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Genetics of Lactococci

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  • Authors: Philippe Gaudu1, Yuji Yamamoto2, Peter Ruhdal Jensen3, Karin Hammer4, Delphine Lechardeur5, Alexandra Gruss6
  • Editors: Vincent A. Fischetti7, Richard P. Novick8, Joseph J. Ferretti9, Daniel A. Portnoy10, Miriam Braunstein11, Julian I. Rood12
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institut Micalis, INRA, 78350 Jouy en Josas, France; 2: Laboratory of Cellular Microbiology, School of Veterinary Medicine, Kitasato University, Towada, 034-8628, Aomori Japan; 3: National Food Institute, Technical University of Denmark, DK-2800 Lyngby, Denmark; 4: DTU Bioengineering, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark; 5: Institut Micalis, INRA, 78350 Jouy en Josas, France; 6: Institut Micalis, INRA, 78350 Jouy en Josas, France; 7: The Rockefeller University, New York, NY; 8: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 9: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 10: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 11: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 12: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
  • Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
  • Received 29 May 2018 Accepted 08 January 2019 Published 12 July 2019
  • Alexandra Gruss, [email protected]
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  • Abstract:

    is the best characterized species among the lactococci, and among the most consumed food-fermenting bacteria worldwide. Thanks to their importance in industrialized food production, lactococci are among the lead bacteria understood for fundamental metabolic pathways that dictate growth and survival properties. Interestingly, lactococci belong to the Streptococcaceae family, which includes food, commensal and virulent species. As basic metabolic pathways (e.g., respiration, metal homeostasis, nucleotide metabolism) are now understood to underlie virulence, processes elucidated in lactococci could be important for understanding pathogen fitness and synergy between bacteria. This chapter highlights major findings in lactococci and related bacteria, and covers five themes: distinguishing features of lactococci, metabolic capacities including the less known respiration metabolism in Streptococcaceae, factors and pathways modulating stress response and fitness, interbacterial dialogue metabolites, and novel applications in health and biotechnology.

  • Citation: Gaudu P, Yamamoto Y, Jensen P, Hammer K, Lechardeur D, Gruss A. 2019. Genetics of Lactococci. Microbiol Spectrum 7(4):GPP3-0035-2018. doi:10.1128/microbiolspec.GPP3-0035-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.GPP3-0035-2018
2019-07-12
2019-10-19

Abstract:

is the best characterized species among the lactococci, and among the most consumed food-fermenting bacteria worldwide. Thanks to their importance in industrialized food production, lactococci are among the lead bacteria understood for fundamental metabolic pathways that dictate growth and survival properties. Interestingly, lactococci belong to the Streptococcaceae family, which includes food, commensal and virulent species. As basic metabolic pathways (e.g., respiration, metal homeostasis, nucleotide metabolism) are now understood to underlie virulence, processes elucidated in lactococci could be important for understanding pathogen fitness and synergy between bacteria. This chapter highlights major findings in lactococci and related bacteria, and covers five themes: distinguishing features of lactococci, metabolic capacities including the less known respiration metabolism in Streptococcaceae, factors and pathways modulating stress response and fitness, interbacterial dialogue metabolites, and novel applications in health and biotechnology.

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Image of FIGURE 1
FIGURE 1

The phylogenetic tree reveals similarities between lactococci and streptococcal pathogens. A phylogenetic tree built on 16S sequences was constructed directly on the Ribosomal Database interface ( 210 ). Branches with a bootstrap value below 60% are indicated with an asterisk. Respiration capacity (see text) is indicated by a red R. R indicates conditional respiration: for , , and spp., aerobic respiration is activated by exogenous heme. For all spp. and , respiration is activated by exogenous heme and menaquinone. Opportunist pathogens are indicated in bold. , ; , ; , ; , ; , ; , . This figure is based on reference 155 .

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Image of FIGURE 2
FIGURE 2

Basics of fermentation. The NADH/NAD ratio is placed as a central determinant of carbon metabolic choice in ( 56 ). Sugar fermentation generates ATP, which is used for amino acid anabolism. In anaerobic conditions and rapid sugar flux, essentially all sugar is converted to lactate (homolactic fermentation) from pyruvate (glycolysis). When sugar flux is slower, in the presence of sugars other than glucose or lactose or in aerobic growth, mixed acid fermentation may occur. The latter conditions are characterized by lower NADH/NAD ratios than those found during homolactic fermentations. Besides NADH, glycolysis generates ATP and pyruvate from sugar degradation. Pyruvate dehydrogenase (Pdh) provides extra NADH from pyruvate when oxygen is present. Lactate dehydrogenase (Ldh) oxidizes NADH into NAD by conversion of pyruvate into lactate, thus maintaining glycolytic activity during fermentation. When oxygen is present, NADH can be oxidized by the cytoplasmic HO-forming NADH oxidase (NoxE), generating NAD. The ATPase expulses H at the expense of ATP to avoid acidification due to glycolysis. Pyruvate build-up leads to synthesis of acetate or the neutral acetoin and diacetyl (also see Fig. 4 ). This figure is modified from reference 155 .

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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FIGURE 3

Basics of respiration. Refer to Fig. 2 for reactions 1, 2, and 5, which are common to fermentation and respiration (numbering is the same). The membrane respiration chain (RC) comprises an electron donor (putatively encoded by [ 45 , 89 ]), menaquinones (encoded by operon genes or provided exogenously [ 80 ]), and a terminal electron acceptor (the cytochrome oxidase encoded by [ 46 , 211 ]). Heme (red star) must be added exogenously (red arrow) to activate cytochrome oxidase. and lactobacilli with respiration capacity (see Fig. 1 legend) require menaquinones (schematic molecule with green center) and heme to activate respiration. Respiration chain activity results in H expulsion. The ATPase might import H, which generates ATP but with low efficiency ( 47 , 77 ). lacks a complete Krebs cycle. Thus, NADH, which is needed for the respiratory chain, is produced by carbon catabolism. Once phosphorylated, sugar is catabolized to pyruvate via glycolysis with production of ATP and NADH. As the respiration chain consumes NADH, Ldh activity decreases and pyruvic acid accumulates. Pyruvic acid dissociates to pyruvate and a proton, decreasing the internal pH. To avoid acidification, pyruvate/pyruvic acid is converted to acetolactate via acetolactate synthase (Als) and then to the neutral compound acetoin with production of CO. Diacetyl is produced by spontaneous oxidation of acetolactate. This pathway raises the pH and improves cell survival. Some LAB convert acetoin to 2,3-butanediol. Pyruvate may also be converted to acetyl-CoA via pyruvate dehydrogenase (Pdh), providing extra NADH and CO. Acetyl-CoA is further converted to acetate with production of ATP, promoting higher cell density. Acetate, acetoin, diacetyl, and 2,3-butanediol diffuse or are secreted into the medium. This figure is modified from reference 155 .

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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FIGURE 4

Schematic representation of heme-sensing and HrtBA-mediated efflux, which regulate heme homeostasis. In and numerous commensal bacteria, heme is suggested to be taken up by gene products (green ovals) and/or by diffusion through membranes ( 75 , 82 ). Internalized heme binds to the HrtR repressor, which releases binding to the operon. Consequent activation of results in heme efflux ( 74 ). Red squares, heme.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Image of FIGURE 5
FIGURE 5

Respiration metabolism increases the survival capacity of lactococci. When supplemented with hemin, aerobically grown lactococci can undergo respiration metabolism. As a result, cells stored at 4°C show markedly better survival compared to cells grown aerobically in the absence of heme or in static conditions. Improved survival was also observed when cells were maintained at 30°C. The experiment shown was performed by Karin Vido in the authors’ laboratory.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Image of FIGURE 6
FIGURE 6

Bacterial root formation in semiliquid medium. Bacterial chains (here, an mutant of ; parental strain) diffuse slowly in a semiliquid (0.035% agar) medium. Bacterial dechained mutants diffuse more quickly to form roots. In this experiment, all the roots corresponded to independent mutants in the same gene, , encoding PBP1A (reproduced from Kulakauskas and coworkers [ 144 ]). Note that a similar strategy of semiliquid medium selection was used to uncover the existence of a cell-surface carbohydrate pellicle in ; the system is readily applied to other bacteria ( 137 ).

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Image of FIGURE 7
FIGURE 7

produces menaquinones that cross-feed the opportunist pathogen . Heme is present in the solid medium. A broad horizontal streak of an strain (NEM316) is shown. Spots of cultures of wild type (left) or that is defective for menaquinone synthesis (right) are deposited directly over the streaks. A stimulated growth zone is observed directly surrounding the wild-type strain but not the mutant. From ( 78 ).

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Image of FIGURE 8
FIGURE 8

Respiring can improve survival of nonrespiring bacteria in coculture. Differentially marked wild-type and (nonrespiring mutant) strains were grown separately or together in coculture. Nonrespiring grew less well and showed poor survival when maintained in an aerobic medium with heme over a 3-day period. However, the respiring wild-type strain thrived. In contrast, the strain fared much better when grown in coculture with the wild-type strain, as determined by cell count determinations. From ( 72 ).

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018
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Tables

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TABLE 1

Characteristics of

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0035-2018

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