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

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Stress Physiology of Lactic Acid Bacteria.

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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

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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.

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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

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