

The review presents the characteristics of bacteria of the Lactobacillus family and their ability to synthesize various bacteriocins. The classification of bacteriocins of lactobacilli is given, which includes three classes: class I — lantibiotics (peptides with a molecular weight of less than 5 kDa, which contain lanthionine), class II — unmodified bacteriocins, also called non-lantibiotics (heat-resistant peptides, which do not contain lanthionine and have a molecular weight less than 10 kDa), and class III — a poorly studied group of thermolabile proteins with a molecular weight of more than 30 kDa. Lactobacilli are shown to synthesize a wide spectrum of bacteriocins, which demonstrate a variety of actions and are able to inhibit the growth of numerous species of opportunistic gram-positive microflora. The article also provides the examples of bacteriocins produced by Lactobacillus isolated from food products (fermented meat, fish, kombucha, goat milk, koumiss, etc.) and various human biotopes (microbiota of breast milk, intestinal tract and vaginal secretions). Lactobacilli possess a diverse spectrum of biological activities, for example, they help to stimulate the secretion of gastric juice and enzymes necessary for enhancement of digestion processes, they are able to reduce the side effects of antibiotics, help to split bile salts and normalize lipid metabolism, protect epithelial cells from damage, enhance the regeneration of the intestinal mucosa, and mitigate inflammatory processes by normalizing the general composition of microflora.

Data Summary:

Bacteriocins of lactobacilli are classified into three classes: class I lantibiotics (molecular weight <5 kDa, contain lanthionine), class II unmodified bacteriocins (molecular weight <10 kDa, no lanthionine), and class III thermolabile proteins (molecular weight >30 kDa). The genus Lactobacillus is phylogenetically divided into seven groups based on 16S rRNA sequence: Lactobacillus buchneri, Lactobacillus casei, Lactobacillus delbrueckii, Lactobacillus plantarum, Lactobacillus reuteri, Lactobacillus sakei, and Lactobacillus salivarius. Traditionally, depending on fermentation pathways, lactobacilli are divided into three groups: obligate homofermentative, facultative heterofermentative, and obligate heterofermentative bacteria. Most lactic acid bacteria synthesize bacteriocins that are thermostable substances with a high molecular weight (up to 10–30 kDa), and their biosynthesis is encoded by special plasmids.

Conclusions:

Bacteriocins do not have any or have little cytotoxicity, mainly because they are produced by lactic acid bacteria which have been used in fermentation and as bio-preservatives. The beneficial properties of bacteriocins allow using them to replace antibiotics or stimulate their action as well as to reduce the spawn rate of antibiotic-resistant strains. Friendly bacteria of the human microbiota can be mobilized to produce bacteriocins and prevent bacterial infection on the outer surface of the human epithelium of the gastrointestinal tract. Additionally, the review shows the prospects of wide application of bacteriocins synthesized by Lactobacillus in the food and pharmaceutical industries.

Practical Significance:

Bacteriocins have already found wide application in medicine, veterinary medicine and food technologies as a therapeutic agent, as well as a food preservative to combat various infectious and food pathogens. The review shows the prospects of wide application of bacteriocins synthesized by Lactobacillus in the food and pharmaceutical industries.

📋 中文结构化总结 Chinese Structured Summary

中文

背景:

目前医药市场上存在多种药物,但由于各种外源性和内源性因素对人体主要系统的正常功能产生负面影响,疾病发病率呈上升趋势。首先,不利的环境因素、不均衡的营养、维生素和微量元素的缺乏、压力性情境的增加以及化学治疗药物和抗生素的大规模无控制使用,均构成了重要影响。上述因素的共同作用导致病原微生物对抗生素产生耐药性,因此有必要开发新型有效的抗菌药物。当前寻找具有抗菌活性药物的一个现代趋势是利用细菌素。细菌素是由细菌核糖体合成的肽或蛋白质,对通常与产生菌株密切相关的其他细菌具有抗菌活性。细菌素由多种微生物合成,已在医学、兽医学和食品技术中作为治疗剂以及食品防腐剂得到广泛应用,用于对抗各种感染性和食源性病原体。某些抗生素对人体健康具有有害的副作用,而细菌素不具有或仅具有很小的细胞毒性,这主要是因为所测试的细菌素由乳酸菌产生。乳酸菌长期以来在发酵和乳制品生产中作为生物防腐剂使用,同时也是健康人体消化道中正常菌群过度定植的因素之一。

方法:

不适用——综述类文章

结果:

本综述介绍了乳杆菌科细菌的特性及其合成多种细菌素的能力。文中给出了乳杆菌细菌素的分类,包括三个类别:I类——羊毛硫抗生素(分子量小于5 kDa、含羊毛硫氨酸的肽);II类——未修饰细菌素,也称为非羊毛硫抗生素(耐热肽,不含羊毛硫氨酸,分子量小于10 kDa);III类——研究较少的热不稳定蛋白质(分子量大于30 kDa)。研究表明,乳杆菌可合成多种细菌素,表现出多样的活性,能够抑制多种机会性革兰氏阳性菌的生长。文中还列举了从食品(发酵肉制品、鱼类、康普茶、山羊奶、马奶酒等)和人体不同生物位点(母乳微生物群、肠道和阴道分泌物)中分离的乳杆菌所产生的细菌素的实例。乳杆菌具有多种生物活性,例如有助于刺激胃液和消化酶的分泌以促进消化过程,能够减轻抗生素的副作用、帮助分解胆汁盐并正常化脂质代谢、保护上皮细胞免受损伤、增强肠道黏膜的再生,并通过正常化菌群总体组成来减轻炎症过程。

数据概要:

乳杆菌细菌素分为三类:I类羊毛硫抗生素(分子量<5 kDa,含羊毛硫氨酸)、II类未修饰细菌素(分子量<10 kDa,不含羊毛硫氨酸)和III类热不稳定蛋白质(分子量>30 kDa)。乳杆菌属根据16S rRNA序列在系统发育上分为七个组:布氏乳杆菌组、干酪乳杆菌组、德氏乳杆菌组、植物乳杆菌组、罗伊氏乳杆菌组、清酒乳杆菌组和唾液乳杆菌组。传统上,根据发酵途径,乳杆菌分为三类:专性同型发酵、兼性异型发酵和专性异型发酵细菌。大多数乳酸菌合成的细菌素是热稳定的高分子量物质(高达10–30 kDa),其生物合成由特殊质粒编码。

结论:

细菌素不具有或仅具有很小的细胞毒性,这主要是因为它们由乳酸菌产生,而乳酸菌长期以来被用于发酵和作为生物防腐剂。细菌素的优良特性使其可用于替代抗生素或增强抗生素的作用,并降低抗生素耐药菌株的产生率。人体微生物群中的有益菌可被动员产生细菌素,从而预防胃肠道上皮外表层上的细菌感染。此外,本综述展示了乳杆菌合成的细菌素在食品和制药工业中广泛应用的良好前景。

实践意义:

细菌素已在医学、兽医学和食品技术中作为治疗剂和食品防腐剂得到广泛应用,用于对抗各种感染性和食源性病原体。本综述展示了乳杆菌合成的细菌素在食品和制药工业中广泛应用的良好前景。

📖 英文全文 English Full Text

EN

Reviews

ISSN 1993-6842 (on-line); ISSN 0233-7657 (print) Biopolymers and Cell. 2021. Vol. 37. N 2. P 85–97 doi: http://dx.doi.org/10.7124/bc.000A4E UDC 606.61:579.864: [579.2/6+612.392.98]

Bacteriocins Lactobacillus — an alternative to antimicrobial drugs I. M. Voloshyna1,2, K. I. Soloshenko2, V. O. Krasinko2, I. V. Lych2, L. V. Shkotova3 1 Kyiv National University of Technologies and Design

2, Nemirovich-Danchenko Str., Kyiv, Ukraine, 01011 2 National University of Food Technologies 68, Volodymyrska Str., Kyiv, Ukraine, 01601 3 Institute of Molecular Biology and Genetics, NAS of Ukraine

150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03143 i_woloschina@yahoo.com

The review presents the characteristics of bacteria of the Lactobacillus family and their abi­li­ ty to synthesize various bacteriocins. The classification of bacteriocins of lactobacilli is given, which includes three classes: class I — lantibiotics (peptides with a molecular weight of less than 5 kDa, which contain lanthionine), class II — unmodified bacteriocins, also called nonlantibiotics (heat-resistant peptides , which do not contain lanthionine and have a molecular weight less than 10 kDa), and class III — a poorly studied group of thermolabile proteins with a molecular weight of more than 30 kDa. Lactobacilli are shown to synthesize a wide spectrum of bacteriocins, which demonstrate a variety of actions and are able to inhibit the growth of numerous species of opportunistic gram-positive microflora. The article also provides the examples of bacteriocins produced by Lactobacillus isolated from food products (fermented meat, fish, kombucha, goat milk, koumiss, etc.) and various human biotopes (microbiota of breast milk, intestinal tract and vaginal secretions). Additionally, the review shows the prospects of wide application of bacteriocins synthesized by Lactobacillus in the food and pharmaceutical industries. K e y w o r d s: bacteriocins, Lactobacillus, lactococci, lactic acid bacteria, probiotics.

Introduction There are many different medicines on the pharmaceutical market, but the trend towards an increase of morbidity is observed due to the influence of various exo- and endogenous factors that negatively affect the normal functio­

ning of the main systems of human body. First of all, this is the influence of unfavorable environmental factors, unbalanced nutrition, deficiency of vitamins and microelements, increased number of stressful situations, as well

© 2021 I. M. Voloshyna et al.; Published by the Institute of Molecular Biology and Genetics, NAS of Ukraine on behalf of Biopolymers and Cell. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited

I. M. Voloshyna, K. I. Soloshenko, V. O. Krasinko 85 I. M. Voloshyna, K. I. Soloshenko, V. O. Krasinko et al.

as the massive uncontrolled use of chemotherapeutic drugs and antibiotics. As a result, the combination of factors listed above leads to the resistance of pathogenic microorganisms to antibiotics, which causes necessity of the development of new effective antimicrobial drugs. One of the modern trends in the search for medicines with antimicrobial activity is the use of bacteriocins [1, 42]. Bacteriocins are ribosomally synthesized peptides or proteins produced by bacteria. These compounds have antibacterial activity against other bacteria, which are usually closely associated with the producent strain [17]. Bacteriocins are synthesized by various microorganisms and have already found wide application in medicine, veterinary medicine and food technologies as a therapeutic agent, as well as a food preservative to combat various infectious and food pathogens. Some antibiotics have harmful side effects on human health whereas bacteriocins do not have any or have little cytotoxicity [1, 9, 17]. It is mainly because the tested bacteriocins were produced by the lactic acid bacteria. The latter have been used in fermentation and milk production as bio-preservatives for a long time, and are also one of the factors of hypercolonization of the digestive tract of a healthy person with a normal microbiota. The beneficial properties of bacteriocins allow using them to replace antibiotics or stimulate their action as well as to reduce the spawn rate of antibiotic-resistant strains. Friendly bacteria of the human microbiota can be mobilized to produce bacteriocins and prevent bacterial infection on the outer surface of the human epithelium of the gastrointestinal tract (GIT) [9, 17, 36]. 86

Characteristics of Lactobacillus Lactic acid bacteria (LAB) are a diverse and extremely valuable group of microorganisms, which, without adhering to a strict taxonomic classification, are united on the basis of their general properties including a common feature: the ability to synthesize lactic acid (LA) as the main or single fermentation product [42]. Bacteria of the Lactobacillus genus are localized in almost all biotopes of the digestive tract and therefore they are referred to as the main human microbiota [8, 45]. The genus Lacto­bacillus has several hundred species. Based on the analysis of the 16S rRNA sequence, lactobacilli are phylogenetically divided into seven groups: Lactobacillus buchneri (bu), Lacto­bacillus casei (ca), Lacto­bacil­ lus delbrueckii (de), Lactobacillus plantarum (pl), Lactobacillus reuteri (re), Lacto­ bacillus sakei (sa) and Lactobacillus sa­li­va­rius (sl). Traditionally, depending on the ways of fermentation of carbohydrates, bacteria of the Lactobacillus genus are divided into three groups: (1) obligate homofermentative; (2) facultative heterofermentative; and (3) obligate heterofermentative bacteria [7]. Lactobacillus are gram-positive non-sporeforming bacteria, obligate or facultative anaerobes with high enzymatic activity, which are incredibly diverse in shape and size. They can be in the form from short to long filamentous rods, arranged singly, in pairs or in short chains. During their normal metabolism lactobacilli are capable of forming lactic acid, hydrogen peroxide, producing lysozyme and substances with antibiotic activity such as reuterin, plantaricin, lactocidin, lactolin [19]. Heterofermentative Lactobacillus species can also produce lactic, acetic, butyric, and a num- Bacteriocins Lactobacillus — an alternative to antimicrobial drugs

ber of other acids, as well as carbon dioxide [33, 36]. Lactobacilli possess a diverse spectrum of biological activities, for example, they help to stimulate the secretion of gastric juice and enzymes necessary for enhancement of digestion processes they are able to reduce the side effects of antibiotics, help to split bile salts and normalize lipid metabolism. Other important characteristics are the abilities to protect epithelial cells from damage, to enhance the regeneration of the intestinal mucosa, and to mitigate inflammatory processes by norma­lizing the general composition of microflora [22, 24]. Most of the lactic acid bacteria are able to synthesize antibiotic substances of proteinpeptide nature, which eliminate or retard the growth of related bacteria species and/or strains; additionally, they have a wide spectrum of antibacterial activity and therefore are called bacteriocins. Basically, bacteriocins are thermostable substances with a high molecular weight (up to 10–30 kDa). Their biosynthesis is encoded by special plasmids and occurs on ribosomes [13, 25]. It is of importance to discuss the classification and properties of lactobacilli bacteriocins in more detail.

Classification of bacteriocins Bacteriocins are conventionally divided into three classes: class I — lantibiotics, class II — unmodified bacteriocins, which are also called non-lantibiotics [12, 25, 27], and class III, which includes a group of thermolabile proteins with a molecular weight of more than 30 kDa [38]. Bacteriocins of class I are peptides with a molecular weight of less than 5 kDa, which

contain lanthionine. They include such amino acids as lanthionine (Lan), α-methylanthionine (MeLan), dehydroalanine and dehydrobuty­ rine. According to the chemical structure and antimicrobial properties, this class is divided into the types A and B lantibiotics [10, 25]. The type A lantibiotics are small cationic peptides, which exhibit antibacterial activity by forming pores in bacterial membranes. The representatives of type B are small anionic or neutral globular peptides, the antimicrobial properties of which are manifested by inhibiting specific enzymes. Bacteriocins of class II are heat-resistant peptides, which do not contain lanthionine and have a molecular weight less than 10 kDa [5, 10, 25]. The representatives of this group exhibit antimicrobial activity against Listeria genus; they are capable of destroying the integrity of the microbial membrane, which leads to ionic imbalance and loss of organic phosphorus in target cells. The representatives of this class are divided into four subgroups. Class IIa includes pediocin-shaped bacteriocins, they contain the N-terminal sequence Tyr-Gly-Asn-Gly-Val-Xaa-Cys (TGAGV). Class IIb consists of two-peptide bacteriocins, the activity of which depends on two different peptides. These two peptides can show their activity independently of each other, but exhibit synergism when they function together. Class IIc includes cyclic bacteriocins and class ІІd — unmodified linear non-pediocineshaped bacteriocins [5, 10, 25]. Bacteriocins of class III include a group of thermolabile proteins with a molecular weight more than 30 kDa. Unfortunately, their properties have not yet been studied enough [25, 38, 39]. 87

I. M. Voloshyna, K. I. Soloshenko, V. O. Krasinko et al.

Variety of bacteriocins produced by Lactobacillus Lactobacilli synthesize a wide spectrum of bacteriocins. These substances have a variety of actions and inhibit the growth of numerous species of opportunistic gram-positive microflora, for example, Listeria monocytogenes, Clostridium butyricum, Clostridium sporogenes, Staphylococcus aureus, Enterococcus faecalis, Bacillus spp. and others. The synthesis of active bacteriocins is one of the factors that provide high colonization properties and play a regulatory role of lactobacilli in maintaining the physiological microbial balance in biocenoses [13]. Most of the bacteriocins are small molecules with amphiphilic properties and high isoelectric points. The producent cells are resistant to the bacteriocins they produce due to the synthesis of specific immunity proteins [11, 21]. Currently, an active research is underway on the mechanisms of the antimicrobial action of bacteriocins. It was found that lactobacilli bacteriocins contain the protein components, which are fixed on specific cellular receptors of target cells and disrupt the transport of various cations through the cell membrane of microorganisms. The most studied bacteriocins of Lactobacillus are amilovorin 471 (L. amylovorus 471119), acidocin B (L. acidophilus), bavaricin MN (L. bavaricus MN), caseicin (L. casei), curvacin FS47 and A (L. curvatus FS47 and L. curvatus LTH1174), lactocin S (L. sake L 45), plantaricin A and C (L. plantarum), plantacin 154 (L. plantarum LTF154), sakacin 674 (L. sake Lb674), etc. [11]. The literature contains also information about new bacteriocins of Lactobacillus, such as salivaricin mmaye1 (L. salivarius), BacF1 and 88

BacF2 (L. plantarum subsp. argentoratensis SJ33) [1, 44].

Bacteriocins of Lactobacillus, isolated from food Due to the unique properties, bacteriocins are widely utilized in the food industry. They are used as preservatives in partially purified or purified concentrated form. Until recently, such bacteriocins as nisin and pediocin PA-1 were licensed as food preservatives [41]. Note­ worthy, the use of bacteriocins reduces the cost of production and preservation of foodstuffs retaining their nutritional and biological value. Lactic acid bacteria (LAB) are important in the technologies of fermented food production, where their role is to prevent the growth of pathogenic microorganisms and spoilage in general. It is due to acidifying the environment and active synthesis of antimicrobial compounds, which contributes not only to quality improvement, but also to safety advancement [3]. Lactic acid bacteria, especially Lactobacillus sakei and Lactobacillus curvatus, are a part of the microbiota of many fermented meat pro­ ducts. These species are well adapted to the meat environment, providing an improved flavor and accelerated maturation of the fermented meat products [15, 26]. Bacteriocins produced by the lactic acid bacteria are well known for their activity against Listeria monocytogenes, a common gram-positive pathogen which caused several outbreaks of foodborne disease in recent decades. In one of the classifications of bacteriocins there is a special class, which includes bacteriocins with the activity against Listeria [21]. The control of L. monocytogenes in food is a major challenge due to its ability to survive

Bacteriocins Lactobacillus — an alternative to antimicrobial drugs at low pH values, increased salt concentration and the presence of nitrites, which are harmful to most other pathogenic microorganisms in the production of dry fermented food. Because of this, the bacteriocinogenic lactic acid bacteria and their bacteriocins are helpful as preservatives in fermented food products and can be used as technological alternatives to che­ mical preservatives, satisfying the demand for foods with fewer or no additives [15]. In recent years, the demand for “natural” products has increased, because consumers prefer them over foods with chemical preservatives. The critical issues connected with natural products are how to maintain their safety and quality, and how to extend their shelf life. In this regard, great attention is paid to the use of the antagonistic characteristics of lactobacilli. It was shown that Lactobacillus plantarum SLG10, isolated from kombucha (a traditional fermented drink in South China), produced bacteriocin SLG10, which had antibacterial activity against both gram-positive and gram-negative bacteria, including multidrugresistant strains. Bacteriocin SLG10 was characterized by thermal stability, pH tolerance, and was sensitive to most proteases, but not to trypsin or pepsin. The study of the antibacterial mechanism showed that bacteriocin SLG10 increases the permeability of the cell membrane, inducing the release of potassium ions, and can inhibit the formation of biofilms [30]. Recently, a large number of antibiotic-resistant bacteria have been found in dairy products, for example, Salmonella enterica in dry milk nutrition, Staphylococcus aureus in raw and pasteurized milk and in ice cream and vancomycin-resistant Enterococcus faecium in cheeses [15, 31]. There is information in the

literature that some bacteriocins produced by lactic acid bacteria can inhibit foodborne multidrug-resistant pathogens, which favorably distinguishes them from other registered bacteriocins with a rather narrow inhibitory spectrum [24, 26]. Researchers pay great attention to studying the characteristics of the production of natural preservatives by lactic acid bacteria. Thus, it was shown that the biosynthesis of bacteriocins by L. curvatus MBSa2 and MBSa3 on the MRS medium begins in the early exponential growth phase (4 h of cultivation). Under the cultivation conditions at 37 °C, after 12 h the amount of produced bacteriocins began to decrease in both strains. Maximum accumulation of MBSa2 bacteriocin (12800 U/ml) was observed after 8-hour cultivation at 25 °C and 37 °C and 6-hour cultivation at 30 °C. This indicates the primary kinetics of the metabolite, which is also observed for other bacteriocins, such as sakacin K (producent L. sakei CTC 494), sakacin P (L. sakei CCUG 42687), curvacin A (L. curvatus LTH 1174), curvaticin L442 (L. curvatus L422) [2, 4]. The Literature data point out that many bacteriocins are thermostable, because they retain their properties after heat treatment (100–120 °C, 15 min) [4, 44, 46]. This indicates that they can be used in the heat-treated foods without a decrease in their preservative action. Usually the low molecular weight bacteriocins are thermostable because they are small polypeptides. These properties have been described for bacteriocins MBSa2 and MBSa3 (L. curvatus), sakacin M and P (L. sakei), pediocin L50 (Pediococcus pentosaceus), aci­ docin D20079 (L. acidophilus), plantaricin LP31 (L. plantarum) [4]. 89

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In view of the unique properties and expanding prospects for the use of bacteriocins of lactic acid bacteria in food technologies, researchers are active in search for and isolation of producents of these biologically active compounds from traditional food products and raw materials. Thus, the Lactobacillus crustorum strain isolated from koumiss (Xinjiang, China) can produce bacteriocin MN047 A [46]. Koumiss is a traditional fermented mare’s milk, popular in the Central Asian steppes, including China, Mongolia, Kazakhstan, Kyrgyzstan and some regions of Russia. For centuries, koumiss was considered not only a drink, but also a functional food product for medical purposes, such as improving function of kidneys, gastrointestinal tract, nervous system and immune system, and treatment of hepatitis, chronic ulcers, tuberculosis, etc. [46]. Koumiss is usually obtained from mare’s milk by fermenting its own natural microbiota, including lactic acid bacteria and yeast. Various strains of Lactobacillus, including L. casei, L. plantarum, L. fermentum, L. helveticus and L. acidophilus, have been found in koumiss but only bacteriocin produced by L. plantarum has been purified and characterized [26, 35, 42, 45]. More and more researchers are engaged in a comprehensive study of the properties of isolated bacteriocins. Thus, bacteriocin LF‑BZ532 synthesized by Lactobacillus fermentum BZ532 appears to be promising for further practical use. This strain was isolated from a Chinese fermented grain drink (bozai) and identified by 16s rRNA sequencing. Bacteriocin LF-BZ532 has a molecular weight of 1105.563 Da [32]. It was found that this bacteriocin possesses a wide spectrum of an90

timicrobial activity against gram-positive and gram-negative bacteria, including Listeria and Pseudomonas. The unique properties of the described bacteriocin are its significant thermal stability with a residual activity of 88.19 % and 56.98 % at 100 and 121 °C (30, 20 min) respectively. Additionally, it is stable over a wide pH range (2–8), but it is highly sensitive to the action of proteolytic (proteinase K, pepsin, and trypsin) enzymes, which indicates its peptide nature. Based on the foregoing, it is assumed that purified LF-BZ532 and its producing strain L. fermentum BZ532 are promising candidates for use as a bioconservative in the food industry [32]. The Lactobacillus sakei GM3 strain isolated from goat milk exhibited resistance to acid and bile and showed antagonistic activity against foodborne pathogens. The Bacteriocin production observed in L. sakei GM3 reached its maximum in the stationary phase, after 18 hours of cultivation [2, 3]. The study of the properties of bacteriocin GM3 showed that it remains active in a wide pH and temperature ranges, it is resistant to organic solvent. At the same time, bacteriocin GM3 is sensitive to some proteolytic enzymes. It was found that the molecular weight of bacteriocin is 4.8 kDa. The study of cytotoxicity in the model of HT29 cells showed the maximum inhibition of survival (45.60 ± 0.5 %) at a bacteriocin concentration of 2240 U/ml. These results indicate that the L. sakei GM3 has potential for use in the food industry as a biopreservative [2]. Bacteriocin DY4-2, synthesized by the strain Lactobacillus plantarum DY4-2, which was isolated from saber fish (Trichiurus lepturus) is quite interesting. This bacteriocin is maximally synthesized in the stationary phase

Bacteriocins Lactobacillus — an alternative to antimicrobial drugs after 24 h of incubation. The molecular weight of bacteriocin DY4-2 was determined to be 1465 Da. Bacteriocin DY4-2 was characterized by significant thermal stability (30 min at 121 °C) preserving activity in the pH range 2.5–5.5, but was sensitive to the proteolytic enzymes. This bacteriocin exhibited a wide spectrum of antimicrobial activity against fish pathogenic bacteria, such as Pseudomonas fluorescens, P. aeruginosa, Vibrio parahaemolyticus, Aeromonas sobria, and Listeria monocytogenes [28, 30]. The addition of partially purified bacteriocin DY4-2 to halibut fillets reduced the number of P. fluorescens cells by 2.7 log units at 4 °C for 12 days. If compared with the control, the samples treated with bacteriocin DY4-2 showed a significant decrease in the total number of viable microorganisms. The results of these studies demonstrated that bacteriocin DY4-2 possesses the potential to act as a bio-preservative for seafood [28]. Highly appreciating the prospects of biotechnological production of bacteriocins, researchers select the substrates for the most cost-effective biosynthesis. Thus, whey, the main by-product obtained after curdling and removing casein in cheese production, is a large-scale waste in the dairy industry [6, 42]. When whey is discharged into water, it weakly biodegradates but the level of dissolved oxygen reduces, which negatively affects the normal natural processes of self-cleaning of water objects and creates a real risk to the life of aquatic inhabitants. The practice of uncontrolled discharge of wastewater containing whey leads to many environmental problems: severe environmental pollution affecting the physicochemical characteristics of the soil,

which in turn results in a decreased yield. Thus, the search for the cheap methods of whey utilization remains relevant [6, 25]. Because whey makes up about 55 % of all milk nutrients, an economical and profitable alternative is to use it as a substrate for the production of biologically active substances. The most common whey nutrients are lactose (75 %), soluble proteins (12 ... 14 %), lipids and mineral salts (1 ... 10 %). They are necessary for the growth of microorganisms, especially for lactic acid bacteria, which are widely used in the food industry [6]. Although bacteriocins can be produced by numerous microorganisms, those produced by lactic acid bacteria are attracting increased attention because they are considered the most “safe” [3]. L. plantarum species can adapt to various niches due to its ability to ferment a wide range of carbohydrates [35]. In particular, the L. plantarum ST16Pa strain can actively grow on the whey based medium and produce a peptide with a molecular weight of 6.5 kDa, exhibiting antimicrobial activity against many different food pathogenic bacteria, including gram-negative bacteria [35]. Although whey can support the growth of most lactic acid bacteria, it lacks nitrogen and other nutrients; therefore the exogenous addition of the latter is required for the successful biosynthesis of bacteriocins. Thus, the researchers demonstrated the ability of the L. plantarum ST16 strain cultivated on MRS medium to synthesize bacteriocins with high antimicrobial activity against several microorganisms. However this strain cultivated on cheese whey does not produce bacteriocin despite the accumulation of biomass [35]. 91

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Lactobacillus bacteriocins isolated from human The normal microbiota of human body plays a significant role in human health. The exceptional function of human symbiotic microorganisms in protection against pathogens, maintenance of stable immunity, and biosynthesis of vital compounds such as vitamins, organic acids, amino acids, etc. has been proven [18, 40]. Lactobacillus bacteria are typical inhabitants of the digestive tract of humans and animals [40, 42]. Microorganisms of normal human microbiota are one of the safest sources of bacteriocins. These bacteriocins are involved in the mechanisms of antagonistic activity inside the human body, and are also used to maintain its microbiota in a state of dynamic equilibrium. The ability to produce bacteriocins is an important characteristic of probiotic strains. According to the requirements of FAO / WHO (2002), probiotic bacteria should have a high ability to survive in the gastrointestinal tract and adhere to intestinal epithelial cells, and, most importantly, should be safe strains for humans and animals [18, 20, 42]. Because lactobacilli are considered safe probiotic microorganisms, they are widely used in the food industry to obtain various products (vegetables, meat, dairy, etc.). Therefore, the resear­ ches devoted to the search, isolation and study of lactobacilli bacteriocins from the human body appear in the scientific literature more and more often. Thus, the results of research have been published in which Lactobacillus bacteriocins were isolated from breast milk. Sixty breast milk samples were collected from volunteer mothers aged 19 to 35 from rural areas of 92

Lorestan and Markazi provinces, Iran. [29]. The isolates were identified using a PCR pri­ mer specific for Lactobacillus and it was shown that eighteen out of thirty-three isolates were the Lactobacillus strains. Lactobacillus reuteri and L. gasseri were identified among these isolates, which survived at low pH values​​ and in the presence of bile salts. It was also shown that all Lactobacillus isolates inhibit the growth of pathogen strains, and the genes associated with the bacteriocin production were found in some of these isolates [29]. The composition of microbiota of the human intestinal tract begins to form even before the birth. The child receives microorganisms through the birth canal [37, 42], as well as with breast milk. A typical childhood type of intestinal microbiota formed soon after birth is characterized by high concentrations of representatives of the genera Bifidobacterium and Lactobacillus [19]. It was logical to assume that representatives of the intestinal microbiota can be a source of obtaining the bacteriocins. Reutericin 6, determined by mass spectrometry, is a bacteriocin with a molecular weight of 5652 D, produced by Lactobacillus reuteri LA6, which was isolated from the feces of a human infant at the age of 2 months. The primary structure of reutericin 6 by the molecular weight was identical to gassericin A produced by Lactobacillus gasseri LA39, which was isolated from the feces of the same human infant at the age of 4 months. It has been shown that reutericin 6 belongs to cyclic bactericins of class IIc. PCR amplification on chromosomal DNA of L. reuteri LA6 as matrix with cloned primers based on DNA sequences (gassericin A and acidocin B from Lactobacillus

Bacteriocins Lactobacillus — an alternative to antimicrobial drugs acidophilus M46) and sequencing showed that L. reuteri LA6 possesses a structural gene which is specific of gassericin A. These results demonstrate that bacteriocin with the same structure was produced by different species of lactobacilli isolated from the same infant [23]. The intestinal microbiota of adults can unite representatives of more than 600 different genera, including many representatives of the Lactobacillus genus [14, 42]. Scientists have found that L. salivarius strain SPW1 isolated from human feces synthesizes a new bacteriocin salivaricin mmaye 1. L. salivarius belongs to the main components of the human intestinal microbiota and does not exhibit any toxi­ city [16, 42]. It also has probiotic properties and improves people and animal health [43]. It has been shown that salivaricin mmaye 1 has a molecular weight of about 1221 Da, it is associated with the cell wall, is effective at micromolar concentrations, and has a wide spectrum of antibacterial activity. Besides, salivaricin mmaye 1 showed high thermal and chemical stability and moderate stability at different pH values [43]. The studies, carried out within the framework of the Human Microbiome project, revealed that Lactobacillus species dominate in the microbiota of reproductive tract of women [18, 42]. Lactobacilli, which were isolated from human vaginal secretions, were tested for the production of antimicrobial substances with the potential to provide physiological protection against pathogenic microorganisms in the vaginal area [34]. About 10 % of the isolates showed antibacterial activity against one or more closely related microorganisms used as indicators. Lactobacillus fermentum CS57 was

the best producent and secreted a bacteriocinlike substance with antagonistic activity against Streptococcus agalactiae and Candida albicans. These substances were sensitive to proteolytic enzymes and resistant to high temperatures. The mechanism of their action was identified as bactericidal, and the molecular weight was determined as more than 30 kDa. Taking into account all the results, the authors consider it possible to use L. fermentum CS57 as a probiotic for the prevention of human vaginal infections [34]. There is rather interesting information about the results of a study of heat-resistant bacteriocin salivaricin CRL 1328, which was synthesized by Lactobacillus salivarius CRL 1328. The scientists isolated this strain from the vagina of a healthy woman and established that this substance can be successfully used for the prevention of urogenital infections [31]. Thus, lactobacilli, the representatives of normal human microbiota, are the most promising source of bacteriocins, considering the safety of strains, which also have probiotic significance.

Conclusions In view of the spreading resistance of pathogenic microorganisms to antibiotics, one of the modern trends in the search for medicines with antimicrobial activity is the use of bacteriocins — the substances of a protein-peptide nature with a wide spectrum of antimicrobial activity. Bacteriocins are conventionally divided into three classes due to their molecular weight, structure and relation to temperature. Bacteriocins of lactic acid bacteria can be isolated from various biotopes of humans, as 93

I. M. Voloshyna, K. I. Soloshenko, V. O. Krasinko et al. well as from various fermented food and milk products. Promising directions for obtaining Lacto­ bacillus bacteriocins include the stages of isolation of microbial cultures from natural sour­ces, screening of the most active producents, and experimental enhancement of the producent’s activity, including classical methods of mutagenesis and genetic engineering manipulations. Bacteriocins of Lactobacillus can be used in medicine, veterinary medicine and food industry as an effective and safe alternative to antibiotics and food preservatives.

📖 中文全文 Chinese Full Text

中文

# 乳酸菌细菌素——抗菌药物的替代选择

**I. M. Voloshyna¹², K. I. Soloshenko², V. O. Krasinko², I. V. Lych², L. V. Shkotova³**

¹ 基辅国立技术与设计大学,乌克兰基辅,01011,Nemirovich-Danchenko街2号 ² 国立食品技术大学,乌克兰基辅,01601,Volodymyrska街68号 ³ 乌克兰国家科学院分子生物学与遗传研究所,乌克兰基辅,03143,Akademika Zabolotnoho街150号

**摘要:** 本综述介绍了乳杆菌科细菌的特征及其合成多种细菌素的能力。文中给出了乳杆菌细菌素的分类,包括三类:I类——羊毛硫抗生素(分子量小于5 kDa、含羊毛硫氨酸的肽类);II类——非修饰细菌素,又称非羊毛硫抗生素(不含羊毛硫氨酸、分子量小于10 kDa的耐热肽类);III类——一组研究尚不充分的分子量大于30 kDa的热不稳定蛋白质。研究表明,乳杆菌可合成广谱细菌素,具有多种作用方式,能够抑制多种机会性革兰氏阳性菌的生长。文中还列举了从食品(发酵肉制品、鱼类、康普茶、山羊奶、马奶酒等)和人体不同生物位点(母乳、肠道和阴道分泌物的微生物群)中分离的乳杆菌所产生的细菌素实例。此外,综述展示了乳杆菌合成的细菌素在食品和制药工业中广泛应用的前景。

**关键词:** 细菌素,乳杆菌,乳酸球菌,乳酸菌,益生菌

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## 引言

医药市场上有众多药物,但由于各种外源性和内源性因素对人体主要系统正常功能产生不利影响,发病率呈上升趋势。首先是环境因素不利、营养不均衡、维生素和微量元素缺乏、应激情况增多,以及化学治疗药物和抗生素的大量无节制使用。上述因素的共同作用导致病原微生物对抗菌药物产生耐药性,因此有必要开发新型有效的抗菌药物。利用细菌素是寻找具有抗菌活性药物的现代趋势之一。

细菌素是由细菌核糖体合成的肽或蛋白质,对通常与产生菌株密切相关的其他细菌具有抗菌活性。细菌素由多种微生物合成,已在医学、兽医学和食品技术中作为治疗剂以及食品防腐剂得到广泛应用,用于对抗各种感染性病原体和食源性病原体。

某些抗生素对人体健康具有有害副作用,而细菌素不具有或仅具有极低的细胞毒性。这主要是因为所测试的细菌素由乳酸菌产生。乳酸菌长期以来被用作发酵和乳制品生产中的生物防腐剂,也是健康人体消化道中正常微生物群过度定植的因素之一。细菌素的优良特性使其可用于替代抗生素或增强抗生素的作用,并降低耐药菌株的产生率。

人体微生物群中的有益菌可被动员产生细菌素,从而防止胃肠道(GIT)外表面上皮细胞的细菌感染。

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## 乳杆菌的特征

乳酸菌(LAB)是一类多样且极具价值的微生物群体,虽未遵循严格的分类学分类,但根据其共同特性归为一类,其共同特征是能够合成乳酸(LA)作为主要或唯一的发酵产物。

乳杆菌属细菌几乎分布于消化道的所有生物位点,因此被认为是人体主要的微生物群。乳杆菌属包含数百个物种。基于16S rRNA序列分析,乳杆菌在系统发育上分为七个类群:布氏乳杆菌群(bu)、干酪乳杆菌群(ca)、德氏乳杆菌群(de)、植物乳杆菌群(pl)、罗伊氏乳杆菌群(re)、清酒乳杆菌群(sa)和唾液乳杆菌群(sl)。传统上,根据碳水化合物发酵方式,乳杆菌属细菌分为三组:(1)专性同型发酵菌;(2)兼性异型发酵菌;(3)专性异型发酵菌。

乳杆菌为革兰氏阳性无芽孢形成菌,专性或兼性厌氧,具有极高的酶活性,形态和大小极为多样。可呈短至长丝状杆状,单个、成对或短链排列。在正常代谢过程中,乳杆菌能够形成乳酸、过氧化氢,产生溶菌酶以及具有抗生素活性的物质,如罗伊菌素、植物乳菌素、乳菌素、乳醇等。异型发酵型乳杆菌还可合成乳酸、乙酸、丁酸等多种酸类以及二氧化碳。

乳杆菌具有多种生物活性,例如有助于刺激胃液和消化酶的分泌以增强消化过程,能够减轻抗生素的副作用,帮助分解胆汁盐并正常化脂质代谢。其他重要特征包括保护上皮细胞免受损伤、促进肠道黏膜再生以及通过正常化微生物群整体组成来减轻炎症过程等特性。

大多数乳酸菌能够合成蛋白质-肽类抗生素物质,抑制或延缓相关细菌种和/或菌株的生长,并具有广谱抗菌活性,因此被称为细菌素。细菌素基本为高分子量(高达10–30 kDa)的热稳定物质。其生物合成由特殊质粒编码,在核糖体上进行。

有必要更详细地讨论乳杆菌细菌素的分类和特性。

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## 细菌素的分类

细菌素通常分为三类:I类——羊毛硫抗生素;II类——非修饰细菌素,又称非羊毛硫抗生素;III类——一组分子量大于30 kDa的热不稳定蛋白质。

I类细菌素为分子量小于5 kDa、含羊毛硫氨酸的肽类,包含羊毛硫氨酸(Lan)、α-甲基羊毛硫氨酸(MeLan)、脱氢丙氨酸和脱氢丁氨酸等氨基酸。根据化学结构和抗菌特性,该类分为A型和B型羊毛硫抗生素。A型羊毛硫抗生素为小的阳离子肽,通过在细菌膜上形成孔道发挥抗菌活性;B型代表为小的阴离子或中性球状肽,其抗菌特性通过抑制特定酶来实现。

II类细菌素为不含羊毛硫氨酸、分子量小于10 kDa的耐热肽类。该组代表对李斯特菌属具有抗菌活性,能够破坏微生物膜的完整性,导致靶细胞内离子失衡和有机磷丢失。该类代表分为四个亚类:IIa类包含片球菌素样细菌素,含有N端序列Tyr-Gly-Asn-Gly-Val-Xaa-Cys(TGAGV);IIb类由双肽细菌素组成,其活性依赖于两种不同的肽,两种肽可独立显示活性,但在协同作用时表现出增效效应;IIc类包含环状细菌素;IId类包含非片球菌素样的非修饰线性细菌素。

III类细菌素包括一组分子量大于30 kDa的热不稳定蛋白质,遗憾的是其特性尚未得到充分研究。

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## 乳杆菌产生的细菌素的多样性

乳杆菌合成广谱细菌素,这些物质具有多种作用方式,抑制多种机会性革兰氏阳性菌的生长,例如单核细胞增生李斯特菌、丁酸梭菌、产芽孢梭菌、金黄色葡萄球菌、粪肠球菌、芽孢杆菌属等。活性细菌素的合成是赋予乳杆菌高定植特性的因素之一,并在维持生物群落中生理微生物平衡方面发挥调节作用。

大多数细菌素为具有两亲性和高等电点的小分子。产生细胞由于合成特异性免疫蛋白而对自身产生的细菌素具有抗性。

目前,关于细菌素抗菌作用机制的研究正在积极进行。研究发现,乳杆菌细菌素含有固定在靶细胞特异性细胞受体上的蛋白质组分,破坏各种阳离子通过微生物细胞膜的转运。研究最为充分的乳杆菌细菌素包括:来自淀粉乳杆菌471(L. amylovorus 471119)的淀粉乳菌素471、来自嗜酸乳杆菌(L. acidophilus)的酸球菌素B、来自巴伐利亚乳杆菌MN(L. bavaricus MN)的巴伐利亚菌素MN、来自干酪乳杆菌(L. casei)的干酪菌素、来自弯曲乳杆菌FS47和弯曲乳杆菌LTH1174(L. curvatus FS47和L. curvatus LTH1174)的弯曲菌素FS47和A、来自清酒乳杆菌L 45(L. sake L 45)的乳菌素S、来自植物乳杆菌(L. plantarum)的植物乳菌素A和C、来自植物乳杆菌LTF154(L. plantarum LTF154)的植物乳菌素154、来自清酒乳杆菌Lb674(L. sake Lb674)的清酒菌素674等。文献中还记载了乳杆菌的新型细菌素,如来自唾液乳杆菌(L. salivarius)的唾液乳菌素mmaye1,以及来自植物乳杆菌亚种argentoratensis SJ33(L. plantarum subsp. argentoratensis SJ33)的BacF1和BacF2。

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## 从食品中分离的乳杆菌细菌素

由于细菌素的独特特性,其在食品工业中被广泛应用。它们以部分纯化或纯化浓缩形式用作防腐剂。直到最近,乳酸链球菌素和片球菌素PA-1等细菌素才被许可作为食品防腐剂。值得注意的是,使用细菌素可降低食品生产和保存成本,同时保持其营养和生物价值。

乳酸菌在发酵食品生产技术中发挥重要作用,其功能是防止病原微生物生长和食品整体变质。这是通过酸化环境和积极合成抗菌化合物实现的,不仅有助于提高质量,还有助于提升安全性。

乳酸菌,尤其是清酒乳杆菌(Lactobacillus sakei)和弯曲乳杆菌(Lactobacillus curvatus),是许多发酵肉制品微生物群的组成部分。这些物种能很好地适应肉类环境,改善发酵肉制品的风味并加速其成熟。

乳酸菌产生的细菌素以其对单核细胞增生李斯特菌的活性而闻名,该菌是常见的革兰氏阳性病原菌,近几十年来已引起多起食源性疾病暴发。在细菌素的一种分类中,有一个专门针对具有抗李斯特菌活性的细菌素的类别。控制食品中的单核细胞增生李斯特菌是一项重大挑战,因为它能够在低pH值、高浓度盐和亚硝酸盐存在下存活,而这些条件对干发酵食品生产中大多数其他病原微生物是有害的。正因如此,产细菌素的乳酸菌及其细菌素作为发酵食品产品中的防腐剂非常有用,可作为化学防腐剂的技术替代品,满足对含较少或无添加剂食品的需求。

近年来,由于消费者偏好含化学防腐剂较少的食品,对"天然"产品的需求有所增加。与天然产品相关的关键问题是如何保持其安全性和质量,以及如何延长保质期。在这方面,人们高度关注利用乳杆菌的拮抗特性。研究表明,从康普茶(中国南方传统发酵饮料)中分离的植物乳杆菌SLG10产生的细菌素SLG10对革兰氏阳性和革兰氏阴性菌(包括多重耐药菌株)均具有抗菌活性。细菌素SLG10具有热稳定性、pH耐受性,对大多数蛋白酶敏感,但对胰蛋白酶或胃蛋白酶不敏感。抗菌机制研究表明,细菌素SLG10增加细胞膜通透性,诱导钾离子释放,并能抑制生物膜形成。

近年来,在乳制品中发现了大量抗生素耐药细菌,例如干奶粉中的肠炎沙门氏菌、原料奶和冰淇淋中的金黄色葡萄球菌以及奶酪中的万古霉素耐药粪肠球菌。文献中有信息表明,乳酸菌产生的某些细菌素可抑制食源性多重耐药病原体,这使其有别于其他已注册但抑菌谱较窄的细菌素。

研究人员高度重视研究乳酸菌产生天然防腐剂的特性。研究表明,弯曲乳杆菌MBSa2和MBSa3在MRS培养基上合成细菌素始于指数生长早期(培养4小时)。在37°C培养条件下,12小时后两株菌株产生的细菌素量均开始减少。MBSa2细菌素的最大积累量(12800 U/ml)在25°C和37°C下培养8小时以及在30°C下培养6小时时观察到。这表明该代谢物具有一级动力学特征,其他细菌素如清酒菌素K(产生菌:清酒乳杆菌CTC 494)、清酒菌素P(清酒乳杆菌CCUG 42687)、弯曲菌素A(弯曲乳杆菌LTH 1174)、弯曲菌素L442(弯曲乳杆菌L422)也观察到类似特征。

文献资料指出,许多细菌素具有热稳定性,因为它们在热处理(100–120°C,15分钟)后仍保持其特性。这表明它们可用于热处理食品而不降低其防腐作用。通常低分子量细菌素具有热稳定性,因为它们是小分子多肽。MBSa2和MBSa3细菌素(弯曲乳杆菌)、清酒菌素M和P(清酒乳杆菌)、片球菌素L50(戊糖片球菌)、酸球菌素D20079(嗜酸乳杆菌)、植物乳菌素LP31(植物乳杆菌)均具有这些特性。

鉴于乳酸菌细菌素在食品技术中的独特性质和不断扩大的应用前景,研究人员正积极从传统食品和原料中寻找和分离这些生物活性化合物的产生菌。因此,从马奶酒(中国新疆)中分离的乳杆菌 crustorum菌株可产生细菌素MN047 A。马奶酒是用马奶发酵制成的传统发酵乳制品,在中亚草原地区广受欢迎,包括中国、蒙古、哈萨克斯坦、吉尔吉斯斯坦和俄罗斯部分地区。几个世纪以来,马奶酒不仅被视为饮料,还被视为具有医疗用途的功能性食品,如改善肾脏、胃肠道、神经系统和免疫系统功能,治疗肝炎、慢性溃疡、结核病等。马奶酒通常通过马奶自身天然微生物群(包括乳酸菌和酵母)发酵制成。在马奶酒中已发现多种乳杆菌菌株,包括干酪乳杆菌、植物乳杆菌、发酵乳杆菌、瑞士乳杆菌和嗜酸乳杆菌,但仅植物乳杆菌产生的细菌素已被纯化和表征。

越来越多的研究人员致力于全面研究分离细菌素的特性。因此,由发酵乳杆菌BZ532合成的细菌素LF-BZ532似乎具有进一步实际应用的潜力。该菌株从中国发酵谷物饮料(bozai)中分离,通过16s rRNA测序鉴定。细菌素LF-BZ532的分子量为1105.563 Da。研究发现,该细菌素对革兰氏阳性和革兰氏阴性菌(包括假单胞菌属和李斯特菌属)具有广谱抗菌活性。所描述细菌素的独特特性包括显著的热稳定性,在100°C和121°C(分别为30分钟和20分钟)下残余活性分别为88.19%和56.98%。此外,它在较宽pH范围(2–8)内稳定,但对蛋白水解酶(蛋白酶K、胃蛋白酶和胰蛋白酶)高度敏感,表明其肽类性质。基于上述结果,推测纯化的LF-BZ532及其产生菌株发酵乳杆菌BZ532是有望作为食品工业生物防腐剂的候选者。

从山羊奶中分离的清酒乳杆菌GM3菌株表现出对酸和胆汁的拮抗性,并对食源性病原体具有拮抗活性。清酒乳杆菌GM3的细菌素产生在静止期(培养18小时)达到最大值。对细菌素GM3特性的研究表明,它在较宽pH和温度范围内保持活性,对有机溶剂具有抗性。同时,细菌素GM3对某些蛋白酶敏感。发现细菌素的分子量为4.8 kDa。在HT29细胞模型中的细胞毒性研究表明,在细菌素浓度为2240 U/ml时,最大存活抑制率为45.60 ± 0.5%。这些结果表明,清酒乳杆菌GM3有潜力作为生物防腐剂应用于食品工业。

由带鱼(Trichiurus lepturus)中分离的植物乳杆菌DY4-2菌株合成的细菌素DY4-2相当有趣。该细菌素在静止期培养24小时后合成量最大。细菌素DY4-2的分子量测定为1465 Da。细菌素DY4-2具有显著的热稳定性(121°C下30分钟),在pH 2.5–5.5范围内保持活性,但对蛋白酶敏感。该细菌素对鱼类病原菌如荧光铜绿假单胞菌、铜绿假单胞菌、副溶血性弧菌、温和气单胞菌和单核细胞增生李斯特菌表现出广谱抗菌活性。将部分纯化的细菌素DY4-2添加到大比目鱼鱼片中,在4°C下12天内使荧光铜绿假单胞菌细胞数减少了2.7个对数单位。与对照相比,经细菌素DY4-2处理的样品中活微生物总数显著减少。这些研究结果表明,细菌素DY4-2具有作为海产品生物防腐剂的潜力。

鉴于细菌素生物技术生产的前景,研究人员正在选择最具成本效益的生物合成底物。乳清是奶酪生产中凝乳和去除酪蛋白后获得的主要副产品,是乳制品工业中的大规模废弃物。当乳清排入水中时,其生物降解性较弱,但溶解氧水平降低,对水体正常自然自净过程产生不利影响,并对水生生物的生存构成实际风险。排放含乳清废水的做法导致许多严重的环境问题:影响土壤理化特性,进而导致产量下降。因此,寻找乳清利用的经济方法仍然具有现实意义。

由于乳清约占牛奶全部营养物质的55%,将其作为生物活性物质生产底物是一种经济且有利可图的选择。乳清中最常见的营养物质为乳糖(75%)、可溶性蛋白质(12–14%)、脂类和矿物盐(1–10%),这些是微生物生长所必需的,尤其是食品工业中广泛使用的乳酸菌。虽然细菌素可由多种微生物产生,但乳酸菌产生的细菌素正受到越来越多的关注,因为它们被认为是最"安全"的。

植物乳杆菌能够发酵多种碳水化合物,因此可适应各种生态位。特别是,植物乳杆菌ST16Pa菌株能在基于乳清的培养基上积极生长,并产生分子量为6.5 kDa的肽,对多种不同食源性病原菌(包括革兰氏阴性菌)表现出抗菌活性。

虽然乳清可支持大多数乳酸菌的生长,但缺乏氮源和其他营养物质,因此需要外源添加这些物质以成功实现细菌素的生物合成。研究人员证明,在MRS培养基上培养的植物乳杆菌ST16菌株能够合成对多种微生物具有高抗菌活性的细菌素。然而,在奶酪乳清上培养的该菌株尽管积累了生物量,却不产生细菌素。

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## 从人体中分离的乳杆菌细菌素

人体正常微生物群对人类健康发挥着重要作用。已证明人体共生微生物在防御病原体、维持稳定免疫以及合成维生素、有机酸、氨基酸等生命必需化合物方面具有独特功能。

乳杆菌是人类和动物消化道的典型栖居菌。人体正常微生物群微生物是细菌素最安全的来源之一。这些细菌素参与人体内的拮抗活性机制,并用于维持其微生物群的动态平衡。产生细菌素的能力是益生菌菌株的重要特征。

根据联合国粮农组织/世界卫生组织(FAO/WHO,2002年)的要求,益生菌细菌应具有在胃肠道中存活的高能力和对肠上皮细胞的黏附能力,最重要的是应对人类和动物安全的菌株。由于乳杆菌被认为是安全的益生菌微生物,因此被广泛用于食品工业以生产各种产品(蔬菜、肉类、乳制品等)。因此,从人体中搜索、分离和研究乳杆菌细菌素的研究在科学文献中越来越频繁地出现。

因此,已有研究结果发表,其中从母乳中分离出乳杆菌细菌素。从伊朗洛雷斯坦省和马克齐省农村地区19至35岁的志愿母亲中采集了60份母乳样本。使用乳杆菌特异性PCR引物对分离物进行鉴定,结果显示33个分离物中有18个为乳杆菌菌株。在这些分离物中鉴定出罗伊氏乳杆菌和加氏乳杆菌,它们能在低pH值和胆汁盐存在下存活。研究还表明,所有乳杆菌分离物均能抑制病原菌株的生长,并在部分分离物中发现了与细菌素产生相关的基因。

人体肠道微生物群的组成在出生前就已开始形成。新生儿通过产道获得微生物,同时也通过母乳获得。出生后不久形成的典型儿童型肠道微生物群以双歧杆菌属和乳杆菌属的高浓度为特征。因此,有理由假设肠道微生物群的代表可作为细菌素的来源。

通过质谱法测定的reutericin 6是一种分子量为5652 Da的细菌素,由从2个月大人类婴儿粪便中分离的罗伊氏乳杆菌LA6产生。reutericin 6的一级分子量结构与加氏乳杆菌LA39产生的gassericin A相同,加氏乳杆菌LA39从同一婴儿4个月大时的粪便中分离。研究表明,reutericin 6属于IIc类环状细菌素。以罗伊氏乳杆菌LA6染色体DNA为模板,利用基于DNA序列(来自嗜酸乳杆菌M46的gassericin A和acidocin B)的克隆引物进行PCR扩增和测序,结果显示罗伊氏乳杆菌LA6具有gassericin A的特异性结构基因。这些结果表明,从同一婴儿中分离的不同种类乳杆菌产生了结构相同的细菌素。

成人肠道微生物群的组成可包含600多个不同属的代表,其中包括许多乳杆菌属的代表。科学家发现,从人类粪便中分离的唾液乳杆菌SPW1菌株合成一种新型细菌素——唾液乳菌素mmaye 1。唾液乳杆菌是人类肠道微生物群的主要成分,不表现出任何毒性。它还具有益生菌特性,可改善人类和动物健康。

研究表明,唾液乳菌素mmaye 1的分子量约为1221 Da,与细胞壁相关,在微摩尔浓度下有效,具有广谱抗菌活性。此外,唾液乳菌素mmaye 1表现出高热和化学稳定性以及在不同pH值下的中等稳定性。

在人类微生物组项目框架内进行的研究揭示,乳杆菌属在女性生殖道微生物群中占主导地位。

从人类阴道分泌物中分离的乳杆菌被测试产生抗菌物质的潜力,以提供针对阴道区域病原微生物的生理保护。约10%的分离物对一个或多个用作指示菌的密切相关微生物表现出抗菌活性。发酵乳杆菌CS57是最佳产生菌,分泌一种具有拮抗活性的细菌素样物质,对无乳念珠菌和白色念珠菌具有抑制作用。这些物质对蛋白酶敏感,对高温具有抗性。其作用机制被确定为杀菌作用,分子量测定为大于30 kDa。综合考虑所有结果,作者认为发酵乳杆菌CS57有可能用作预防人类阴道感染的益生菌。

关于由唾液乳杆菌CRL 1328合成的耐热细菌素唾液乳菌素CRL 1328的研究结果相当有趣。科学家从健康女性的阴道中分离出该菌株,并确定该物质可成功用于预防泌尿生殖道感染。

因此,作为人体正常微生物群代表的乳杆菌是细菌素最有前景的来源,考虑到菌株的安全性及其益生菌意义。

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## 结论

鉴于病原微生物对抗生素耐药性的蔓延,利用细菌素——一类具有广谱抗菌活性的蛋白质-肽类物质——是寻找具有抗菌活性药物的现代趋势之一。

细菌素通常根据其分子量、结构和与温度的关系分为三类。

乳酸菌的细菌素可从人体的各种生物位点以及各种发酵食品和乳制品中获得。

获得乳杆菌细菌素的有前景方向包括从天然来源分离微生物培养物、筛选最活跃的产生菌,以及通过实验增强产生菌的活性,包括经典诱变方法和基因工程操作。

乳杆菌细菌素可在医学、兽医学和食品工业中用作抗生素和食品添加剂的有效且安全的替代品。