Cited by 916Probiotics and Fermented FoodsBacterial Genetics and BiotechnologyMicrobial Inactivation Methods

The DOI matches its Crossref record; 647 of the 647 references it cites were found in a registry or an index.

Stress Physiology of Lactic Acid Bacteria.

Open access

Papadimitriou, Konstantinos, Alegría, Ángel, Bron, Peter A., de Angelis, Maria, Gobbetti, Marco, Kleerebezem, Michiel, Lemos, José A., Linares, Daniel M., Ross, Paul, Stanton, Catherine, Turroni, Francesca, van Sinderen, Douwe, Varmanen, Pekka, Ventura, Marco, Zúñiga, Manuel, Tsakalidou, Effie, Kok, Jan·2016·Microbiology and Molecular Biology Reviews

DOI 10.1128/mmbr.00076-15PMC PMC4981675

Open this paper in CoChat — free account Open PDF

Abstract

Lactic acid bacteria (LAB) are important starter, commensal, or pathogenic microorganisms. The stress physiology of LAB has been studied in depth for over 2 decades, fueled mostly by the technological implications of LAB robustness in the food industry. Survival of probiotic LAB in the host and the potential relatedness of LAB virulence to their stress resilience have intensified interest in the field. Thus, a wealth of information concerning stress responses exists today for strains as diverse as starter (e.g., Lactococcus lactis), probiotic (e.g., several Lactobacillus spp.), and pathogenic (e.g., Enterococcus and Streptococcus spp.) LAB. Here we present the state of the art for LAB stress behavior. We describe the multitude of stresses that LAB are confronted with, and we present the experimental context used to study the stress responses of LAB, focusing on adaptation, habituation, and cross-protection as well as on self-induced multistress resistance in stationary phase, biofilms, and dormancy. We also consider stress responses at the population and single-cell levels. Subsequently, we concentrate on the stress defense mechanisms that have been reported to date, grouping them according to their direct participation in preserving cell energy, defending macromolecules, and protecting the cell envelope. Stress-induced responses of probiotic LAB and commensal/pathogenic LAB are highlighted separately due to the complexity of the peculiar multistress conditions to which these bacteria are subjected in their hosts. Induction of prophages under environmental stresses is then discussed. Finally, we present systems-based strategies to characterize the "stressome" of LAB and to engineer new food-related and probiotic LAB with improved stress tolerance.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1128/mmbr.00076-15

Cites

647 of 647 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Random Forests
Breiman, L. (2001) · Machine Learning · doi:10.1023/a:1010933404324 · Cited by 133,538
Whole-Genome Random Sequencing and Assembly of Haemophilus influenzae Rd
Fleischmann, R. D., Adams, M. D., White, O. R., Clayton, R. A., Kirkness, E. F., Kerlavage, A. R., Bult, C. J., Tomb, J.-F., Dougherty, B. A., Merrick, J. M., et al. (1995) · Science · doi:10.1126/science.7542800 · Cited by 5,731
DNA Repair and Mutagenesis
Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (2005) · doi:10.1128/9781555816704 · Cited by 5,683
Two-Component Signal Transduction
Stock, A., Robinson, V. L., & Goudreau, P. N. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.183 · Cited by 3,653
The human microbiome: at the interface of health and disease
Cho, I., & Blaser, M. J. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3182 · Cited by 3,449
Guidelines for the evaluation of probiotics in food
Who, F. (2002) · Medical Entomology and Zoology · Cited by 1,843
Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger
Römling, U., Galperin, M. Y., & Gomelsky, M. (2013) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00043-12 · Cited by 1,726
Complete genome sequence of Lactobacillus plantarum WCFS1
Kleerebezem, M., Boekhorst, J., van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., Tarchini, R., Peters, S. A., Sandbrink, H. M., Fiers, M. W. E. J., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337704100 · Cited by 1,472
Self-citation
Surviving the Acid Test: Responses of Gram-Positive Bacteria to Low pH
Cotter, P. D., & Hill, C. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.3.429-453.2003 · Cited by 1,427
Comparative genomics of the lactic acid bacteria.
Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607117103 · Cited by 1,391

Show all 646 references

Research works printed but not linked: 3

Henick-Kling T, Cox DJ, Olsen EB. 1991. Production de l'energie durant la fermentation malolactique. Rev Fr Oenol 132:63–66.
Aprea G, Mullan WMA, Mullan A, Murru N, Tozzi M, Cortesi ML. 2005. Isolation of polyphosphate-accumulating lactic acid bacteria from natural whey starters. Milchwissenschaft 60:256–258.
Lim B, Gross CA. 2011. Cellular response to heat shock and cold shock, p 93–114. In Storz G, Hengge R (ed), Bacterial stress responses, 2nd ed. ASM Press, Washington, DC.

Sorted by citations

Metabolism Characteristics of Lactic Acid Bacteria and the Expanding Applications in Food Industry
Wang, Y., Wu, J., Lv, M., Shao, Z., Hungwe, M., Wang, J., Bai, X., Xie, J., Wang, Y., & Geng, W. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.612285 · Cited by 1,001
Microbial Fermentation and Its Role in Quality Improvement of Fermented Foods
Sharma, R., Garg, P., Kumar, P., Bhatia, S. K., & Kulshrestha, S. (2020) · Fermentation · doi:10.3390/fermentation6040106 · Cited by 824
The Lactobacillus casei group: history and health related applications
Hill, D., Sugrue, I., Tobin, C., Hill, C., Stanton, C., & Ross, R. P. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02107 · Cited by 318
Self-citation
Tumor-resident Lactobacillus iners confer chemoradiation resistance through lactate-induced metabolic rewiring
Colbert, L. E., Alam, M. B. E., Wang, R., Karpinets, T. V., Lo, D., Lynn, E. J., Harris, T. A., Elnaggar, J. H., Yoshida-Court, K., Tomasic, K., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.09.012 · Cited by 286
Bacterial exopolysaccharides as emerging bioactive macromolecules: from fundamentals to applications
Kaur, N., & Dey, P. (2022) · Research in Microbiology · doi:10.1016/j.resmic.2022.104024 · Cited by 285
Exopolysaccharide production by lactic acid bacteria: the manipulation of environmental stresses for industrial applications
Nguyen, P.-T., Nguyen, T.-T., Bui, D., Hong, P.-T., Hoang, Q.-K., & Nguyen, H. (2020) · AIMS Microbiology · doi:10.3934/microbiol.2020027 · Cited by 279
Probiotic strains detect and suppress cholera in mice
Mao, N., Cubillos-Ruiz, A., Cameron, D. E., & Collins, J. J. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aao2586 · Cited by 272
Ecological succession and functional characteristics of lactic acid bacteria in traditional fermented foods
Wang, Y., Zhang, C., Liu, F., Jin, Z., & Xia, X. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.2025035 · Cited by 223
Lactic acid bacteria: from starter cultures to producers of chemicals
Hatti‐Kaul, R., Chen, L., Dishisha, T., & Enshasy, H. A. E. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny213 · Cited by 214
Biotechnological advances in lactic acid production by lactic acid bacteria: lignocellulose as novel substrate
Cubas‐Cano, E., González‐Fernández, C., Ballesteros, M., & Tomás‐Pejó, E. (2018) · Biofuels Bioproducts and Biorefining · doi:10.1002/bbb.1852 · Cited by 199
Quorum sensing for population-level control of bacteria and potential therapeutic applications
Wu, S., Liu, J., Liu, C., Yang, A., & Qiao, J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03326-8 · Cited by 188
Toward dental caries: Exploring nanoparticle-based platforms and calcium phosphate compounds for dental restorative materials
Balhaddad, A. A., Kensara, A. A., Hidan, D., Weir, M. D., Xu, H. H. K., & Melo, M. A. S. (2018) · Bioactive Materials · doi:10.1016/j.bioactmat.2018.12.002 · Cited by 175
Volatile profile of elderberry juice: Effect of lactic acid fermentation using L. plantarum , L. rhamnosus and L. casei strains
Ricci, A., Cirlini, M., Levante, A., Dall’Asta, C., Galaverna, G., & Lazzi, C. (2017) · Food Research International · doi:10.1016/j.foodres.2017.11.042 · Cited by 169
Advantages and disadvantages of non‐starter lactic acid bacteria from traditional fermented foods: Potential use as starters or probiotics
Grujović, M. Ž., Mladenović, K., Semedo‐Lemsaddek, T., Laranjo, M., Stefanović, O. D., & Kocić‐Tanackov, S. (2022) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12897 · Cited by 163
Updates on understanding of probiotic lactic acid bacteria responses to environmental stresses and highlights on proteomic analyses
Mbye, M., Baig, M. A., AbuQamar, S. F., El-Tarabily, K. A., Obaid, R. S., Osaili, T. M. I., Al‐Nabulsi, A. A., Turner, M. S., Shah, N. P., & Ayyash, M. M. (2020) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12554 · Cited by 155
The Impact of Physicochemical Conditions on Lactic Acid Bacteria Survival in Food Products
Sionek, B., Szydłowska, A., Trząskowska, M., & Kołożyn‐Krajewska, D. (2024) · Fermentation · doi:10.3390/fermentation10060298 · Cited by 167
The Efficient Clade: Lactic Acid Bacteria for Industrial Chemical Production
Sauer, M., Rußmayer, H., Grabherr, R. M., Peterbauer, C., & Marx, H. (2017) · Trends in biotechnology · doi:10.1016/j.tibtech.2017.05.002 · Cited by 145
How probiotics face food stress: They get by with a little help
Fiocco, D., Longo, A., Arena, M. P., Russo, P., Spano, G., & Capozzi, V. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2019.1580673 · Cited by 150
Abundance, diversity and plant‐specific adaptations of plant‐associated lactic acid bacteria
Yu, A. O., Leveau, J. H. J., & Marco, M. L. (2019) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12794 · Cited by 141
Recent Advances in the Understanding of Stress Resistance Mechanisms in Probiotics: Relevance for the Design of Functional Food Systems
Bustos, A. Y., Taranto, M. P., Gerez, C. L., Agriopoulou, S., Smaoui, S., Varzakas, T. H., & Enshasy, H. A. E. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-024-10273-9 · Cited by 142
Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms
Yang, H., He, M., & Wu, C. (2021) · LWT · doi:10.1016/j.lwt.2021.111203 · Cited by 129
Lactobacillus , Bifidobacterium and Lactococcus response to environmental stress: Mechanisms and application of cross‐protection to improve resistance against freeze‐drying
Gao, X., Kong, J., Zhu, H., Mao, B., Cui, S., & Zhao, J. (2021) · Journal of Applied Microbiology · doi:10.1111/jam.15251 · Cited by 124
Glycerol metabolism and its regulation in lactic acid bacteria
Doi, Y. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-09830-y · Cited by 119
The potential of lactic acid bacteria in mediating the control of plant diseases and plant growth stimulation in crop production - A mini review
Jaffar, N. S., Jawan, R., & Chong, K. P. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1047945 · Cited by 108
Factors influencing the membrane fluidity and the impact on production of lactic acid bacteria starters
Fonseca, F., Pénicaud, C., Tymczyszyn, E. E., Gómez‐Zavaglia, A., & Passot, S. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10002-1 · Cited by 111
Cell wall homeostasis in lactic acid bacteria: threats and defences
Martínez, B., Rodríguez, A., Kulakauskas, S., & Chapot, M.-P. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa021 · Cited by 113
Trends and hassles in the microbial production of lactic acid from lignocellulosic biomass
Nwamba, M. C., Sun, F. F., Mukasekuru, M. R., Song, G., Harindintwali, J. D., Ajeje, S. B., & Sun, H. (2020) · Environmental Technology & Innovation · doi:10.1016/j.eti.2020.101337 · Cited by 104
The efficacy of three double-microencapsulation methods for preservation of probiotic bacteria
Pupa, P., Apiwatsiri, P., Sirichokchatchawan, W., Pirarat, N., Muangsin, N., Shah, A. A., & Prapasarakul, N. (2021) · Scientific Reports · doi:10.1038/s41598-021-93263-z · Cited by 103
Enhancement of γ-aminobutyric acid (GABA) production by Lactobacillus brevis CRL 2013 based on carbohydrate fermentation
Cataldo, P. G., Villegas, J. M., de Giori, G. S., Saavedra, L., & Hebert, E. M. (2020) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2020.108792 · Cited by 105
Fermented Dairy Products as Precision Modulators of Gut Microbiota and Host Health: Mechanistic Insights, Clinical Evidence, and Future Directions
Gao, Y., Liu, Y., Ma, T., Liang, Q., Sun, J., Wu, X., Song, Y., Nie, H., HUANG, J. C., & Mu, G. (2025) · Foods · doi:10.3390/foods14111946 · Cited by 110
A rapid and versatile tool for genomic engineering in Lactococcus lactis
Guo, T., Xin, Y., Zhang, Y., Gu, X., & Kong, J. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1075-3 · Cited by 99
Lactic Acid for Green Chemical Industry: Recent Advances in and Future Prospects for Production Technology, Recovery, and Applications
Kim, J., Kim, Y., Lebaka, V. R., & Wee, Y. (2022) · Fermentation · doi:10.3390/fermentation8110609 · Cited by 98
Redox cofactor engineering in industrial microorganisms: strategies, recent applications and future directions
Jia-heng, L., Li, H., Zhao, G.-R., Caiyin, Q., & Qiao, J. (2018) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-018-2031-7 · Cited by 96
Systems Biology of Lactic Acid Bacteria: For Food and Thought
Teusink, B., & Molenaar, D. (2017) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2017.07.005 · Cited by 95
Microbial abundance, composition, and function in nectar are shaped by flower visitor identity
Morris, M. M., Frixione, N. J., Burkert, A., Dinsdale, E. A., & Vannette, R. L. (2020) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiaa003 · Cited by 88
Evaluation of potentially probiotic yeasts and Lactiplantibacillus plantarum in co-culture for the elaboration of a functional plant-based fermented beverage
Ferreira, I. V. A., Melo, D. D. S., Menezes, A. G. T., Fonseca, H. C., de Assis, B. B. T., Ramos, C. L., Magnani, M., Dias, D. R., & Schwan, R. F. (2022) · Food Research International · doi:10.1016/j.foodres.2022.111697 · Cited by 88
Enhanced viability of probiotics encapsulated within synthetic/natural biopolymers by the addition of gum arabic via electrohydrodynamic processing
Ma, J., Li, T., Wang, Q., Xu, C., Yu, W., Yu, H., Wang, W., Feng, Z., Chen, L., Hou, J., et al. (2023) · Food Chemistry · doi:10.1016/j.foodchem.2023.135680 · Cited by 88
Coinoculation of lactic acid bacteria and yeasts increases the quality of wet fermented Arabica coffee
Cassimiro, D. M. D. J., Batista, N. N., Fonseca, H. C., Naves, J. A. O., Dias, D. R., & Schwan, R. F. (2022) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2022.109627 · Cited by 87
Measuring and modeling energy and power consumption in living microbial cells with a synthetic ATP reporter
Deng, Y., Beahm, D. R., Ionov, S., & Sarpeshkar, R. (2021) · BMC Biology · doi:10.1186/s12915-021-01023-2 · Cited by 90
Review: Adaptation of Beneficial Propionibacteria, Lactobacilli, and Bifidobacteria Improves Tolerance Toward Technological and Digestive Stresses
Gaucher, F., Bonnassié, S., Rabah, H., Marchand, P., Blanc, P., Jeantet, R., & Jan, G. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00841 · Cited by 88
The effect of fermentation conditions (temperature, salt concentration, and pH) with lactobacillus strains for producing Short Chain Fatty Acids
Hadinia, N., Dovom, M. R. E., & Yavarmanesh, M. (2022) · LWT · doi:10.1016/j.lwt.2022.113709 · Cited by 83
Microencapsulation of Probiotics for Enhanced Stability and Health Benefits in Dairy Functional Foods: A Focus on Pasta Filata Cheese
D’Amico, V., Cavaliere, M., Ivone, M., Lacassia, C., Celano, G., Vacca, M., la Forgia, F. M., Fontana, S., Angelis, M. D., Denora, N., et al. (2025) · Pharmaceutics · doi:10.3390/pharmaceutics17020185 · Cited by 91
Journey of the Probiotic Bacteria: Survival of the Fittest
Mendonça, A. A., Pinto-Neto, W. D. P., da Paixão, G. A., Santos, D. D. S., De Morais, M. A., & De Souza, R. B. (2022) · Microorganisms · doi:10.3390/microorganisms11010095 · Cited by 82
Analysis of the probiotic characteristics and adaptability of Lactiplantibacillus plantarum DMDL 9010 to gastrointestinal environment by complete genome sequencing and corresponding phenotypes
Liu, D., Huang, Y., & Liang, M. (2022) · LWT · doi:10.1016/j.lwt.2022.113129 · Cited by 85
Lifestyle, metabolism and environmental adaptation in Lactococcus lactis
Kleerebezem, M., Bachmann, H., van Pelt‐KleinJan, E., Douwenga, S., Smid, E. J., Teusink, B., & van Mastrigt, O. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa033 · Cited by 85
Self-citation
Comprehensive Review of Aflatoxin and Ochratoxin A Dynamics: Emergence, Toxicological Impact, and Advanced Control Strategies
Nazareth, T. D. M., Pérez, E. S., Luz, C., Meca, G., & Quiles, J. M. (2024) · Foods · doi:10.3390/foods13121920 · Cited by 83
Key Stress Response Mechanisms of Probiotics During Their Journey Through the Digestive System: A Review
Castro-López, C., Romero‐Luna, H. E., Garcia, H. S., Vallejo‐Córdoba, B., González-Córdova, A. F., & Hernández‐Mendoza, A. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09981-x · Cited by 80
Enhanced acid-stress tolerance in Lactococcus lactis NZ9000 by overexpression of ABC transporters
Zhu, Z., Yang, J., Yang, P., Wu, Z., Zhang, J., & Du, G. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1188-8 · Cited by 79
Acid Stress Response Mechanisms of Group B Streptococci
Shabayek, S., & Spellerberg, B. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00395 · Cited by 80
An oral “Super probiotics” with versatile self-assembly adventitia for enhanced intestinal colonization by autonomous regulating the pathological microenvironment
Yang, J., Zhang, G., Yang, X., Peng, M., Ge, S., Tan, S., Wen, Z., Wang, Y., Wu, S., Liang, Y., et al. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.137204 · Cited by 78
Generally Stressed Out Bacteria: Environmental Stress Response Mechanisms in Gram-Positive Bacteria
Bonilla, C. Y. (2020) · Integrative and Comparative Biology · doi:10.1093/icb/icaa002 · Cited by 80
Evolutionary engineering of Lactobacillus pentosus improves lactic acid productivity from xylose-rich media at low pH
Cubas‐Cano, E., González‐Fernández, C., & Tomás‐Pejó, E. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.121540 · Cited by 76
Beneficial bacteria activate type-I interferon production via the intracellular cytosolic sensors STING and MAVS
Gutierrez‐Merino, J., Isla, B., Combes, T., Martínez, F. O., & de Motes, C. M. (2020) · Gut Microbes · doi:10.1080/19490976.2019.1707015 · Cited by 76
Effects of freeze drying in complex lyoprotectants on the survival, and membrane fatty acid composition of Lactobacillus plantarum L1 and Lactobacillus fermentum L2
Cheng, Z., Xu, Y., Wu, J., Weng, P., & Wu, Z. (2022) · Cryobiology · doi:10.1016/j.cryobiol.2022.01.003 · Cited by 75
Proteome constraints reveal targets for improving microbial fitness in nutrient‐rich environments
Chen, Y., van Pelt‐KleinJan, E., van Olst, B., Douwenga, S., Boeren, S., Bachmann, H., Molenaar, D., Nielsen, J., & Teusink, B. (2021) · Molecular Systems Biology · doi:10.15252/msb.202010093 · Cited by 73
Lactic Acid Bacteria Diversity and Characterization of Probiotic Candidates in Fermented Meats
Parlindungan, E., Lugli, G. A., Ventura, M., van Sinderen, D., & Mahony, J. (2021) · Foods · doi:10.3390/foods10071519 · Cited by 78
Self-citation
Strategies to enhance stress tolerance in lactic acid bacteria across diverse stress conditions
Derunets, A. S., Selimzyanova, A. I., Rykov, S. V., Kuznetsov, A. Y., & Berezina, O. V. (2024) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-024-03905-3 · Cited by 73
Application of lactic acid fermentation to elderberry juice: Changes in acidic and glucidic fractions
Cirlini, M., Ricci, A., Galaverna, G., & Lazzi, C. (2019) · LWT · doi:10.1016/j.lwt.2019.108779 · Cited by 72
Engineer probiotic bifidobacteria for food and biomedical applications - Current status and future prospective
Zuo, F., Chen, S., & Marcotte, H. (2020) · Biotechnology Advances · doi:10.1016/j.biotechadv.2020.107654 · Cited by 72
Modification of the functional and bioactive properties of camel milk casein and whey proteins by ultrasonication and fermentation with Lactobacillus delbrueckii subsp. lactis
Gammoh, S., Alu'datt, M. H., Tranchant, C. C., Al-U'datt, D. G. F., Alhamad, M. N., Rababah, T., Kubow, S. J., Haddadin, M. S. Y., Ammari, Z., Maghaydah, S., et al. (2020) · LWT · doi:10.1016/j.lwt.2020.109501 · Cited by 69
The Evolution of gene regulation research in Lactococcus lactis
Kok, J., van Gijtenbeek, L. A., de Jong, A., van der Meulen, S. B., Solopova, A., & Kuipers, O. P. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux028 · Cited by 70
Self-citation
Deciphering the crucial roles of transcriptional regulator GadR on gamma-aminobutyric acid production and acid resistance in Lactobacillus brevis
Gong, L.-C., Ren, C., & Xu, Y. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1157-2 · Cited by 68
Systems Biology – A Guide for Understanding and Developing Improved Strains of Lactic Acid Bacteria
Liu, J., Chan, S. H. J., Chen, J., Solem, C., & Jensen, P. R. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00876 · Cited by 68
Untargeted LC-QTOF-MS/MS based metabolomics approach for revealing bioactive components in probiotic fermented coffee brews
Chan, M. Z. A., Lau, H., Lim, S. Y., Li, S. F. Y., & Liu, S. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110656 · Cited by 66
Dehydrogenases of acetic acid bacteria
Qin, Z., Yu, S., Chen, J., & Zhou, J. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107863 · Cited by 66
Pneumococcal within-host diversity during colonization, transmission and treatment
Tonkin‐Hill, G. Q., Ling, C. L., Chaguza, C., Salter, S. J., Hinfonthong, P., Nikolaou, E., Tate, N., Pastusiak, A., Turner, C., Chewapreecha, C., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01238-1 · Cited by 70
Potential of Lactic Acid Bacteria Isolated From Different Forages as Silage Inoculants for Improving Fermentation Quality and Aerobic Stability
Puntillo, M., Gaggiotti, M., Oteiza, J. M., Binetti, A., Massera, A., & Vinderola, G. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.586716 · Cited by 65
Challenges associated with spray drying of lactic acid bacteria: Understanding cell viability loss
Moreira, M. T. C., Martins, E., Perrone, Í. T., de Freitas, R., Queiroz, L. S., & de Carvalho, A. F. (2021) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12774 · Cited by 65
Gamma-aminobutyric acid (GABA) production in fermented milk by lactic acid bacteria isolated from spontaneous raw milk fermentation
Galli, V., Venturi, M., Mari, E., Guerrini, S., & Granchi, L. (2021) · International Dairy Journal · doi:10.1016/j.idairyj.2021.105284 · Cited by 65
Response mechanisms to acid stress of acid-resistant bacteria and biotechnological applications in the food industry
Xu, J., Guo, L., Zhao, N., Meng, X., Zhang, J., Wang, T., Wei, X., & Fan, M. (2022) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2021.2025335 · Cited by 65
Stress Response in Bifidobacteria
Schöpping, M., Zeidan, A. A., & Franzén, C. J. (2022) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00170-21 · Cited by 69
Production of d-lactic acid by Lactobacillus delbrueckii ssp. delbrueckii from orange peel waste: techno-economical assessment of nitrogen sources
de la Torre, I., Ladero, M., & Santos, V. E. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9432-4 · Cited by 65
Prominent use of lactic acid bacteria in soil-plant systems
Murindangabo, Y. T., Kopecký, M., Perná, K., Nguyen, T. G., Konvalina, P., & Kavková, M. (2023) · Applied Soil Ecology · doi:10.1016/j.apsoil.2023.104955 · Cited by 64
Producing Powders Containing Active Dry Probiotics With the Aid of Spray Drying
Fu, N., Huang, S., Xiao, J., & Chen, X. D. (2018) · Advances in food and nutrition research · doi:10.1016/bs.afnr.2018.02.003 · Cited by 67
A Combined Metagenomics and Metatranscriptomics Approach to Unravel Costa Rican Cocoa Box Fermentation Processes Reveals Yet Unreported Microbial Species and Functionalities
Verce, M., Schoonejans, J., Aguirre, C. H., Bravo, R. M., Vuyst, L. D., & Weckx, S. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.641185 · Cited by 63
Lactobacilli and human dental caries: more than mechanical retention
Wen, Z. T., Huang, X., Ellepola, K., Liao, S., & Li, Y. (2022) · Microbiology · doi:10.1099/mic.0.001196 · Cited by 66
Lactobacilli biology, applications and host interactions
Mejía-Caballero, A., & Marco, M. L. (2025) · Nature Reviews Microbiology · doi:10.1038/s41579-025-01205-7 · Cited by 65
Prebiotics for Lactose Intolerance: Variability in Galacto-Oligosaccharide Utilization by Intestinal Lactobacillus rhamnosus
Arnold, J. W., Simpson, J. B., Roach, J. M., Bruno-Bárcena, J. M., & Azcárate-Peril, M. A. (2018) · Nutrients · doi:10.3390/nu10101517 · Cited by 61
Comparative Genomics of Wild Bee and Flower Isolated Lactobacillus Reveals Potential Adaptation to the Bee Host
Vuong, H. Q., & McFrederick, Q. S. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz136 · Cited by 61
Starter cultures as a reservoir of antibiotic resistant microorganisms
Zarzecka, U., Zadernowska, A., & Chajęcka‐Wierzchowska, W. (2020) · LWT · doi:10.1016/j.lwt.2020.109424 · Cited by 58
Antagonistic Activity against Ascosphaera apis and Functional Properties of Lactobacillus kunkeei Strains
Iorizzo, M., Lombardi, S. J., Ganassi, S., Testa, B., Ianiro, M., Letizia, F., Succi, M., Tremonte, P., Vergalito, F., Cozzolino, A., et al. (2020) · Antibiotics · doi:10.3390/antibiotics9050262 · Cited by 57
Global transcriptomic analysis of Lactobacillus plantarum CAUH2 in response to hydrogen peroxide stress
Zhai, Z., Yang, Y., Wang, H., Wang, G., Ren, F., Li, Z., & Hao, Y. (2019) · Food Microbiology · doi:10.1016/j.fm.2019.103389 · Cited by 56
Probiotics, their action modality and the use of multi-omics in metamorphosis of commensal microbiota into target-based probiotics
Idrees, M., Imran, M., Atiq, N., Zahra, R., Abid, R., Alreshidi, M. M., Roberts, T. K., Abdelgadir, A., Tipu, M. K., Farid, A., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.959941 · Cited by 56
Engineering Clinically Relevant Probiotics with Switchable “Nano‐Promoter” and “Nano‐Effector” for Precision Tumor Therapy
Cao, F., Jin, L., Zhang, C., Gao, Y., Qian, Z., Wen, H., Yang, S., Ye, Z., Hong, L., Huang, Y., et al. (2023) · Advanced Materials · doi:10.1002/adma.202304257 · Cited by 61
How Lactobacillus plantarum shapes its transcriptome in response to contrasting habitats
Filannino, P., Angelis, M. D., Cagno, R. D., Gozzi, G., Riciputi, Y., & Gobbetti, M. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14372 · Cited by 57
Self-citation
On the use of resting L. delbrueckii spp. delbrueckii cells for D-lactic acid production from orange peel wastes hydrolysates
de la Torre, I., Acedos, M. G., Ladero, M., & Santos, V. E. (2019) · Biochemical Engineering Journal · doi:10.1016/j.bej.2019.02.012 · Cited by 56
Evaluation of the safety and probiotic properties of Lactobacillus gasseri LGZ1029 based on whole genome analysis
Wu, J.-J., Zhou, Q.-Y., Liu, D., Xiong, J., Liang, M., Tang, J., & Xu, Y.-Q. (2023) · LWT · doi:10.1016/j.lwt.2023.114759 · Cited by 54
Transcriptome responses of Lactobacillus acetotolerans F28 to a short and long term ethanol stress
Yang, X., Teng, K., Zhang, J., Wang, F., Zhang, T., Ai, G., Han, P., Bai, F., & Zhong, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-02975-8 · Cited by 53
Growth, survival, and metabolic activities of probiotics Lactobacillus rhamnosus GG and Saccharomyces cerevisiae var. boulardii CNCM-I745 in fermented coffee brews
Chan, M. Z. A., Toh, M., & Liu, S. (2021) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2021.109229 · Cited by 52
Arginine deiminase pathway of Tetragenococcus halophilus contributes to improve the acid tolerance of lactic acid bacteria
Yang, H., Wang, D., Jin, Y., Zhou, R., Huang, J., & Wu, C. (2023) · Food Microbiology · doi:10.1016/j.fm.2023.104281 · Cited by 51
Extremophiles: the species that evolve and survive under hostile conditions
Rekadwad, B. N., Li, W.-J., Grau, J. M. G., Devasya, R. P., Bhagwath, A. A., Urana, R., & Parwez, K. (2023) · 3 Biotech · doi:10.1007/s13205-023-03733-6 · Cited by 51
Stress Suppressor Screening Leads to Detection of Regulation of Cyclic di-AMP Homeostasis by a Trk Family Effector Protein in Streptococcus pneumoniae
Zarrella, T. M., Metzger, D. W., & Bai, G. (2018) · Journal of Bacteriology · doi:10.1128/jb.00045-18 · Cited by 52
Bioconversion of Milk Permeate with Selected Lactic Acid Bacteria Strains and Apple By-Products into Beverages with Antimicrobial Properties and Enriched with Galactooligosaccharides
Zokaitytė, E., Černauskas, D., Klupšaitė, D., Lėlė, V., Starkutė, V., Zavistanavičiūtė, P., Ružauskas, M., Gružauskas, R., Juodeikienė, G., Rocha, J. M., et al. (2020) · Microorganisms · doi:10.3390/microorganisms8081182 · Cited by 51
Understanding the Probiotic Bacterial Responses Against Various Stresses in Food Matrix and Gastrointestinal Tract: A Review
Kathiriya, M. R., Vekariya, Y. V., & Hati, S. (2023) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-023-10104-3 · Cited by 50
Advancements in the Use of Fermented Fruit Juices by Lactic Acid Bacteria as Functional Foods: Prospects and Challenges of Lactiplantibacillus (Lpb.) plantarum subsp. plantarum Application
Plessas, S. (2021) · Fermentation · doi:10.3390/fermentation8010006 · Cited by 50
Contribution of YthA, a PspC Family Transcriptional Regulator of Lactococcus lactis F44 Acid Tolerance and Nisin Yield: a Transcriptomic Approach
Wu, H., Liu, J., Miao, S., Zhao, Y., Zhu, H., Qiao, M., Saris, P. E. J., & Qiao, J. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.02483-17 · Cited by 50
Purification and Biochemical Characterization of Phytase Enzyme from Lactobacillus coryniformis (MH121153)
Demir, Y., Dikbaş, N., & Beydemir, Ş. (2018) · Molecular Biotechnology · doi:10.1007/s12033-018-0116-1 · Cited by 50
Prevalence, Genetic Diversity, and Technological Functions of the Lactobacillus sanfranciscensis in Sourdough: A Review
Zhang, G., Tu, J., Sadiq, F. A., Zhang, W., & Wang, W. (2019) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12459 · Cited by 50
Impact of Freezing and Freeze Drying on Lactobacillus rhamnosus GG Survival: Mechanisms of Cell Damage and the Role of Pre-Freezing Conditions and Cryoprotectants
Wang, J., Wu, P., Dhital, S., Yu, A., & Chen, X. D. (2025) · Foods · doi:10.3390/foods14101817 · Cited by 49
Enhanced Acid Tolerance in Lactobacillus acidophilus by Atmospheric and Room Temperature Plasma (ARTP) Coupled with Adaptive Laboratory Evolution (ALE)
Nyabako, B. A., Fang, H., Cui, F., Liu, K., Tao, T.-L., Zan, X., & Sun, W. (2020) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-020-03264-3 · Cited by 49

Authors: Papadimitriou, K., Alegría, Á., Bron, P. A., de Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J. A., Linares, D. M., Ross, P., Stanton, C., Turroni, F., van Sinderen, D., Varmanen, P., Ventura, M., Zúñiga, M., Tsakalidou, E., & Kok, J.
Affiliations: Agricultural University of Athens (GR)
University of Groningen (NL)
TiFN (NL)
Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Bari, Italy
University of Bari Aldo Moro (IT)
Department of Oral Biology, University of Florida College of Dentistry, Gainesville, Florida, USA
Teagasc - The Irish Agriculture and Food Development Authority (IE)
APC, Microbiome Institute, University College Cork, Cork, Ireland
University of Parma (IT)
University of Helsinki (FI)
Consejo Superior de Investigaciones Científicas (ES)
ORCID: Papadimitriou, Konstantinos
Alegría, Ángel
Bron, Peter A.
Gobbetti, Marco
Kleerebezem, Michiel
Stanton, Catherine
Turroni, Francesca
Varmanen, Pekka
Ventura, Marco
Zúñiga, Manuel
Tsakalidou, Effie
Kok, Jan
Venue: Microbiology and Molecular Biology Reviews
Publisher: American Society for Microbiology
Published: 2016-09
Volume: 80
Issue: 3
Pages: 837-890
ISSN: 1092-2172 (ISSN-L)
1098-5557
DOI: 10.1128/mmbr.00076-15
PMC: PMC4981675
OpenAlex: W2499564842
Cited by: 914
References: 646
Citations by year: 2026: 173 · 2025: 163 · 2024: 97 · 2023: 92 · 2022: 86 · 2021: 92 · 2020: 83 · 2019: 56 · 2018: 48 · 2017: 20 · 2016: 3
FWCI: 4.84
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Microbiology and Molecular Biology Reviews (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Socio-Environmental Systems Modeling (acceptedVersion)
CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion, cc-by-nc-nd)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
Open Research (University of Surrey) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: European Commission (2007–2013, FP7 2007-2013, FP7/2007, 623448)
Science Foundation Ireland (13/IA/1953, 12/RC/2273, 12/RC/)
APC Microbiome Institute
National Institute of Dental and Craniofacial Research (DE019783, DE022559, R01DE019783, R01DE022559)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
Keywords: lactic acid bacteria, stress physiology, stress response, probiotics, Lactobacillus, Lactococcus lactis, Enterococcus, Streptococcus, stress tolerance, biofilm, dormancy, prophage induction, stress tolerance engineering, food industry
MeSH terms: Energy Metabolism, Fermentation, Food Microbiology, Lactobacillus, Osmotic Pressure, Streptococcus, Stress, Physiological, Signal Transduction, Enterococcus, Biofilms, Lactic Acid, Probiotics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Stress Physiology of Lactic Acid Bacteria.

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks