Elsevier

Current Opinion in Food Science

Volume 31, February 2020, Pages 71-80
Current Opinion in Food Science

Host-adapted lactobacilli in food fermentations: impact of metabolic traits of host adapted lactobacilli on food quality and human health

https://doi.org/10.1016/j.cofs.2020.02.002Get rights and content

Back-slopping of fermentation cultures in food fermentations can ensure stability of fermentation microbiota at the species or even at the strain level over extended periods of time. In contrast to the fermentation organisms in spontaneous food fermentations, which are derived from plant-associated or environmental micro-organisms, dominant micro-organisms in back-slopped fermentations are often recruited from lactic acid bacteria that are associated with insect or vertebrate hosts. Lifestyle-associated metabolic traits that relate to the ecological fitness of lactic acid bacteria in the host environment include biofilm formation through production of exopolysaccharides, acid resistance mediated by urease, glutaminase or glutamate decarboxylase, and polysaccharide hydrolysis mediated by extracellular glucosyl hydrolases. This review will discuss the ecological fitness of these organisms in food fermentations, and relate their specific metabolic properties to the safety, quality, and nutritional properties of food.

Introduction

A substantial proportion of the human diet consists of fermented foods, where the metabolic activity of fermentation micro-organisms determines and maintains the safety and quality of the products. Historically, non-alcoholic food fermentations aimed to improve the digestibility, nutritional value and/or the storage life of products [1]; their unique sensory properties maintained their popularity even when alternative processing methods become available. Fermented foods are not only a source of nutrients but also a major source of dietary micro-organisms if the fermentation organisms are not killed by a cooking or pasteurization step after the fermentation [2].

The microbiota of traditional food fermentations is controlled by the selection of raw materials, the product formula and the fermentation processes, and by back-slopping or the use of starter cultures. Back-slopping, the practice of inoculating a fermentation with a previous batch, profoundly alters the composition of fermentation microbiota when compared to spontaneous fermentations. In spontaneous fermentations, fermentation micro-organisms are selected from those organisms that are associated with the raw material or the processing environment [1,3,4]. In contrast, micro-organisms in back-slopped fermentations are challenged by microbiota of the raw materials in every new batch. Every time the raw material or the processing environment introduces a new strain that is more competitive than resident strains, the latter will be out-competed after a few fermentation cycles; a process that results eventually in stabilization of fermentation microbiota after a sufficient number of fermentation cycles [5••]. Once stabilization of fermentation microbiota is achieved, back-slopping maintains undefined, mixed cultures over decades or centuries with remarkable stability at the species or even strain level [5••,6••].

Section snippets

Back-slopping of food fermentations recruits host-adapted fermentation organisms

The origin of fermentation micro-organisms in back-slopped food fermentations and hence the source of ‘contamination’ or inoculation with desirable fermentation organisms is in many cases enigmatic. For example, the microbial community of surface-ripened cheeses, which includes Staphylococcus, Brevibacterium, and Corynebacterium species, is independent of the geographic location but resembles human skin microbiota [1,7,8]; experimental evidence for a human origin of cheese rind microbiota,

Species of host-adapted lactobacilli prevalent in fermented foods

Fermentation control by back-slopping is commonly used in dairy fermentations including cheese cultures, yoghurt, kefir and other fermented milk beverages, and in many cereal fermentations including sourdough fermentations, several African fermentations for production of porridges or beverages, and mash fermentations for production of vinegar or liquor in East Asia [1,16]. Owing to their importance in fermentation control, seed cultures that are used in back-slopped fermentations often have a

Metabolic properties in host-adapted lactobacilli associated with fermented food

Host-adapted lactobacilli harbour lifestyle-associated metabolic traits, including acid resistance, biofilm formation, extracellular hydrolysis of polysaccharides, bacteriocin producing and tetracycline resistance. An overview on metabolic properties of host-adapted lactobacilli that relate to their adaptation to the host is provided in Figure 1.

Acid resistance system is essential for competitiveness of vertebrate-host adapted organisms as colonization of a new host by oral or intestinal

The contribution of metabolic traits in host-adapted lactobacilli to food quality

The metabolic traits of host-adapted lactobacilli that contribute to the flavour, structure, and quality of fermented food are shown in Table 2. Glutamine and glutamate metabolism enhance bread quality by generating glutamate and γ-aminobutyric acid (GABA), respectively. The glutaminase mediated glutamate accumulation exceeds the taste threshold in bread and ripened cheese and thus contributes to the umami taste [72,73]. Dietary GABA has relaxing properties [74,75]. In baked goods, arginine

Note added in proof

The taxonomy of the genus Lactobacillus was revised at the proof stage [111]. This communication uses current nomenclature and mentions the previous classification in brackets on first mention. The generic term “lactobacilli” refers to all species that were classified as Lactobacillus species until 2020.

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Qing Li and Michael Gänzle acknowledge the China Scholarship Council and the Canada Research Chairs program, respectively, for funding. Fazer Oy, the Alberta Wheat Commission, and the Saskatchewan Wheat Development Commission are acknowledged for financial support.

References (111)

  • J. Aires et al.

    Tetracycline resistance mediated by tet(W), tet(M), and tet(O) genes of Bifidobacterium isolates from humans

    Appl Environ Microbiol

    (2007)
  • E. Riboulet-Bisson et al.

    Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota

    PLoS One

    (2012)
  • L. Morelli

    In vitro selection of probiotic lactobacilli: a critical appraisal

    Curr Issues Interstinal Microbiol

    (2000)
  • X.B. Lin et al.

    Genetic determinants of reutericyclin biosynthesis in Lactobacillus reuteri

    Appl Environ Microbiol

    (2015)
  • V.S. Ocaña et al.

    Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain

    Appl Environ Microbiol

    (1999)
  • D. Drider et al.

    The continuing story of class IIa bacteriocins

    Microbiol Mol Biol Rev

    (2006)
  • N. Gómez-Torres et al.

    Prevention of late blowing defect by reuterin produced in cheese by a Lactobacillus reuteri adjunct

    Food Microbiol

    (2014)
  • M. Ávila et al.

    Industrial-scale application of Lactobacillus reuteri coupled with glycerol as a biopreservation system for inhibiting Clostridium tyrobutyricum in semi-hard ewe milk cheese

    Food Microbiol

    (2017)
  • D. Fiocco et al.

    How probiotics face food stress: they get by with a little help

    Crit Rev Food Sci Nutr

    (2019)
  • M.L. Marco et al.

    Health benefits of fermented foods: microbiota and beyond

    Curr Opin Biotechnol

    (2017)
  • X. Zhao et al.

    Impact of probiotic Lactobacillus sp. on autochthonous lactobacilli in weaned piglets

    J Appl Microbiol

    (2018)
  • S.A. Frese et al.

    Comparison of the colonization ability of autochthonous and allochthonous atrains of lactobacilli in the human gastrointestinal tract

    Adv Microbiol

    (2012)
  • J. Rong et al.

    Probiotic and anti-inflammatory attributes of an isolate Lactobacillus helveticus NS8 from Mongolian fermented koumiss microbe-host interactions and microbial pathogenicity

    BMC Microbiol

    (2015)
  • B. Sekwati-Monang et al.

    Microbiological and chemical characterisation of ting, a sorghum-based sourdough product from Botswana

    Int J Food Microbiol

    (2011)
  • J.P. Tamang et al.

    Review: diversity of microorganisms in global fermented foods and beverages

    Front Microbiol

    (2016)
  • M.G. Gänzle

    Fermented foods

  • J.M. Lang et al.

    The microbes we eat: abundance and taxonomy of microbes consumed in a day’s worth of meals for three diet types

    PeerJ

    (2014)
  • F. Pswarayi et al.

    Composition and origin of the fermentation microbiota of mahewu, a Zimbabwean fermented cereal beverage

    Appl Environ Microbiol

    (2019)
  • O. Erkus et al.

    Multifactorial diversity sustains microbial community stability

    ISME J

    (2013)
  • B.E. Wolfe et al.

    Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity

    Cell

    (2014)
  • K. Findley et al.

    Topographic diversity of fungal and bacterial communities in human skin

    Nature

    (2013)
  • Q.S. McFrederick et al.

    Flowers and wild megachilid bees share microbes

    Microb Ecol

    (2017)
  • S.A. Frese et al.

    The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri

    PLoS Genet

    (2011)
  • M.M. O’ Donnell et al.

    Lactobacillus ruminis strains cluster according to their mammalian gut source

    BMC Microbiol

    (2015)
  • H.M.B. Harris et al.

    Phylogenomics and comparative genomics of Lactobacillus salivarius, a mammalian gut commensal

    Microb Genomics

    (2017)
  • R.M. Duar et al.

    Experimental evaluation of host adaptation of Lactobacillus reuteri to different vertebrate species

    Appl Environ Microbiol

    (2017)
  • M.S.-W. Su et al.

    Intestinal origin of sourdough Lactobacillus reuteri isolates as revealed by phylogenetic, genetic, and physiological analysis

    Appl Environ Microbiol

    (2012)
  • R.W. Hutkins

    Microbiology and Technology of Fermented Foods

    (2019)
  • M. van de Guchte et al.

    The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution

    PNAS

    (2006)
  • W. Wang et al.

    Metagenomic reconstructions of gut microbial metabolism in weanling pigs

    BMC Microbiome

    (2019)
  • T. Lähteinen et al.

    Probiotic properties of Lactobacillus isolates originating from porcine intestine and feces

    Anaerobe

    (2010)
  • O. Biology et al.

    Role of Streptococcus mutans in human dental decay

    Microbiol Rev

    (1986)
  • L.S. Weyrich et al.

    Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus

    Nature

    (2017)
  • B. Couvigny et al.

    Identification of new factors modulating adhesion abilities of the pioneer commensal bacterium Streptococcus salivarius

    Front Microbiol

    (2018)
  • J.A. Krumbeck et al.

    Characterization of the ecological role of genes mediating acid resistance in Lactobacillus reuteri during colonization of the gastrointestinal tract

    Environ Microbiol

    (2016)
  • S. Kakimoto et al.

    Isolation and taxonomic characterization of acid urease-producing bacteria

    Agric Biol Chem

    (1989)
  • Y.Y.M. Chen et al.

    Dual functions of Streptococcus salivarius urease

    J Bacteriol

    (2000)
  • D. Mora et al.

    Urease biogenesis in Streptococcus thermophilus

    Res Microbiol

    (2005)
  • Y.Y.M. Chen et al.

    Transcriptional regulation of the Streptococcus salivarius 57.I urease operon

    J Bacteriol

    (1998)
  • Q. Li et al.

    Contribution of glutaminases to glutamine metabolism and acid resistance in Lactobacillus reuteri and other vertebrate host adapted lactobacilli

    Food Microbiol

    (2020)
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