Stress Physiology of Lactic Acid Bacteria

doi:10.1128/MMBR.00076-15

Review

. 2016 Jul 27;80(3):837-90.

doi: 10.1128/MMBR.00076-15. Print 2016 Sep.

Stress Physiology of Lactic Acid Bacteria

Konstantinos Papadimitriou¹, Ángel Alegría², Peter A Bron³, Maria de Angelis⁴, Marco Gobbetti⁴, Michiel Kleerebezem⁵, José A Lemos⁶, Daniel M Linares⁷, Paul Ross⁸, Catherine Stanton⁷, Francesca Turroni⁹, Douwe van Sinderen¹⁰, Pekka Varmanen¹¹, Marco Ventura⁹, Manuel Zúñiga¹², Effie Tsakalidou¹, Jan Kok¹³

Affiliations

¹ Laboratory of Dairy Research, Department of Food Science and Human Nutrition, Agricultural University of Athens, Athens, Greece.
² Department of Molecular Genetics, University of Groningen, Groningen, The Netherlands.
³ NIZO Food Research, Ede, The Netherlands Top Institute Food and Nutrition, Wageningen, The Netherlands.
⁴ Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Bari, Italy.
⁵ Top Institute Food and Nutrition, Wageningen, The Netherlands Host Microbe Interactomics Group, Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands.
⁶ Department of Oral Biology, University of Florida College of Dentistry, Gainesville, Florida, USA.
⁷ Food Biosciences Department, Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland APC, Microbiome Institute, University College Cork, Cork, Ireland.
⁸ APC, Microbiome Institute, University College Cork, Cork, Ireland.
⁹ Laboratory of Probiogenomics, Department of Life Sciences, University of Parma, Parma, Italy.
¹⁰ APC, Microbiome Institute, University College Cork, Cork, Ireland School of Microbiology, University College Cork, Cork, Ireland.
¹¹ Department of Food and Environmental Sciences, University of Helsinki, Helsinki, Finland.
¹² Department of Food Biotechnology, Institute of Agrochemistry and Food Technology, CSIC, Paterna, Spain.
¹³ Department of Molecular Genetics, University of Groningen, Groningen, The Netherlands Top Institute Food and Nutrition, Wageningen, The Netherlands jan.kok@rug.nl.

PMID: 27466284
PMCID: PMC4981675
DOI: 10.1128/MMBR.00076-15

Review

Stress Physiology of Lactic Acid Bacteria

Konstantinos Papadimitriou et al. Microbiol Mol Biol Rev. 2016.

. 2016 Jul 27;80(3):837-90.

doi: 10.1128/MMBR.00076-15. Print 2016 Sep.

Authors

Affiliations

¹ Laboratory of Dairy Research, Department of Food Science and Human Nutrition, Agricultural University of Athens, Athens, Greece.
² Department of Molecular Genetics, University of Groningen, Groningen, The Netherlands.
³ NIZO Food Research, Ede, The Netherlands Top Institute Food and Nutrition, Wageningen, The Netherlands.
⁴ Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Bari, Italy.
⁵ Top Institute Food and Nutrition, Wageningen, The Netherlands Host Microbe Interactomics Group, Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands.
⁶ Department of Oral Biology, University of Florida College of Dentistry, Gainesville, Florida, USA.
⁷ Food Biosciences Department, Teagasc Food Research Centre, Moorepark, Fermoy, County Cork, Ireland APC, Microbiome Institute, University College Cork, Cork, Ireland.
⁸ APC, Microbiome Institute, University College Cork, Cork, Ireland.
⁹ Laboratory of Probiogenomics, Department of Life Sciences, University of Parma, Parma, Italy.
¹⁰ APC, Microbiome Institute, University College Cork, Cork, Ireland School of Microbiology, University College Cork, Cork, Ireland.
¹¹ Department of Food and Environmental Sciences, University of Helsinki, Helsinki, Finland.
¹² Department of Food Biotechnology, Institute of Agrochemistry and Food Technology, CSIC, Paterna, Spain.
¹³ Department of Molecular Genetics, University of Groningen, Groningen, The Netherlands Top Institute Food and Nutrition, Wageningen, The Netherlands jan.kok@rug.nl.

PMID: 27466284
PMCID: PMC4981675
DOI: 10.1128/MMBR.00076-15

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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Figures

**FIG 1**
Schematic representation of selected LAB stress sensory systems. HK, histidine kinase; RR, response regulator.

**FIG 2**
Schematic representation of changes of the carbohydrate metabolism, glycolysis, and fate of pyruvate in lactic acid bacteria. Colored arrows and enzymes indicate common reactions (black), those mainly induced during fermentation by unstressed cells (blue), and those induced in respiratory and/or environmentally stressed cells (red). LDH, lactate dehydrogenase; ACK, acetate kinase; POX, pyruvate oxidase; PFL, pyruvate formate lyase; PdhABCD, pyruvate dehydrogenase complex; α-ASL, α-acetolactate synthase; AdhE, alcohol dehydrogenase; NOX, NADH oxidase; α-ALD, α-acetolactate decarboxylase; DAR, diacetyl reductase.

**FIG 3**
Schematic representation of the main free amino acid pathways of lactic acid bacteria induced under acid stress and/or starvation conditions. GABA, γ-aminobutyric acid; ADI, arginine deiminase; cOTC, catabolic ornithine transcarbamoylase; CK, carbamate kinase; AguA, agmatine deiminase; AguB, putrescine carbamoyl transferase; AguC, carbamate kinase; AguD, agmatine/putrescine antiporter; GAD, glutamate decarboxylase; HDC, histidine decarboxylase; AspD, aspartic acid decarboxylase; AspT, aspartate-alanine antiporter; Bcat, α-ketoglutarate-dependent branched-chain aminotransferase; HycDH, hydroxyacid dehydrogenase; KaDH, keto acid dehydrogenase; KDC, 2-keto acid decarboxylase; ADH, alcohol dehydrogenase; AIDH, aldehyde dehydrogenase; PTAC, phosphotransacylase; ACK, acetate kinase.

**FIG 4**
Schematic representation of the main molecular mechanisms preventing macromolecules from being damaged in LAB. SOD, superoxide dismutase.

**FIG 5**
Schematic representation of the main molecular mechanisms repairing damaged macromolecules in LAB.

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References

1. Papadimitriou K, Pot B, Tsakalidou E. 2015. How microbes adapt to a diversity of food niches. Curr Opin Food Sci 2:29–35. doi:10.1016/j.cofs.2015.01.001. - DOI
1. Orla-Jensen S. 1919. The lactic acid bacteria. Fred Host and Son, Copenhagen, Denmark.
1. Klein G, Pack A, Bonaparte C, Reuter G. 1998. Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103–125. doi:10.1016/S0168-1605(98)00049-X. - DOI - PubMed
1. Stiles ME, Holzapfel WH. 1997. Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36:1–29. doi:10.1016/S0168-1605(96)01233-0. - DOI - PubMed
1. Sun Z, Harris HM, McCann A, Guo C, Argimon S, Zhang W, Yang X, Jeffery IB, Cooney JC, Kagawa TF, Liu W, Song Y, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O'Sullivan O, Ritari J, Douillard FP, Paul Ross R, Yang R, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui Y, Zhang H, O'Toole PW. 2015. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. doi:10.1038/ncomms9322. - DOI - PMC - PubMed

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[1] Papadimitriou K, Pot B, Tsakalidou E. 2015. How microbes adapt to a diversity of food niches. Curr Opin Food Sci 2:29–35. doi:10.1016/j.cofs.2015.01.001. - DOI

[2] Papadimitriou K, Pot B, Tsakalidou E. 2015. How microbes adapt to a diversity of food niches. Curr Opin Food Sci 2:29–35. doi:10.1016/j.cofs.2015.01.001. - DOI

[3] Orla-Jensen S. 1919. The lactic acid bacteria. Fred Host and Son, Copenhagen, Denmark.

[4] Orla-Jensen S. 1919. The lactic acid bacteria. Fred Host and Son, Copenhagen, Denmark.

[5] Klein G, Pack A, Bonaparte C, Reuter G. 1998. Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103–125. doi:10.1016/S0168-1605(98)00049-X. - DOI - PubMed

[6] Klein G, Pack A, Bonaparte C, Reuter G. 1998. Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103–125. doi:10.1016/S0168-1605(98)00049-X. - DOI - PubMed

[7] Stiles ME, Holzapfel WH. 1997. Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36:1–29. doi:10.1016/S0168-1605(96)01233-0. - DOI - PubMed

[8] Stiles ME, Holzapfel WH. 1997. Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol 36:1–29. doi:10.1016/S0168-1605(96)01233-0. - DOI - PubMed

[9] Sun Z, Harris HM, McCann A, Guo C, Argimon S, Zhang W, Yang X, Jeffery IB, Cooney JC, Kagawa TF, Liu W, Song Y, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O'Sullivan O, Ritari J, Douillard FP, Paul Ross R, Yang R, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui Y, Zhang H, O'Toole PW. 2015. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. doi:10.1038/ncomms9322. - DOI - PMC - PubMed

[10] Sun Z, Harris HM, McCann A, Guo C, Argimon S, Zhang W, Yang X, Jeffery IB, Cooney JC, Kagawa TF, Liu W, Song Y, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O'Sullivan O, Ritari J, Douillard FP, Paul Ross R, Yang R, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui Y, Zhang H, O'Toole PW. 2015. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. doi:10.1038/ncomms9322. - DOI - PMC - PubMed

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Stress Physiology of Lactic Acid Bacteria

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Stress Physiology of Lactic Acid Bacteria

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