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A Physiological Comparative Study of Acid Tolerance of Lactobacillus Plantarum ZDY 2013 and L

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A Physiological Comparative Study of Acid Tolerance of Lactobacillus Plantarum ZDY 2013 and L Ann Microbiol (2017) 67:669–677 DOI 10.1007/s13213-017-1295-x ORIGINAL ARTICLE A physiological comparative study of acid tolerance of Lactobacillus plantarum ZDY 2013 and L. plantarum ATCC 8014 at membrane and cytoplasm levels Yilin Guo 1 & Ximei Tian1 & Renhui Huang1 & Xueying Tao1 & Nagendra P. Shah2 & Hua Wei1,3 & Cuixiang Wan3 Received: 8 April 2017 /Accepted: 4 August 2017 /Published online: 23 August 2017 # Springer-Verlag GmbH Germany and the University of Milan 2017 Abstract This study aimed to disclose the acid tolerance metabolism, increased amino acid and enzyme level) of mechanism of Lactobacillus plantarum by comparing L. plantarum ZDY 2013 can protect the cells from acid stress. L. plantarum ZDY 2013 with the type strain L. plantarum ATCC 8014 in terms of cell membrane, energy metabolism, Keywords Lactobacillus plantarum . Acid tolerance . Cell and amino acid metabolism. L. plantarum ZDY 2013 had a membrane . Energy metabolism . Amino acids superior growth performance under acidic condition with 100-fold higher survival rate than that of L. plantarum ATCC 8014 at pH 2.5. To determine the acid tolerance Introduction physiological mechanism, cell integrity was investigated through scanning electron microscopy. The study revealed Lactic acid bacteria (LAB) have been used to produce that L. plantarum ZDY 2013 maintained cell morphology fermented food over the past decades and have been de- and integrity, which is much better than L. plantarum veloped as probiotics, which are generally recognized as ATCC 8014 under acid stress. Analysis of energy metabo- safe (GRAS) (De Vries et al. 2006), for their health- lism showed that, at pH 5.0, L. plantarum ZDY 2013 en- promoting functions in the human gastrointestinal tract hanced the activity of Na+/K+-ATPase and decreased the (Duary et al. 2010). Probiotics must maintain viability in ratio of NAD+/NADH in comparison with L. plantarum the gut at a high concentration (at least 106 cfu/mL) to be ATCC 8014. Similarly, amino acid metabolism of intracel- beneficial to the human host (Ferrando et al. 2015). lular arginine, glutamate, and alanine was improved in Therefore, the stronger resistance of LAB strains against L. plantarum ZDY 2013. Correspondingly, the activity of various extreme environments is a prerequisite for the de- arginine deiminase and glutamate decarboxylase of velopment of probiotic supplements. L. plantarum ZDY 2013 increased by 1.2-fold and 1.3-fold LAB are exposed to various stress conditions, such as acid, compared with L. plantarum ATCC 8014 in acid stress. In temperature, osmotic stress, or freeze drying in fermented food summary, it is demonstrated that the special physiological as well as in the gastrointestinal tract (Guchte et al. 2002). The behaviors (integrity of cell membrane, enhanced energy tolerance of LAB to these stressors is critical for screening potential candidates for LAB application. As probiotic candi- dates, bacteria have to survive under extreme acidic conditions or digestion by various enzymes in the entire gastrointestinal * Cuixiang Wan [email protected] tract (Wall et al. 2007). Given that acid stress is a pivotal issue for microbial survival, acid tolerance is generally considered as 1 State Key Laboratory of Food Science and Technology, Nanchang one of the criteria for selection of potential probiotics (De University, 235 Nanjing Donglu, Nanchang, Jiangxi 330047, China Angelis and Gobbetti 2004;Parvezetal.2006). 2 Food and Nutritional Science, School of Biological Science, The Few publications have focused on the acid tolerance mech- University of Hong Kong, Pokfulam Road, Hong Kong, China anism of LAB such as Lactococcus lactis (Rallu et al. 2000), 3 Jiangxi-OAI Joint Research Institute, Nanchang University, 235 Lactobacillus bulgaricus (Hernandez-Hernandez et al. 2012), Nanjing Donglu, Nanchang 330047, People’s Republic of China Lactobacillus casei (Broadbent et al. 2010), Lactobacillus 670 Ann Microbiol (2017) 67:669–677 plantarum (Hamon et al. 2014), and Lactobacillus reuteri type strain, L. plantarum ATCC 8014, were used in this study. (Teixeira et al. 2014) or on the aspect of proteomic analysis Both strains were incubated in MRS broth (Beijing Solarbio level. More routinely studied are the acid tolerance, H+- Science & Technology, Beijing, China) at 37 °C for 24 h under ATPase proton pump, glutamate decarboxylase (GAD) system, anaerobic condition. Growth conditions in MRS were applied and arginine deiminase (ADI) system of bacteria involved in in all subsequent experiments. For acid tolerance analyses, the pH homeostasis in Gram-positive bacteria (Cotter and Hill pH of MRS broth was adusted to 6.2, 4.5 and 3.5. 2003). For example, the activity of H+-ATPase increases under acidic conditions to support the acid tolerance of Bacillus spp. (Shobharani and Halami 2014); the GAD system contributes to Acid tolerance analyses and acid treatment acid tolerance of Listeria monocytogenes in gastric fluid (Cotter et al. 2001); and ADI protects Bacillus cereus ATCC14579 Growth of both L. plantarum strains was assessed under dif- (Senouci-Rezkallah et al. 2011), Escherichia coli (Lin et al. ferent acid conditions (pH 6.2, 4.5 and 3.5) in MRS broth, and 1995), and L. monocytogenes (Lin et al. 1995; Ryan et al. the optical density (OD) at 600 nm was monitored at different 2009) against acid stress through the production of ammonia. time points using a microplate reader (VersaMaxTM Tunable On the other hand, alterations in cell membrane and metabolic microplate reader; Molecular Devices, Sunnyvale, CA). pathways (e.g., energy metabolic pathway and amino acid me- Additionally, the survival of L. plantarum ZDY 2013 was tabolism) also control acid tolerance (Cotter and Hill 2003). For evaluated at pH 2.5 for 1.0 h in 0.01 M PBS with L plantarum instance, an increased proportion of long-chained, monounsat- ATCC 8014 for comparison. urated fatty acids were produced in Streptococcus mutans Cells of L. plantarum ZDY 2013 and L. plantarum ATCC UA159 in response to acid stress (Fozo and Quivey 2004); 8014 at mid-exponential growth phase were centrifuged at NADH oxidase, an enzyme responsible for oxidative stress, 10,000 g for 1 min, and incubated in PBS (pH 3.5, 4.5 and and which could possibly contribute to acid resistance, its ac- 5.0) at 37 °C for 1.0 h. Then, the acid-treated and untreated tivity of L. lactis (DeFelipeetal.1998), and Lactobacillus cells were used for further study. delbrueckii subsp. bulgaricus (Marty-Teysset et al. 2000)in- creased under acidic conditions; addition of glutamine in- creased the survival rate of L. reuteri 100–23 at pH 2.5 Scanning electron microscopy (Teixeira et al. 2014). To our best of our knowledge, few liter- ature reports have disclosed information on the physiological The morphological structure of acid treated and untreated changes of LAB due to acid stress, especially in L. plantarum. cells were examined using scanning electron microscopy Among a variety of LAB species, L. plantarum is one of (SEM). The samples were prepared as described by Bron themostwidelyusedstartersorprobioticsinmanyproducts et al. (2004), with some modifications. Briefly, cells were (Brinques and Ayub 2011). In our previous study, a strain of harvested by centrifugation at 5000 g for10minandfixed L. plantarum ZDY 2013 was proven to be an ideal probiotic in 2.5% (v/v) glutaraldehyde for 4 h at 4 °C. Subsequently, candidate because of its tolerance to the extreme environment the cells were washed three times with deionized water, of the gastrointestinal tract. Moreover, L. plantarum ZDY then dehydrated with ethanol by using 30%, 50%, 70%, 2013 underwent a global acid tolerance reaction in terms of 80% and 90% ethanol for one time, successively, and fi- mRNA levels (Huang et al. 2015), indicating that some un- nally with absolute ethyl ethanol for three times, and then known physiological changes takes place under extreme acid- freeze-dried. The samples were fixed on an aluminum foil ic conditions. To explore the acid stress mechanisms of and sprayed with gold. L. plantarum ZDY 2013 through a physiological response, we used the type strain of L. plantarum ATCC 8014 as a standard. In the present study, we investigated the acid toler- Measurement of membrane permeability ance ability, cell integrity, and changes in energy and amino acid metabolism based on the different acid stress responses of Membrane permeability was measured using the β- L. plantarum ZDY 2013 and L. plantarum ATCC 8014. galactosidase substrate o-nitrophenyl-β-D-galactopyranoside (ONPG) as a probe, which can be degraded by β-galacto- sidase to produce o-nitrophenol (yellow color) (Zhu et al. Materials and methods 2014). Cells were rinsed once by centrifugation (5000 g, 5min)andresuspendedin0.01MPBS(pH7.4)toanOD600 Bacteria strains, media, and growth conditions of 1.0, then ONPG was added to a final concentration of 1.5 mM. After incubation at 37 °C for 30 min, the cell suspen- L. plantarum ZDY 2013, isolated from a traditional fermented sion was monitored at 420 nm using a spectrophotometer acid beans in our previous study (Huang et al. 2015), and a (Precision and Scientific, Shanghai, China). Ann Microbiol (2017) 67:669–677 671 Measurement of Na+/K+-ATPase activity cooling for 10 min, the absorbance was measured at 460 nm. The standard curve for citrulline was determined by applying The Na+/K+-ATPase assay was carried out using the Na+/K+- the same procedure to five standard solutions of citrulline (0, ATPase assay kit (Suzhou Comin Biotechnology. Suzhou, 10, 20, 30 and 40 μg/mL). One unit of activity was defined as China) following the manufacturer’s protocol. The activity the amount of enzyme catalyzing the formation of 1 μmol of the Na+/K+-ATPase was expressed in Na+/K+-ATPase cat- citrulline per hour per milligram of total protein. Protein con- alyzing ATP and the formation of 1 μmol inorganic phospho- centration in the enzyme preparation was determined as de- rus per hour per milligram of total protein.
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