Thermotolerant Probiotic—The Potential of Improving the Survivability of Beneficial Bacteria
Abstract
1. Introduction
2. The Mechanism Underlying Heat Resistance in Beneficial Bacteria
3. Methods for Adapting Lactic Acid Bacterial Cells to High Temperatures
3.1. Environmental Stress
Method | Organism | Adaptation Conditions | Results | Reference |
---|---|---|---|---|
Environmental stress | Lactobacillus acidophilus NCFM | Initial selection for thermotolerance: incubation at 65 °C for 10, 15, 20, 25, 30, 35, and 40 min. | Heat challenge: 65 °C for 10, 15, 20, 25, 30, 35, and 40 min. At least a 1-log higher percent survival in comparison to wild-type L. acidophilus; survival ratio up to 1000-fold higher than wild type was achieved. | [29] |
Enterococcus faecium SFM1; SFM2 | Pasteurization—usually heated at 62.5 °C for 30 min or at 72–75 °C for 15 s(sic). | Heat challenge: 50 °C for 120 min. Heat-preadapted (pasteurized) E. faecium SFM1 and E. faecium SFM2 survived incubation at 50 °C for 2 h at rates of 28.20 ± 0.04% and 82.58 ± 0.01%, respectively. | [30] | |
Tetragenococcus halophilus CGMCC 3792 | 45 °C for 90 min in 10% skim milk, 30% skim milk, 10% sucrose, and 5% trehalose. | Heat challenge: 120 °C for an unspecified amount of time (spray drying). Survival increased in 10% skim milk, 30% skim milk, 10% sucrose, and 5% trehalose 3.71-, 1.96-, 1.69-, and 2.32-fold, respectively. Spray drying conditions (as specified in the paper): inlet/outlet temperature = 120/75 °C, volumetric airflow = 40 m3/h, feed rates = 7.5 mL/min, and atomizing pressure < −50 mbar. | [26] | |
Lactococcus lactis ssp. cremoris; Lactobacillus acidophilus NCFM; Lactobacillus rhamnosus GG. | Cultured at following temperatures: L. lactis, 33 °C; L. acidophilus, 42 °C; L. rhamnosus, 42 °C. | Heat challenge: 60 °C for 2, 4, 6, 8, 10, 12, and 14 min (L. cremoris); 60 °C for 6 min (L. rhamnosus); 60 °C for 4 min (L. acidophilus). Both L. cremoris and L. rhamnosus cultures showed increased survival rates compared to non-pretreated cultures. Preadapted L. acidophilus cultures showed lower survival rates than non-pretreated cultures. When L. acidophilus culture incubation time at preadaptation temperature (42 °C) was doubled (12 to 24 h), survival rates increased (from 60.1% to 63.7%), but viability decreased (from 8.2 to 6.8 log CFU/mL). | [31] | |
Lactobacillus casei Zhang; Lactobacillus plantarum P8; Lactobacillus rhamnosus GG; Lactobacillus casei BL23. | Reconstituted milk powder; total solids contents of 5.0, 10.0, 20.0, 25.0, 30.0, 35.0, and 40.0 wt%; stationary incubation at 37 °C for 36 h. | Heat challenge: 65 °C or 70 °C for 10 min. Reconstituted skim milk with 20–30 wt% solid content proved most efficient in increasing survival rates of heat-challenged LAB. | [27] | |
Environmental stress | Lactobacillus plantarum KLDS 1.0628 | 45 °C for 1 h, 15 °C for 1 h; 1 mmol/L H2O2 for 1 h at 37 °C; pH 4.0 for 1 h at 37 °C; 0.2% bile salt for 1 h at 37 °C; and 2% NaCl for 1 h at 37 °C. | Heat challenge: 60 °C for 1 h. Heat preadaptation proved most effective—heat tolerance of preadapted bacteria increased 31.38-fold in comparison to non-preadapted cells. | [32] |
Tetragenococcus halophilus CGMCC 3792 | 45 °C for 1.5 h | Heat challenge: 60 °C for 2.5 h. Thermotolerance increased 18-fold. | [23] | |
Lactococcus lactis ssp. cremoris; Lactobacillus acidophilus NCFM | Media supplementation with CaCl2. | Heat challenge: 97 +/− 5 °C for an unspecified amount of time (spray-drying). Both L. lactis and L. acidophilus grown with 10 mM CaCl2 showed enhanced thermotolerance with increased spray-drying survival rates from 49.9% to 64.9% and 35.5% to 43.3%, respectively. Spray-drying conditions (as specified in the paper): […] inlet and out temperatures were controlled at 97 +/− 5 and 58 +/− 2 °C. Mass flow rate was around 0.85 +/− 0.08 g/min. | [28] | |
Enterococcus faecium HL7 | 15 min at 52 °C; exposure to sublethal levels of acid (pH 5.0 for 30 min). | Heat challenge: 60 °C for 40 min. Heat-adapted E. faecium survival rate was 103–105-fold higher than that of non-pretreated culture. Acid-adapted E. faecium survival rate was 17-fold higher than that of non-pretreated culture; cell viability equaled 92.73% and 5.19%, respectively. | [24] | |
Lactobacillus rhamnosus hsryfm 1301 | Pretreatment under 50 °C(sic); 0.5 mM H2O2 for 1 h. | Heat challenge: 54 °C for 60 min. 0.5 mM H2O2-pretreated L. rhamnosus survival rates increased from approximately 5.5 Lg(CFU/mL) to approx. 7.8 Lg(CFU/mL). Heat-pretreated L. rhamnosus survival rates increased from approximately 5.5 Lg(CFU/mL) to approx. 7.5 Lg(CFU/mL). | [33] | |
Lactobacillus kefiranofaciens M1 | 37 °C for 1 h, 20 °C for 1 h, pH 5.0 for 1 h at 30 °C, and 0.05% bile salts for 1 h at 30 °C. | Heat challenge: 52 °C for 2 h. Heat challenge survival rates were the highest in heat-adapted cells (0.21%), followed by bile salt- adapted cells (0.18%) then acid-adapted cells (0.07%). | [34] | |
Environmental stress | Lactiplantibacillus plantarum Lp 790; Lp 813; Lp 998 | 45 °C for 30 min. | Heat challenge: 52 °C for 15 min. Thermal adaptation (30 min) clearly improved cell resistance against thermal shock. | [35] |
Lactobacillus sanfranciscensis DSM 20451T | 1.9% NaCl at 30 °C; pH 3.7 at 30 °C; 80 MPa at 30 °C; 43 °C and 12.5 °C. | Heat challenge: 50 °C for 30 min. Application of sublethal high pressure (80 MPa) pretreatment resulted in increased heat resistance (3.6-fold). | [25] | |
Adaptative Laboratory Evolution | L. lactis ssp. lactis bv. diacetylactis SD96. | ALE performed for 400 generations: 67 generations at 39 °C; 83 at 40 °C; and 250 generations at 41 °C. | Strains RD01 (150th generation isolate) and RD07 (400th generation isolate) acidified milk faster than parent strain at 30 °C and 37 °C; RD01 acidified milk 1.7-fold slower than RD07 at 40 °C; only RD07 strain could acidify milk at 41 °C. | [36] |
Lacticaseibacillus casei N; Lactobacillus helveticus NRRL B-4526 | 500 generations cultured at 45 °C. | Biomass increased two-fold when grown at 45 °C in both studied strains. Continued ALE by subculturing at 47 °C for 300 generations, 50 °C for 20 generations, and 55 °C for 10 generations resulted in decreased biomass; not studied further. | [37] | |
L. acidophilus EG004 | 60 °C for 1 min, then cultivation at 37 °C for 24 h; process repeated twice; identical procedure repeated with rising temperature in increments of 3 °C. Repeated in ranges from 60 °C to 72 °C. | Newly developed L. acidophilus EG008 showed improved thermal resistance (in comparison to L. acidophilus EG004), understood as survival rates in temperatures from 65 °C to 75 °C. | [38] | |
Lactobacillus delbrueckii ssp. bulgaricus ET45 | Cultivation temperature was raised from 37 °C to 40 °C in increments of 1 °C and then from 40 °C to 45 °C in increments of 0.2 °C. ALE consisted of 68 passages. | Newly developed L. bulgaricus strain was able to perform simultaneous saccharification and fermentation at 45 °C. | [39] | |
Adaptative Laboratory Evolution | Enterococcus faecium BIOPOP-3 | Screening for thermotolerant bacteria by thermal adaptation starting at 60 °C, rising in increments of 3 °C, then ALE: heat challenge at 75 °C, then cultivation at 37 °C for 24 h, repeated for 25 days. | Newly developed Enterococcus faecium BIOPOP-3 ALE strain showed 75.85% survival rate compared to ~5% survival rate of wild type and heat-preadapted strain. | [40] |
Genetic modification | Streptococcus thermophilus sp. | Transformation of shsp gene-containing plasmid into S. thermophilus cells deprived of or lacking shsp gene. | Heat challenge: 60 °C for 60 min. Presence of shsp encoding plasmid increased resistance to heat challenge and allowed for growth at 52 °C in different S. thermophilus strains. The shsp gene codes for small heat-shock protein and is present on S. thermophilus plasmid pSt04. | [41] |
Lactobacillus plantarum WCFS1 | Transient overproduction of hsp 18.5, hsp 18.55, and hsp 19.3 genes. | Heat challenge: 40 °C and 37 °C for 14 h. Unmodified strain viability decreased after heat challenge (~3 log CFU/mL at 37 °C and ~4 log CFU/mL at 40 °C after 14 h); recombinant strain viability was almost unchanged (≤0.2 log CFU/mL and ≤0.5 log CFU/mL, respectively). The hsp 18.5, hsp 18.55, and hsp 19.3 genes code for heat-shock proteins (HSPs) HSP 18.5, HSP 18.55, and HSP 19.3, respectively. | [42] | |
Lactobacillus salivarius Ren | Homologous overexpression of oppA gene. | Heat challenge: 55 °C for 1 h. Recombinant L. salivarius Ren displayed higher resistance than unmodified strain: A 4 log CFU/mL viability increase was observed (6 log CFU/mL compared to 2 log CFU/mL). The oppA gene codes for a transport protein involved in oligopeptide uptake. | [43] | |
Lactococcus lactis ssp. cremoris NZ9000 | The uvrA gene overexpression. | Heat challenge: 46 °C for 6 h. UvrA-overexpressing strain survival rate increased 1.22-fold in comparison to non-overexpressing strain. Gene uvrA codes for a protein involved in DNA repair, replication, and recombination. | [44] |
3.2. Adaptive Laboratory Evolution
3.3. Genetic Manipulation
4. Application of Thermotolerant Beneficial Microorganisms in Food Technology and Industry
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Wang, H.; Wei, C.X.; Min, L.; Zhu, L.Y. Good or Bad: Gut Bacteria in Human Health and Diseases. Biotechnol. Biotechnol. Equip. 2018, 32, 1075–1080. [Google Scholar] [CrossRef]
- Mazziotta, C.; Tognon, M.; Martini, F.; Torreggiani, E.; Rotondo, J.C. Probiotics Mechanism of Action on Immune Cells and Beneficial Effects on Human Health. Cells 2023, 12, 184. [Google Scholar] [CrossRef] [PubMed]
- NIH Human Microbiome Project—About the Human Microbiome. Available online: https://www.hmpdacc.org/hmp/overview/ (accessed on 20 May 2025).
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S. The International Scientific Association for Probiotics and Prebiotics Consensus Statement on the Scope and Appropriate Use of the Term Probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [Google Scholar] [CrossRef] [PubMed]
- Sionek, B.; Szydłowska, A.; Zielińska, D.; Neffe-Skocińska, K.; Kołożyn-Krajewska, D. Beneficial Bacteria Isolated from Food in Relation to the next Generation of Probiotics. Microorganisms 2023, 11, 1714. [Google Scholar] [CrossRef]
- Yang, H.; He, M.; Wu, C. Cross Protection of Lactic Acid Bacteria during Environmental Stresses: Stress Responses and Underlying Mechanisms. LWT 2021, 144, 111203. [Google Scholar] [CrossRef]
- Varmanen, P.; Savijoki, K. Responses of Lactic Acid Bacteria to Heat Stress. In Stress Responses of Lactic Acid Bacteria; Springer: Boston, MA, USA, 2011; pp. 55–66. [Google Scholar]
- Papadimitriou, K.; Alegria, A.; Bron, P.A.; Angelis, M.; Gobbetti, M.; Kleerebezem, M.; Lemos, J.A.; Linares, D.M.; Ross, P.; Stanton, C. Stress Physiology of Lactic Acid Bacteria. Microbiol. Mol. Biol. Res. 2016, 80, 837–890. [Google Scholar] [CrossRef]
- Yamamori, T.; Ito, K.; Yura, T.; Suzuki, T.; Iino, T. Ribonucleic Acid Polymerase Mutant of Escherichia coli Defective in Flagella Formation. J. Bacteriol. 1977, 132, 254–261. [Google Scholar] [CrossRef]
- Arsène, F.; Tomoyasu, T.; Bukau, B. The heat shock response of Escherichia coli. Int. J. Food Microbiol. 2000, 55, 3–9. [Google Scholar] [CrossRef]
- Zhao, N.; Yu, T.; Yan, F. Probiotic Role and Application of Thermophilic Bacillus as Novel Food Materials. Trends Food Sci. Technol. 2023, 138, 1–15. [Google Scholar] [CrossRef]
- Darmon, E.; Noone, D.; Masson, A.; Bron, S.; Kuipers, O.P.; Devine, K.M.; Dijl, J.M.V. A Novel Class of Heat and Secretion Stress-Responsive Genes Is Controlled by the Autoregulated CssRS Two-Component System of Bacillus Subtilis. J. Bacteriol. 2002, 184, 5661–5671. [Google Scholar] [CrossRef]
- Mansilla, M.C.; Cybulski, L.E.; Albanesi, D.; Mendoza, D. Control of Membrane Lipid Fluidity by Molecular Thermosen-Sors. J. Bacteriol. 2004, 186, 6681–6688. [Google Scholar] [CrossRef] [PubMed]
- Konings, W.N.; Albers, S.V.; Koning, S.; Driessen, A.J. The Cell Membrane Plays a Crucial Role in Survival of Bacteria and Archaea in Extreme Environments. Antonie Van. Leeuwenhoek 2002, 81, 61–72. [Google Scholar] [CrossRef] [PubMed]
- Rezanka, T.; Siristova, L.; Melzoch, K.; Sigler, K. Hopanoids in Bacteria and Cyanobacteria-Their Role in Cellular Biochemistry and Physiology, Analysis and Occurrence. Mini-Rev. Org. Chem. 2010, 7, 300–313. [Google Scholar] [CrossRef]
- Kathiriya, M.R.; Vekariya, Y.V.; Hati, S. Understanding the Probiotic Bacterial Responses Against Various Stresses in Food Ma-Trix and Gastrointestinal Tract: A Review. Probiotics Antimicro Prot. 2023, 15, 1032–1048. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, H.T.; Razafindralambo, H.; Blecker, C.; N’Yapo, C.; Thonart, P.; Delvigne, F. Stochastic Exposure to Sub-Lethal High Tem-Perature Enhances Exopolysaccharides (EPS) Excretion and Improves Bifidobacterium Bifidum Cell Survival to Freeze–Drying. Bio-Chem. Eng. J. 2014, 88, 85–94. [Google Scholar]
- Angelis, M.; Cagno, R.; Huet, C.; Crecchio, C.; Fox, P.F.; Gobbetti, M. Heat Shock Response in Lactobacillus Plantarum. Ap-Plied Environ. Microbiol. 2004, 70, 1336–1346. [Google Scholar] [CrossRef]
- Russo, P.; Luz Mohedano, M.; Capozzi, V.; Palencia, P.F.; López, P.; Spano, G.; Fiocco, D. Comparative Proteomic Analysis of Lactobacillus Plantarum WCFS1 and Δ ctsR Mutant Strains under Physiological and Heat Stress Conditions. Int. J. Mol. Sci. 2012, 13, 10680–10696. [Google Scholar] [CrossRef]
- Khaskheli, G.B.; Zuo, F.; Yu, R.; Chen, S. Overexpression of Small Heat Shock Protein Enhances Heat- and Salt-Stress Tolerance of Bifidobacterium Longum NCC2705. Curr. Microbiol. 2015, 71, 8–15. [Google Scholar] [CrossRef]
- Haddaji, N.; Mahdhi, A.K.; Krifi, B.; Ismail, M.B.; Bakhrouf, A. Change in Cell Surface Properties of Lactobacillus Casei under Heat Shock Treatment. FEMS Microbiol. Lett. 2015, 362, fnv047. [Google Scholar] [CrossRef]
- Pandi, S.; Basheer, S. Adaptation of Lactobacillus sp. and Saccharomyces sp. to Heat Stress. Int. J. Microbiol. Allied Sci. 2016, 283, 7–16. [Google Scholar]
- Yang, H.; Yao, S.; Zhang, M.; Wu, C. Heat Adaptation Induced Cross Protection Against Ethanol Stress in Tetragenococcus halophilus: Physiological Characteristics and Proteomic Analysis. Front. Microbiol. 2021, 12, 686672. [Google Scholar] [CrossRef] [PubMed]
- Shin, Y.; Kang, C.-H.; Kim, W.; So, J.-S. Heat Adaptation Improved Cell Viability of Probiotic Enterococcus Faecium HL7 upon Various Environmental Stresses. Probiotics Antimicrob. Proteins 2019, 11, 618–626. [Google Scholar] [CrossRef]
- Scheyhing, C.H.; Hörmann, S.; Ehrmann, M.A.; Vogel, R.F. Barotolerance Is Inducible by Preincubation under Hydrostatic Pressure, Cold-, Osmotic- and Acid-Stress Conditions in Lactobacillus Sanfranciscensis DSM 20451T. Lett. Appl. Microbiol. 2004, 39, 284–289. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Huang, P.; Hao, L.; Che, Y.; Dong, S.; Wang, Z.; Wu, C. Enhancing Viability of Dried Lactic Acid Bacteria Prepared by Freeze Drying and Spray Drying via Heat Preadaptation. Food Microbiol. 2023, 112, 104239. [Google Scholar] [CrossRef]
- Suo, X.; Huang, S.; Wang, J.; Fu, N.; Jeantet, R.; Chen, X.D. Effect of Culturing Lactic Acid Bacteria with Varying Skim Milk Concentration on Bacteria Survival during Heat Treatment. J. Food Eng. 2021, 294, 110396. [Google Scholar] [CrossRef]
- Wang, Y.; Hao, F.; Lu, W.; Suo, X.; Bellenger, E.; Fu, N.; Jeantet, R.; Chen, X.D. Enhanced Thermal Stability of Lactic Acid Bacteria during Spray Drying by Intracellular Accumulation of Calcium. J. Food Eng. 2020, 279, 109975. [Google Scholar] [CrossRef]
- Kulkarni, S.; Haq, S.F.; Samant, S.; Sukumaran, S. Adaptation of Lactobacillus Acidophilus to Thermal Stress Yields a Thermotolerant Variant Which Also Exhibits Improved Survival at pH 2. Probiotics Antimicrob. Proteins 2018, 10, 717–727. [Google Scholar] [CrossRef]
- Zhao, J.; Gong, J.; Liang, W.; Zhang, S. Microbial Diversity Analysis and Isolation of Thermoresistant Lactic Acid Bacteria in Pasteurized Milk. Sci. Rep. 2024, 14, 29705. [Google Scholar] [CrossRef]
- Hao, F.; Fu, N.; Ndiaye, H.; Woo, M.W.; Jeantet, R.; Chen, X.D. Thermotolerance, Survival, and Stability of Lactic Acid Bacteria After Spray Drying as Affected by the Increase of Growth Temperature. Food Bioprocess Technol. 2021, 14, 120–132. [Google Scholar] [CrossRef]
- Ma, J.; Xu, C.; Liu, F.; Hou, J.; Shao, H.; Yu, W. Stress Adaptation and Cross-Protection of Lactobacillus Plantarum KLDS 1.0628. CyTA—J. Food 2021, 19, 72–80. [Google Scholar] [CrossRef]
- Zhang, C.; Lu, J.; Yang, D.; Chen, X.; Huang, Y.; Gu, R. Stress Influenced the Aerotolerance of Lactobacillus Rhamnosus Hsryfm 1301. Biotechnol. Lett. 2018, 40, 729–735. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.-J.; Tang, H.-Y.; Chiang, M.-L. Effects of Heat, Cold, Acid and Bile Salt Adaptations on the Stress Tolerance and Protein Expression of Kefir-Isolated Probiotic Lactobacillus kefiranofaciens M1. Food Microbiol. 2017, 66, 20–27. [Google Scholar] [CrossRef]
- Ferrando, V.; Quiberoni, A.; Reinhemer, J.; Suárez, V. Resistance of Functional Lactobacillus plantarum Strains against Food Stress Conditions. Food Microbiol. 2015, 48, 63–71. [Google Scholar] [CrossRef]
- Dorau, R.; Chen, J.; Liu, J.; Ruhdal Jensen, P.; Solem, C. Adaptive Laboratory Evolution as a Means To Generate Lactococcus Lactis Strains with Improved Thermotolerance and Ability To Autolyze. Appl. Environ. Microbiol. 2021, 87, e01035-21. [Google Scholar] [CrossRef]
- Bommasamudram, J.; Kumar, P.; Kapur, S.; Sharma, D.; Devappa, S. Development of Thermotolerant Lactobacilli Cultures with Improved Probiotic Properties Using Adaptive Laboratory Evolution Method. Probiotics Antimicrob. Proteins 2023, 15, 832–843. [Google Scholar] [CrossRef] [PubMed]
- Jeon, S.; Kim, H.; Choi, Y.; Cho, S.; Seo, M.; Kim, H. Complete Genome Sequence of the Newly Developed Lactobacillus Acidophilus Strain With Improved Thermal Adaptability. Front. Microbiol. 2021, 12, 697351. [Google Scholar] [CrossRef] [PubMed]
- Vishnu Prasad, J.; Sahoo, T.K.; Naveen, S.; Jayaraman, G. Evolutionary Engineering of Lactobacillus Bulgaricus Reduces Enzyme Usage and Enhances Conversion of Lignocellulosics to D-Lactic Acid by Simultaneous Saccharification and Fermentation. Biotechnol. Biofuels 2020, 13, 171. [Google Scholar] [CrossRef] [PubMed]
- Min, B.; Yoo, D.; Lee, Y.; Seo, M.; Kim, H. Complete Genomic Analysis of Enterococcus Faecium Heat-Resistant Strain Developed by Two-Step Adaptation Laboratory Evolution Method. Front. Bioeng. Biotechnol. 2020, 8, 828. [Google Scholar] [CrossRef]
- El Demerdash, H.A.M.; Heller, K.J.; Geis, A. Application of the Shsp Gene, Encoding a Small Heat Shock Protein, as a Food-Grade Selection Marker for Lactic Acid Bacteria. Appl. Environ. Microbiol. 2003, 69, 4408–4412. [Google Scholar] [CrossRef]
- Fiocco, D.; Capozzi, V.; Goffin, P.; Hols, P.; Spano, G. Improved Adaptation to Heat, Cold, and Solvent Tolerance in Lactobacillus Plantarum. Appl. Microbiol. Biotechnol. 2007, 77, 909–915. [Google Scholar] [CrossRef]
- Wang, G.; Li, D.; Ma, X.; An, H.; Zhai, Z.; Ren, F.; Hao, Y. Functional Role of oppA Encoding an Oligopeptide-Binding Protein from Lactobacillus Salivarius Ren in Bile Tolerance. J. Ind. Microbiol. Biotechnol. 2015, 42, 1167–1174. [Google Scholar] [CrossRef] [PubMed]
- Moghaddam, T.K.; Zhang, J.; Du, G. UvrA Expression of Lactococcus Lactis NZ9000 Improve Multiple Stresses Tolerance and Fermentation of Lactic Acid against Salt Stress. J. Food Sci. Technol. 2017, 54, 639–649. [Google Scholar] [CrossRef] [PubMed]
- Dragosits, M.; Mattanovich, D. Adaptive Laboratory Evolution—Principles and Applications for Biotechnology. Microb. Cell Factories 2013, 12, 64. [Google Scholar] [CrossRef] [PubMed]
- Derunets, A.S.; Selimzyanova, A.I.; Rykov, S.V.; Kuznetsov, A.E.; Berezina, O.V. Strategies to Enhance Stress Tolerance in Lactic Acid Bacteria across Diverse Stress Conditions. World J. Microbiol. Biotechnol. 2024, 40, 126. [Google Scholar] [CrossRef]
- Johansen, E. Future Access and Improvement of Industrial Lactic Acid Bacteria Cultures. Microb. Cell Factories 2017, 16, 230. [Google Scholar] [CrossRef]
- Gao, H.; Li, X.; Chen, X.; Hai, D.; Wei, C.; Zhang, L.; Li, P. The Functional Roles of Lactobacillus Acidophilus in Different Physiological and Pathological Processes. J. Microbiol. Biotechnol. 2022, 32, 1226–1233. [Google Scholar] [CrossRef]
- Zhao, L.; Liu, S.; Li, M.; Lee, J.H.; Zhu, Y.; Liang, D.; Zhi, H.; Ding, Q.; Zhao, G.; Ma, Y.; et al. Bibliometric Analysis of Probiotic Bacillus in Food Science: Evolution of Research Trends and Systematic Evaluation. Probiotics Antimicrob. Proteins 2025. [Google Scholar] [CrossRef]
- Kim, Y.S.; Lee, J.; Heo, S.; Lee, J.H.; Jeong, D.W. Technology and Safety Evaluation of Bacillus coagulans Exhibiting Antimi-Crobial Activity for Starter Development. LWT 2021, 137, 110464. [Google Scholar] [CrossRef]
- Cizeikiene, D.; Jagelaviciute, J.; Stankevicius, M.; Maruska, A. Thermophilic Lactic Acid Bacteria Affect the Characteristics of Sourdough and Whole-Grain Wheat Bread. Food Biosci. 2020, 38, 100791. [Google Scholar] [CrossRef]
- Almada-Érix, C.N.; Almada, C.N.; Pedrosa, G.T.S.; Biachi, J.P.; Bonatto, M.S.; Schmiele, M.; Nabeshima, E.H.; Clerici, M.T.P.; Magnani, M.; Sant’Ana, A.S. Bread as Probiotic Carriers: Resistance of Bacillus coagulans GBI-30 6086 Spores through Processing Steps. Food Res. Int. 2022, 155, 111040. [Google Scholar] [CrossRef]
- Majeed, M.; Majeed, S.; Nagabhushanam, K.; Arumugam, S.; Beede, K.; Ali, F. Evaluation of Probiotic Bacillus coagulans MTCC 5856 Viability after Tea and Coffee Brewing and Its Growth in GIT Hostile Environment. Food Res. Int. 2019, 121, 497–505. [Google Scholar] [CrossRef] [PubMed]
- Bull, M.; Plummer, S.; Marchesi, J.; Mahenthiralingam, E. The Life History of Lactobacillus Acidophilus as a Probiotic: A Tale of Revisionary Taxonomy, Misidentification and Commercial Success. FEMS Microbiol. Lett. 2013, 349, 77–87. [Google Scholar] [CrossRef]
- Slattery, L.; O’Callaghan, J.; Fitzgerald, G.F.; Beresford, T.; Ross, R.P. Invited Review: Lactobacillus helveticus—A Thermophilic Dairy Starter Related to Gut Bacteria. J. Dairy Sci. 2021, 93, 4435–4454. [Google Scholar] [CrossRef]
- Helinck, S.; Le Bars, D.; Moreau, D.; Yvon, M. Ability of Thermophilic Lactic Acid Bacteria to Produce Aroma Compounds from Amino Acids. Appl. Environ. Microbiol. 2004, 70, 3855–3861. [Google Scholar] [CrossRef]
- Ma, S.; Cao, J.; Liliu, R.; Li, N.; Zhao, J.; Zhang, H.; Chen, W.; Zhai, Q. Effects of Bacillus coagulans as an Adjunct Starter Culture on Yogurt Quality and Storage. J. Dairy. Sci. 2021, 104, 7466–7479. [Google Scholar] [CrossRef]
- Marcial-Coba, M.S.; Pjaca, A.S.; Andersen, C.J.; Knøchel, S.; Nielsen, D.S. Dried Date Paste as Carrier of the Proposed Probiotic Bacillus coagulans BC4 and Viability Assessment during Storage and Simulated Gastric Passage. LWT 2019, 99, 197–201. [Google Scholar] [CrossRef]
- Villalobos, M.C.; Serradilla, M.J.; Martín, A.; Pereira, C.; López-Corrales, M.; Córdoba, M.G. Evaluation of Different Drying Systems as an Alternative to Sun Drying for Figs (Ficus carica L.). Innov. Food Sci. Emerg. Technol. 2016, 36, 156–165. [Google Scholar] [CrossRef]
- He, H.; Yu, Q.; Ding, Z.; Zhang, L.; Shi, G.; Li, Y. Biotechnological and Food Synthetic Biology Potential of Platform Strain: Bacillus Licheniformis. Synth. Syst. Biotechnol. 2023, 8, 281–291. [Google Scholar] [CrossRef] [PubMed]
- Ohair, J.; Jin, Q.; Yu, D.; Wu, J.; Huang, H. Non-sterile fermentation of food waste using thermophilic and alkaliphilic Bacillus licheniformis YNP5-TSU for 2,3-butanediol production. Waste Manag. 2021, 120, 248–256. [Google Scholar] [CrossRef]
- Ghosh, A.; Sutradhar, S.; Baishya, D. Delineating Thermophilic Xylanase from Bacillus Licheniformis DM5 towards Its Po-Tential Application in Xylooligosaccharides Production. World J. Microbiol. Biotechnol. 2019, 35, 34. [Google Scholar] [CrossRef]
- Yan, Z.; Zheng, X.W.; Han, B.Z.; Yan, Y.Z.; Zhang, X.; Chen, J.Y. 1H NMR-Based Metabolomics Approach for under-Standing the Fermentation Behaviour of Bacillus Licheniformis. J. Inst. Brew. 2015, 121, 425–431. [Google Scholar] [CrossRef]
- Voigt, B.; Schroeter, R.; Schweder, T.; Jürgen, B.; Albrecht, D.; van Dijl, J.M.; Maurer, K.H.; Hecker, M. A Proteomic View of Cell Physiology of the Industrial Workhorse Bacillus Licheniformis. J. Biotechnol. 2014, 191, 139–149. [Google Scholar] [CrossRef] [PubMed]
- Zhao, S.; Dorau, R.; Tømmerholt, L.; Gu, L.; Tadesse, B.T.; Zhao, G.; Solem, C. Simple & Better–Accelerated Cheese Ripening Using a Mesophilic Starter Based on a Single Strain with Superior Autolytic Properties. Int. J. Food Microbiol. 2023, 407, 110398. [Google Scholar]
- Zhang, C.; Yang, L.; Gu, R.; Ding, Z.; Guan, C.; Lu, M.; Gu, R. Mild Heat Stress Limited the Post-Acidification Caused by Lactobacillus Rhamnosus Hsryfm 1301 in Fermented Milk. Biotechnol. Lett. 2019, 41, 633–639. [Google Scholar] [CrossRef]
- Pérez-Chabela, M.D.L.; Totosaus, A.; Guerrero, I. Evaluation of Thermotolerant Capacity of Lactic Acid Bacteria Isolated from Com-Mercial Sausages and the Effects of Their Addition on the Quality of Cooked Sausages. Ciênc. Tecnol. Aliment. Camp. 2008, 28, 132–138. [Google Scholar] [CrossRef]
- Bommasamudram, J.; Muthu, A.; Devappa, S. Effect of Prebiotics on Thermally Acclimatized Lactobacilli Cultures and Their Application as Synbiotics in RTD Fruit Drinks. 3 Biotech 2023, 13, 311. [Google Scholar] [CrossRef]
- Lestari, S.D.; Rinto, R.; Wahyuni, I.S.; Ridhowati, S.; Wulandari, W. Heat Resistance of Probiotic Candidate Enterococcus Faecalis R22B in Different Matrices. Squalen Bull. Mar. Fish. Postharvest Biotechnol. 2021, 16, 19–27. [Google Scholar] [CrossRef]
- Pitiwittayakul, N.; Bureenok, S.; Schonewille, J.T. Selective Thermotolerant Lactic Acid Bacteria Isolated from Fermented Juice of Epiphytic Lactic Acid Bacteria and Their Effects on Fermentation Quality of Stylo Silages. Front. Microbiol. 2021, 12, 673946. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zielińska, D.; Krawczyk, M.; Neffe-Skocińska, K. Thermotolerant Probiotic—The Potential of Improving the Survivability of Beneficial Bacteria. Fermentation 2025, 11, 313. https://doi.org/10.3390/fermentation11060313
Zielińska D, Krawczyk M, Neffe-Skocińska K. Thermotolerant Probiotic—The Potential of Improving the Survivability of Beneficial Bacteria. Fermentation. 2025; 11(6):313. https://doi.org/10.3390/fermentation11060313
Chicago/Turabian StyleZielińska, Dorota, Miłosz Krawczyk, and Katarzyna Neffe-Skocińska. 2025. "Thermotolerant Probiotic—The Potential of Improving the Survivability of Beneficial Bacteria" Fermentation 11, no. 6: 313. https://doi.org/10.3390/fermentation11060313
APA StyleZielińska, D., Krawczyk, M., & Neffe-Skocińska, K. (2025). Thermotolerant Probiotic—The Potential of Improving the Survivability of Beneficial Bacteria. Fermentation, 11(6), 313. https://doi.org/10.3390/fermentation11060313