Acta Biochimica Polonica, Vol. 64, No 3/2017, 459–464, https://doi.org/10.18388/abp.2017_1496

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Lactic acid bacteria stress response to preservation processes in the beverage and juice industry

Joanna Bucka-Kolendo* and Barbara Sokołowska

Department of Fruit and Vegetable Products Technology, prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology,
Warsaw, Poland

In this review we summarize stress factors that affect the lactic acid bacteria (LAB) and cause different molecular stress responses. LAB belong to a group of bacteria that is very widespread in food and beverages. They are present, and desired, in fermented products like yogurts, cheese, vegetables, meat or wine. In most of them, LAB are providing positive sensory and nutritive features. However, as harmless and desired microbes in one product, LAB can cause spoilage and a bad taste of others, especially in juices and beverages. LAB are resistant to many stress factors which allows them to survive in harsh environments. The most common stress factors they have to deal with are: heat, cold, acidity, NaCl and high hydrostatic pressure (HHP). Their ability to survive depends on their skills to cope with stress factors. Under stress conditions, LAB activate mechanisms that allow them to adjust to the new conditions, which can influence their viability and technological properties. This ability to adapt to different stress conditions may come from the cross-protection systems they have, as resistance to one factor may help them to deal with the other stress effectors. LAB are highly valuable for the food industry and that is why it is important to understand their stress response mechanisms.

Key words: Lactic acid bacteria, LAB, stress factors, stress response, cross-protection

Received: 05 January, 2017; revised: 12 April, 2017; accepted:
12 April, 2017; available on-line: 09 August, 2017

*e-mail: joanna.bucka@ibprs.pl

Abbreviations: HHP, high hydrostatic pressure; LAB, lactic acid bacteria

Introduction

Lactic Acid Bacteria (LAB) are the most widespread group of bacteria that is used in fermented foods. They are natural inhabitants of the human gastric intestine, and can be applied in different fermented products and probiotic foods (Ficco et al., 2009). They are present in products like yogurts, sourdoughs, sour vegetables, cheese, wine or meat and play a crucial role in the development of the organoleptic and hygienic quality of fermented products (van de Gutche et al., 2002). The technological benefit of Lactic Acid Bacteria depends on the ability to enhance safety, flavour, texture and nutritional value (Salminen & von Wright, 2004). Some LAB, due to their probiotic properties, can be used in the production of functional food and potential oral vaccines (Shah 2007; Siragusa et al., 2007; Parente et al., 2010).

At the same time, LAB can cause spoilage of food. They can grow in improperly pasteurized beverages and juices in bottles and cans, in vacuum packed products with a deficit of oxygen. LAB can enter a given product along with the raw material, additives or with packing materials (Lawlor et al., 2009). The most common species that cause spoilage of beverages are Lactobacillus paracasei and Leuconostoc mesenteroides (Back, 2005), as well as Lactobacillus brevis, Lactobacillus buchneri, Lactobacillus plantarum, Lactobacillus perolens and Weissella confusa. Many bacteria from these species are also responsible for beer spoilage.

LAB mainly ferment sucrose to lactic acid. Depending on the species and growth conditions, catabolism of sugars can also lead to the formation of ethanol, acetate, formic acid or succinate (Hammes & Hertel, 2009). Some of the bacteria can produce diacetyl that gives a bitter taste and flavour of the products. That is why LAB are undesirable in beverages and juices. It has been reported that formic acid in apple juices can indicate food spoilage (Gökmen & Acar, 2004). The L. mesenteroides and W. confusa bacteria can synthesize compounds which cause ropiness of the final product (Back, 2005). Ropiness caused by LAB is the reason why these bacteria are believed to be potentially a cider spoilage indicator (Ibarburu et al., 2010).

In alcohol beverages, LAB can influence the bitter flavor by converting glycerol to 3-hydroxypropionaldehyde, which can transform to acrolein and bind with polyphenols creating bitter compounds (Sauvageot et al., 2000; Garai-Ibabe et al., 2008; Juvonen et al., 2011).

Preservation methods

Many factors affecting bacteria during the preservation process of beverages and juices can act as potential stress effectors for them. Physical preservation techniques of food are used in order to reduce the number, or to prevent the growth of unwanted microflora in the products (Juvonen et al., 2011). Traditional prevention techniques used in the beverage industry include thermal processing and filtration. Thermal processing is the most efficient technique of food preservation. It can prevent not only the growth of unwanted microflora but also can suppress unwanted enzymatic activity (Back 2005). However, processes that use high temperatures destroy many bioactive and aromatic compounds, causing modification of the flavor, color and nutritional value. The increase of consumer demands for “fresh like” foods brings new challenges for techniques used in food preservation. Nowadays, high hydrostatic pressure techniques (HHP) are used more often, as they can reduce the number of microbes in liquid food products like beverages, juices and alcohol beverages – beer, wine or cider.

High hydrostatic pressure can induce in bacteria many changes, like physiological changes (Wouters et al., 1998; Korakli et al., 2002), changes in gene expression (Welch et al., 1993; Drews et al., 2002; Wemekamp-Kamphuis et al., 2002) and in protein translation (Sato et al., 1995; Ehrmann et al., 2001), and can also lead to cell damage (Ulmer et al., 2002) and death (Vogel et al., 2002; Scheyhing et al., 2004). HHP does not break the covalent bindings. Thanks to this, the primary structure of proteins and fatty acids stays unaffected (Considine et al., 2008; Reundueles et al., 2011). Molecules, like vitamins, amino acids, flavor compounds and other small molecules stay undamaged by HHP, as well as organoleptic characteristics of food. Serrazanetti and coworkers (2009 and 2013) had shown that some proteins undergo induction as a result of HHP, and a few of them are also involved in different types of stress responses including cross-protection.

Stress response to HHP cannot be expected in LAB while it is perfomred in their natural environment, as those bacteria are not normally exposed to this stress factor (Lorca & Font de Valdez, 2009). Compared to other stress factors, LAB response to HHP is more complex, as some of the effects are very similar to those caused by other factors. Their ability to react to HHP can be explained by a bacteria cross-protection system to different stress factors (Scheyhing et al., 2004; Lorca & Font de Valdez, 2009). However, the LAB cross-protection response to HHP is not well documented in the literature as yet. In Lactobacillus plantarum, higher sensitivity to HHP was observed when heat shock was used at the same time as HHP.

As shown by Sokołowska and coworkers (2012 and 2014), LAB belong to a group of organisms that are resistant to the effect of high hydrostatic pressure, and their growth can be a valuable tool to evaluate the shelf life of preserved products with this method (Mathias et al., 2013).

LAB stress response mechanisms

It is believed that environmental stress response in LAB can vary between species and depends on the type of stress that has been applied (van de Gutche et al., 2002). The well- known LAB stress responses are those to heat shock (De Angelis et al., 2004), bile (Bron et al., 2006), and oxidative (Serrano et al., 2007), low pH and ethanol stresses (Alegría et al., 2004; Parente et al., 2010).

Bacterial stress response is based on coordinated genes expression that affects different cellular processes (cell division, transport, cell membrane composition, DNA metabolism) (Stortz & Hengge-Aronis, 2000; van de Gutche et al., 2002). LAB achieve an integrated stress response through a regulatory web that allows them to react to environmental changes. Bacteria activate mechanisms allowing them to adapt to new conditions, which can influence the viability and technological properties. Adaptation to stress conditions can also cause morphological changes which affect food spoilage (Asano et al., 2007). Many typical spoilages that occur in beverages, juices and alcohol beverages, like ropiness and volatile phenols formation, are related to stress. LAB have a significance in the food industry and that is why knowing their stress effectors is very important (van de Guchte et al., 2002; Parente et al., 2010). Under stress conditions, in order to protect cells from influence of the same or other type of stress factors, bacteria can trigger a cross-protection response (van de Guchte et al., 2002; Smits & Brul, 2005; Chung et al., 2006).

Gene regulation in the LAB stress response

In an unfavourable environment, many forms of LAB can convert into VBNC – a viable but nonculturable state. In this state, the bacteria cannot be identified with classical microbiology methods, and this can be achieved only with the use of more advanced molecular biology techniques. Considering niche differentiation that LAB are able to colonize, a high phenotype and genotype diversity is observed (Molenaar et al., 2005; Di Cagno et al., 2010; Siezen et al., 2010; Ricciardi et al., 2012). Gene expression caused by different stress factors allows to identify biomarkers responsible for stress resistance (Juvonen et al., 2011).

Depending on the type of regulation, these genes are divided into six classes (Helman et al., 2001; Darmon et al., 2002; Schumann, 2003; Castaldo et al., 2006).

Class I and III are controlled by two types of transcriptional repressors: HrcA and CtsR. The first class is comprised by heat shock genes, including the dnaK and groEL operons. They encode proteins belonging to two chaperon complexes, DnaK-GrpE-DnaJ and GroES-GroEL, respectively (Castaldo et al., 2006). Both operons are regulated by the HrcA repressor protein, which binds with the CIRCE operator (Controlling Inverted Repeat for Chaperon Expression) under the stress-free conditions. Genes encoding heat shock proteins and HrcA are being used for taxonomical purposes of several species, including Lactobacillus (Blaiotta et al., 2008; Fiocco et al., 2010; Huang et al., 2010; Guidone et al., 2015).

The class II gene expression is dependent on the σB sigma factor, the synthesis and activity of which is increased under different stresses (Hecker et al., 1996; Kruger & Hecker, 1998; Varmanen et al., 2000).

Mechanisms of class IV transcriptional activation are not very well documented, while class V genes undergo regulation by a two-component signal transduction system (2CSs); for class VI, the regulation is still unknown (Schumann, 2003).

Initially, mechanism of the LAB response to stress conditions was compared with that of the documented model species – B. subtilis and E. coli. The best known stress response mechanisms are those present in the Bacillus subtilis species, where, at high temperatures over 200 genes are expressed (as shown by Castaldo et al., 2006). However, it had turned out that there were some differences in these mechanisms. As Ricciardi and coworkers had shown, the Class I and Class III genes’ stress response regulation differs in Lactobacillus plantarum from Bacillus subtilis, a model organism of Gram-positive bacteria. Other data suggest that stress response factors, like sigma factors, that are responsible for stress response in many Gram-positive and Gram-negative bacteria, are not important for LAB. The most striking difference is the lack of the σβ sigma factor, while several stress proteins, like DnaK, GroEL, Clp etc., and their regulators HrcA and CtsR are conserved.

The LAB stress response is regulated by a one-component regulatory system. For the Class I genes, major complexes of chaperons, like GroES-GroEL and GroE-DnaK-DnaJ (Lorca & Font de Valdez, 2009), are induced. Induction of these genes correlates with acid, ethanol, cold, osmotic, starvation and temperature stresses. In some bacteria, regulation of the GroES-GroEL and GroE-DnaK-DnaJ complexes, requires the presence of a σA sigma factor promoter and a highly conserved inverted repeat CIRCE, which binds the HrcA repressor (Zuber and Schumann 1994).

Regulation of heat stress response genes in Gram-positive bacteria was described as HrcA or CtsR dependent. This statement is still valid for B. subtilis and closely related to them Clostridum perfingens or Listeria monocytogenes bacteria (Chastanet et al., 2003, Chastanet and Msadek 2003, Lorca and Font de Valdez 2009).

The Class III heat shock genes CtsR repressor binds directly to a specific repeat sequence (the CtsR Box: a/ggtcaaaNaNa/ggtcaaa)(Derre et al., 2000). This sequence was found in other Gram-positive bacteria, like: Listeria monocytogenes, Streptococcus salivarius, Streptococcus pneumonia, Streptococcus pyogenes, Streptococcus thermophilus, Enterococcus faecalis, Staphylococcus aureus, Leuconostoc oenos, Lactobacillus sake, Lactobacillus lactis, and Clostridium acetobutylicum (Smeds et al., 1998, Derre et al., 1999, Ingmer et al., 1999).

In Lactobacillus plantarum, CtsR regulates transcription of the ctsR-clpC operon, hsp1 and ftsH (Russo et al., 2012). Deletion of CtsR influences the temperature sensitivity and changes morphology of cells under stress. It suggests that in L. plantarum, CtsR has a significant role in the heat shock tolerance by controlling the processes of protein quality (Fiocco et al., 2009, Fiocco et al., 2010). CtsR gene homologs were also identified in other bacteria: Listeria, Streptococcus, Leuconostoc, Lactococcus or Clostridium, which indicates that heat shock gene regulation by CtsR is highly conserved in those bacteria. That allows us to state that heat shock response regulation by CtsR is highly conserved in the Gram-positive bacteria (Derre et al., 1999).

Stress response to HPP has been well studied in the L. sakei and L. sanfranciscensis strains (Hörmann et al., 2006; Jofré et al., 2007). Hörmann et al.,(2006) had observed changes in the expression of 16 genes in Lactobacillus sanfranciscensis as an effect of HPP. Nine of those genes were over-expressed and seven were silenced as a result of stress. That can suggest that in LAB the stress response to HPP is negatively regulated by a one component protein system HrcA or CtsR, and by a two-component system of signal transduction (2CSs).

An overview of different types of the LAB stresses, their reported cross-resistance and the resistance mechanisms are shown in Table 1.

Conclusion

Growing pressure to lower the use of thermal processes and chemical preservatives in beverages and juices leads to maintain more natural products. However, this process may cause higher contamination by unwanted compounds produced by LAB. Although they may be harmless and desired microbes in one product, LAB can cause spoilage of other products.

A comparative study of the response of different bacterial strains to the same stress factors shows their diverse characteristics. In the context of food protection treatment, it is important to take under consideration that even closely related organisms can posses their individual, specific stress response mechanisms.

That is why, for different bacterial strains, there is a cross-response to various stress factors and cross-protection to different food preservation systems, like HHP, acidic, cold, and salt treatment, which needs to be taken under consideration.

Therefore the identification of stress response regulatory genes, like HrcA, CtsR, DnaK and FtsH, is necessary to control and evaluate the relationship between polymorphism of LAB in food products and the ability to cope with stress. At the same time, as a consequence of a highly conserved status in bacteria, these genes can be use as biomarkers.

Although present molecular methods allow to better understand the LAB taxonomy, it is believed that more data is needed to understand the stress related physiological dependence of those bacteria (De Angelis & Gobetti, 2011).

Genetic diversity evaluation of lactic acid bacteria, as an effect of stress factors that can occur during beverage and juice preservation processes, is important to control LAB in those products. A better understanding of the stress response related mechanisms in LAB allows to understand the basis of adaptation response and cross-protection mechanism they undergo (Van de Guchte et al., 2002), and thus can make these bacteria more useful in industrial processes.

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