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Chapter 33 : Fermented Foods

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Abstract:

In fermented foods, microbial and enzymatic conversions determine and maintain food safety and quality. The deliberate use of microorganisms for food production is one of the oldest unit operations in food processing. In this chapter, products, production processes, and fermentation microbiotas are described for major products from tubers, cereals, beans, milk, fish, and meat. In addition, the origins and properties of fermentation microbiota are described, and metabolic pathways that contribute to the quality of fermented foods are discussed.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.1

Periodic table of fermented foods, indicating the diversity of products, fermentation organisms, and raw materials. Fermented foods are grouped by product category and ranked within a group by flavor intensity or ripening time, if applicable. Fermentation organisms that contribute to fermentation are indicated by color coding of specific fields (see the key at the top of the table). Typical organisms, the concentration of relevant metabolites, and the ripening or fermentation times are also indicated. Genus abbreviations used in this chapter are introduced in the figure. Food products are generally listed in the language of origin. The figure is formatted for large-scale (A0) printing; a high-resolution image file is available as “Document” under the Activities tab of the author's homepage at https://www.ualberta.ca/agriculture-life-environment-sciences/about-us/contact-us/facultylecturer-directory/michael-gaenzle. Modified from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.2

Overview of carbohydrate fermentation in lactic acid bacteria. Major end products of metabolism are in boldface type; branching points of metabolism, or metabolic switches, are underlined. The formation of reduced and oxidized cofactors (in white on a blue background and in blue, respectively) is indicated if it occurs upstream or downstream of relevant metabolic branching points; ATP consumption (in white on a red background) and synthesis (in red) are shown to indicate the ATP yield of the metabolic pathway. (A) Homofermentative metabolism of hexoses via the Embden-Meyerhof pathway and alternative fates of pyruvate. The alternative fate of pyruvate depends on the substrate availability, the availability of oxygen, and the pH. (B) Heterofermentative metabolism of hexoses via the phosphoketolase pathway and alternative routes of acetylphosphate. Conversion of acetylphosphate to acetic acid is dependent on alternative routes for regeneration of reduced cofactors (upper right, steps 7 and 8). Enzymes are indicated by numbers as follows: 1, lactate dehydrogenase; 2, pyruvate formate lyase; 3, acetaldehyde dehydrogenase; 4, alcohol dehydrogenase; 5, phosphotransacetylase; 6, acetate kinase; 7, NADH oxidase or NADH peroxidase; 8, mannitol dehydrogenase, glutathione reductase, or alcohol reductase. Modified from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.3
Figure 33.3

Metabolism of organic acids in lactic acid bacteria: alternative fates of citrate and malate in lactic acid bacteria to support pH homeostasis or cofactor regeneration. Major end products of metabolism are in boldface type. The formation of oxidized cofactors is indicated by blue type; ATP synthesis is in red; proton-consuming decarboxylation reactions are on a gray background. Dashed arrows indicate chemical conversions. Tartrate is converted by tartrate dehydratase; citrate is converted to succinate to achieve regeneration of two reduced cofactors or to acetoin to achieve proton consumption and proton motive force generation by two decarboxylation reactions. Tartrate metabolism has been observed only in . Citrate conversion to lactate or acetate and ethanol combines oxidation of 1 mol of NADH and one decarboxylation reaction. Lactobacilli convert citrate to succinate or lactate; converts citrate preferentially via pyruvate formate lyase acetate and ethanol; , spp., and convert citrate to the alternative end product acetoin or lactate. Enzymes are indicated by numbers as follows: 1, tartrate dehydratase; 2, citrate lyase; 3, malate dehydrogenase;4, fumarate hydratase, 5, succinate dehydrogenase; 6, oxaloacetate decarboxylase; 7, malolactic enzyme; 8, lactate dehydrogenase; 9, acetolactate synthase; 10, acetolactate dehydrogenase; 11, pyruvate formate lyase; 12, acetaldehyde dehydrogenase; 13, alcohol dehydrogenase; 14, phosphotransacetylase; 15, acetate kinase. Modified from reference with information from reference 39.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.4
Figure 33.4

Overview of pathways for formation of flavor volatiles by yeasts. Flavor volatiles are shown in red. Drawn using data from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.5

Examples of bioactive secondary metabolites of . (A) The yellow pigments monascin (R = CH) and ankaflavin (R = CH); B, the red pigments rubropunctamine (R = CH) and monascorubramine (R = CH); C, the mycotoxin citrinin; D, monacolin K (lovastatin), a potent inhibitor of cholesterol synthesis in humans. Drawn with data from references and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.6
Figure 33.6

Flow chart for production of cereal wines and spirits. (A) Flow chart for production of Japanese rice wine (sake). Rice is polished, washed, and steamed. A part of the raw material is inoculated with koji, the saccharification starter composed of ; a second part is used with koji for production of the starter containing yeasts and lactic acid bacteria (LAB). Both are combined for the mash fermentation. After completion of the fermentation, the mash is filtered, pasteurized, and aged. (B) Flow chart for production of daqu, the saccharification starter used in Chinese rice wines, spirits, and vinegar fermentations. Cereals are ground, mixed with water to a water content of 40%, and shaped into blocks about 6 by 20 by 30 cm. The blocks are stacked in a fermentation room, and the spontaneous fermentation is controlled by control of the temperature to produce low-temperature daqu (45 to 50°C), medium-temperature daqu (50 to 60°C), or high-temperature daqu (60 to 65°C). After fermentation, daqu is dried, ground, and stored dry. (C) Alcoholic fermentation for production of baijiu. Ground cereals are soaked, cooked, cooled, and fermented after the addition of daqu. Fermentation occurs at ambient temperature in earthen jars or in mud pits that are inoculated with part of the material from the previous batch. For some products, such as sauce-flavored baijiu, a 4- to 5-day aerobic fermentation is conducted prior to anaerobic fermentation in pits. After fermentation, the mash is distilled and the distiller's grains undergo a second fermentation which is again inoculated with daqu and part of a previous batch. The cycle of distillation and fermentation is repeated two to seven times. Drawn with information from references and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.7
Figure 33.7

Degradation of linamarin in cassava fermentations. Linamarin is a toxic cyanogenic β-glucoside that is degraded by linamarase activity of the raw material or by β-glucosidases of lactobacilli (1). The degradation product decomposes spontaneously (2) to the volatile compounds hydrogen cyanide and acetone.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.8
Figure 33.8

Flow charts for production of selected cereal beverages. Shown are processes for production of mahewu (Zimbabwe and South Africa), kvass (Russia), and bushera (Uganda). Kvass is alternatively produced with rye malt and boiled rye flour. Drawn with information from references , and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.9
Figure 33.9

Flow charts for production of selected cereal porridges. Shown are processes for production of ting (Botswana and South Africa), idli (India and Sri Lanka), and koko (Ghana). Drawn with information from references , and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.10
Figure 33.10

Metabolism of phenolic acids by lactic acid bacteria using the example of coumaric acid metabolism by . Protein numbers refer to the genome sequence of WCFS1 (GenBank accession number NC_004567.2).

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.11
Figure 33.11

Schematic representation of type I (A) and type II (B) sourdough fermentation processes. Times indicate typical fermentation times for each fermentation step; the percentage values indicate the percentage of the flour in the bread recipe that is fermented at a specific step. Type I sourdoughs are propagated for use as the sole leavening agent; this necessitates the use of two to four fermentation cycles per batch of bread, which uses an increasing proportion of the flour. Fermentations are conducted at an ambient temperature of 15 to 30°C. Sourdoughs are maintained by use of a small proportion of the last sourdough or the bread dough as the inoculum for the next fermentation cycle. Type II sourdoughs are generally fermented at a higher temperature (30 to >40°C); if the fermentation is carried out by ingredient suppliers, type II doughs are pasteurized, dried, or refrigerated prior to use in the bakery.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.12
Figure 33.12

Flow chart for production of Japanese soy sauce (A) and miso (B). Koji fermentation by generates saccharolytic and proteolytic enzymes that hydrolyze starch and proteins in the subsequent mash (moromi) fermentation. The high salt concentration selects for the halophilic organism as the dominant bacterial representative of the moromi microbiota; and other halophilic yeasts contribute to ethanol and flavor formation. Products in other East Asian countries use cooked soybeans as the sole ingredient and employ salt concentrations of up to 27%. Drawn with information from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.13
Figure 33.13

Schematic representation of the typical succession of fermentation microbiota in spontaneous plant fermentations, including most cereal fermentations, sauerkraut or kimchi, and olives (the usual suspects). Plant-associated include , , , and ; among lactococci and enterococci, , , and are most frequently observed. Later fermentation stages include growth of , , , and . and are lactate-utilizing spoilage organisms. Drawn with information from references , and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.14

Production of diacetyl by lactic starter cultures. Enzymes are indicated by numbers as follows: 1, citrate lyase; 2, oxaloacetate decarboxylase; 3, lactate dehydrogenase; 4, acetolactate synthase; 5, diacetyl/acetoin reductase; 6, NADH oxidase or NADH peroxidase. The formation of reduced and oxidized cofactors (in white on a blue background and in blue, respectively) is indicated if it occurs upstream or downstream of relevant metabolic branching points. Drawn with information from references and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.15
Figure 33.15

Synthesis of exopolysaccharides by intracellular glycosyltransferases. Shown is the example of exopolysaccharide synthesis in B40. (1) The priming glycyltransferase links glucose to the membrane-bound lipid carrier undecaprenyl phosphate using UDP-glucose as the substrate. (2 to 5) Successive activity of the glycosyltransferases EpsE, EpsF, EpsG, EpsH, EpsH, and EpsJ assembles the repeating unit of the EPS, with UDP-glucose, UDP-galactose, and dTDP-rhamnose as substrates. (6) EpsK translocates the repeating unit, which is then (7) polymerized by EpsI with EpsA and EpsB, determining the chain length. The lipid carrier is retranslocated and dephosphorylated. Drawn using data from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.16
Figure 33.16

Overview of basic processing steps during cheese production. Variables related to processing steps are on the left; variables related to fermentation microbiota are on the right.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.17

Mechanisms of phage resistance in dairy starter cultures. (A) Inhibition of adsorption by masking or modification of the phage receptor, which is usually a surface polysaccharide. (B) Inhibition of transfer of phage DNA into the host cytoplasm by membrane-associated Sie-like proteins ( and ). (C and D) Cutting of phage nucleic acids by restriction-modification systems, which recognize DNA methylation patterns, or by CRISPR-Cas systems, which recognize proto-spacer sequences of the phage DNA. (E) Inhibition of replication of the phage DNA or of phage assembly by abortive infection (Abi) systems. In , 23 different Abi systems have been described; these are generally plasmid encoded and interfere with DNA replication, RNA transcription, or packaging of the phage DNA. Abi systems also lead to the death of the infected cell. Drawn with information from references and and icons from https://www.flaticon.com.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.18
Figure 33.18

Lactate and aspartate metabolism by propionibacteria. The oxidizing branch of the pathway converts lactate to acetate and CO via lactate dehydrogenase (1), pyruvate dehydrogenase (2), and phosphotransacetylase/acetate kinase. This branch generates 2 mol of NADH (indicated as [H]) and ATP. The reducing branch of the pathway (Wood-Werkman cycle) consumes 2 mol of NADH by conversion of pyruvate to propionate via oxaloacetate transcarboxylase (3), fumarate reductase (4), and CoA transferase (5). Fumarate reductase may be linked to an anaerobic electron transfer chain that contributes to ATP synthesis. Cometabolism of aspartate and lactate via aspartate-ammonia lyase (aspartase) (6) provides an alternative route for cofactor regeneration and accumulates succinate as the end product. The formation of reduced and oxidized cofactors (in white on a blue background and in blue, respectively) is indicated if it occurs upstream or downstream of relevant metabolic branching points; synthesis (in red) is shown to indicate the ATP yield of the metabolic pathway. Drawn using data from references and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.19
Figure 33.19

Proteolytic system of lactic acid bacteria. Protein degradation is initiated by extracellular and cell wall-bound proteases that are present in some lactic acid bacteria, particularly strains that dominate dairy fermentations, but absent in most species of lactobacilli. Peptides are transported by the dipeptide transporters DtpT and DtpP or the oligopeptide transporter Opp and hydrolyzed by a strain-specific array of intracellular peptidases. Drawn according to information from references , and .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Figure 33.20

Glutamine and glutamate metabolism in lactic acid bacteria. “[H]” indicates NAD(P)H-consuming or -generating reactions; individual enzymes are indicated by numbers and discussed below. Amino acids are taken up as peptides and cleaved by an array of intracellular peptidases; glutamate and glutamine are additionally transported by the Gln- or Glu-γ-aminobutyrate (GABA) antiporter GadC. (1) Glutamine is converted to glutamate by glutaminase of glutamine amidotransferases. (2) Strain-specific conversion of glutamate to GABA. (3) Heterofermentative lactobacilli convert glutamate to γ-glutamyl peptides via glutamyl-cysteine ligase. (4) NADH-dependent conversion of glutamate to α-ketoglutarate (αKG) by glutamate dehydrogenase is a strain-specific property of , , and other LAB. (5) LAB generally exhibit transaminase activity and convert αKG to glutamate in the presence of other amino acids as amino donors. (6) Heterofermentative lactobacilli convert αKG to α-hydroxyglutarate. The formation of reduced and oxidized cofactors (in white on a blue background and in blue, respectively) is indicated if it occurs upstream or downstream of relevant metabolic branching points; proton-consuming decarboxylation of deamidation reactions is on a gray background. Modified from reference .

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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Image of Figure 33.21
Figure 33.21

Basic processing steps for production of dry-cured ham (A) and dry-cured sausage (B). Ham is produced from whole-muscle pork meat; pork is also a major ingredient in sausage production, but product formulas may additionally include beef and/or horse and donkey meat. Sausages are generally cured with nitrite or nitrate, but not all hams are cured with nitrite or nitrate. Fermentation microbiotas in sausage production are introduced by back-slopping or by use of starter cultures or derived from house microbiota of the production facility.

Citation: Gänzle M. 2019. Fermented Foods, p 855-900. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch33
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