当前位置：文档库 › Production of Aroma Compounds in Lactic Fermentations

Production of Aroma Compounds in Lactic Fermentations

Click here for quick links to Annual Reviews content online, including:

? Other articles in this volume ? Top cited articles

? Top downloaded articles ? Our comprehensive search

Further

ANNUAL REVIEWS

INTRODUCTION

Lactic acid bacteria (LAB)constitute a group of Gram-positive nonsporulating bacteria belonging to the phylum of Firmicutes.Many species of LAB are found in association with food products,either as spoilage organisms or as abundant members of the microbiota of naturally fermented food products (Leroy &de Vuyst 2004).The main functionality of LAB in food fermentation processes is the rapid acidi?cation of the food matrix.This process is caused by the fast conversion of fermentable carbohydrates into mainly lactic acid but also other organic acids such as acetic acid,formic acid,and ethanol.The rapid acidi?cation of the food matrix and,simultaneously,the fast consumption of readily fermentable sugars are two main factors that determine the competitive edge of LAB in nutrient-rich environments such as fermentable food raw materials.These raw materials can be of animal (milk,meat)or plant (cereals,fruits,etc.)origin.Under optimal fermen-tation conditions,LAB can rapidly become the most abundant group of microorganisms in these niches (Schoustra et al.2013,Park et al.2012,Prins et al.2010).The low pH and relatively high concentration of organic acids explain the long shelf life of LAB-fermented food products,given that these conditions inhibit the growth of groups of competing microbes.Consequently,LAB fer-mentation not only impacts the shelf life but also improves the microbial safety of fermented food products by the acidi?cation and production of antimicrobial metabolites,which create a physico-chemical environment that prevents the growth of potential spoilage and pathogenic organisms.In addition to these two fundamental,or primary,functionalities of fermented food products (i.e.,extended shelf life and microbial safety),LAB also introduce activities in the food matrix that drive the production of various secondary functionalities,such as texture,nutritional value,and aroma.The delivery of these functionalities of fermented food products depends on metabolic activities of the fermenting microbes,which alter the chemical composition of the fermentable food raw material.

This review focuses on recent developments in the research on the production of aroma com-pounds by LAB in fermented food products.We discuss the various precursor molecules for the formation of aroma compounds in connection with the metabolic pathways involved.The roles of nonmetabolic properties such as cell lysis are discussed in relation to aroma formation.Finally,we review the literature for methods to steer and control aroma formation by LAB in de?ned and mixed culture fermentations.

AROMA COMPOUNDS AND THEIR METABOLIC PRECURSORS

Flavor formation in food fermentation processes is caused by the accumulation of volatile and non-volatile aroma compounds as well the formation of compounds that are related to taste (bitterness,umami,sweetness,sourness,and saltiness).The compounds responsible for aroma constitute var-ious categories (chemical classes)of compounds such as alcohols,aldehydes,ketones,fatty acids,esters,and sulfur compounds (Engels et al.1997).Additionally,as with their chemical natures,the origins of the (bio)chemical precursors of these aroma compounds are diverse.All three main constituents of food materials (i.e.,proteins,carbohydrates,and lipids)deliver precursors for the conversion to aroma compounds.Most of the formation routes of aroma compounds in LAB rely on the presence of functional metabolic pathways,rather than single-enzyme conversions.Taste-related metabolites produced in food fermentation processes belong to different chemical compound classes.Some examples are amino acids (sweetness,umami),oligopeptides (bitterness),and simple organic acids (sourness).This review focuses primarily on the formation of aroma compounds rather than taste compounds and also describes the formation of taste and aroma compounds that share parts of the same metabolic pathway.

314

Smid

Kleerebezem

A n n u . R e v . F o o d S c i . T e c h n o l . 2014.5:313-326. D o w n l o a d e d f r o m w w w .a n n u a l r e v i e w s .o r g A c c e s s p r o v i d e d b y S h a n g h a i J i a o t o n g U n i v e r s i t y o n 12/21/15. F o r p e r s o n a l u s e o n l y .

EXTRACELLULAR ENZYMATIC CONVERSIONS

Aroma formation is a complex process that can be separated into two subprocesses:(a )the gen-eration of precursor molecules and (b )the conversion of the precursor molecules into the actual aroma compounds.These two processes do not always take place in the same compartment.For instance,if the precursors are not synthesized by the microorganisms,but rather are recruited from the medium or food matrix,the ?rst part of the process is operational outside the cell and depends on either secreted enzymes or sometimes enzymes released by cell lysis.(We discuss the role of cell lysis in the next paragraph.)Subsequent steps in this process rely on the transport of precursor molecules into the cell followed by their intracellular conversion.The breakdown of milk proteins (caseins)by dairy LAB during cheesemaking is an example of a process that takes place in two compartments:extracellular and intracellular.In general,LAB have multiple amino acid auxotrophies and thus rely on external amino acid sources for growth (Wegkamp et al.2010).The proteins in milk,in particular caseins,ful?ll that role,for instance for Lactococcus lactis,which is used in cheese manufacturing as a starter culture.The caseins are hydrolyzed by a lactococcal,extracellular,cell envelope–bound proteinase (PrtP).This enzyme has a broad speci?city and can produce more than 100different oligopeptides from caseins (Steele et al.2013).These peptides are subsequently transported by dipeptide (Smid et al.1989)and oligopeptide transporters into the cell,where they ?nd their way to an array of intracellular peptidases,which release free amino acids in the cytoplasm (Kunji et al.1996,Smid et al.1991).These amino acids ?rst feed the de novo pro-tein synthesis machinery,thereby supporting growth and maintenance of the LAB residing in the food matrix.In protein-rich environments such as milk,and provided there is suf?cient proteolytic activity,the supply of amino acids from the environment exceeds the biosynthetic requirements of the fermenting LAB.In addition,the amino acid composition of the protein source usually does not match the amino acid composition of the biomass of fermenting microbes.Therefore,the second fate of the liberated amino acids is to be converted by catabolic reactions (Ard ¨o 2006,Smit et al.2005b).Intracellular amino acid catabolism leads to the formation of a broad array of volatile aroma compounds and depends on the presence and activity of various enzymes and metabolic pathways such as the transaminase pathway,the lyase pathway,and also nonenzymatic conversions (Smit et al.2005b).[We discuss in more detail below amino acid degradation and aroma formation;for more information on extracellular proteolytic enzymes in LAB,we refer readers to various reviews published throughout the years (Grif?ths &Tellez 2013,Savijoki et al.2006,Kunji et al.1996).]

AROMA FORMATION AND CELL LYSIS

As mentioned above,not only intact but also lysed LAB cells contribute to the process of aroma formation during the fermentation of food raw materials.Cell lysis results in the release of cy-toplasmic enzymes in the matrices of the fermentable food materials.Many of these released enzymes retain their functionality outside the cell and will continue converting substrates in the food matrix.Proteins,oligopeptides,lipids,fats,and fatty acids are the main substrates in food matrices for cytoplasmic enzymes released by fermenting LAB,which have,potentially,an impact on the aroma pro?le of the fermented food product.

Lysis of LAB is caused by peptidoglycan hydrolases (PGHs)(Steen et al.2005)or by bacteriophages (Samson &Moineau 2013).Examples of PGHs are N-acetylmuramidases,N-acetylglucosaminidase,and endopeptidases,each acting on different bonds in the cell wall peptidoglycan,thereby weakening the cell envelope,which eventually leads to cell lysis (Lortal &Chapot-Chartier 2005).With respect to the role of bacteriophages,virulent phages can lead to

https://www.wendangku.net/doc/2c777664.html, ?Aroma Compounds in Lactic Fermentations

315

cell lysis;induction of prophages residing in the chromosome potentially can lead to cell lysis as well and thus the release of intracellular enzymes (Lortal &Chapot-Chartier 2005).It has been demonstrated that lysis of LAB in dairy starters plays an essential role in the process of cheese maturation,mainly because of the release of intracellular peptidases acting on the oligopeptides derived from partially hydrolyzed caseins (Guldfeldt et al.2001).Genetic engineering studies have aimed to accelerate cheese ripening by constructing strains in which lytic behavior can be controlled by environmental conditions,which when triggered could be shown to release sig-ni?cantly higher amounts of cytoplasmic enzymes into the matrix that would enhance ripening kinetics (Nauta et al.1997,de Ruyter et al.1997).Hydrolysis of peptides indirectly affects aroma formation in,for instance,the cheese matrix.This is done by increasing the pool of free amino acids that are substrates for subsequent catabolism by the remaining intact cells in the product matrix.Furthermore,hydrolysis of peptides by peptidases released from the cytoplasm of lysed starter culture cells directly affects taste by reducing the amount of bitter peptides (Baankreis et al.1995).

Also fat and lipid degradation plays a role in aroma formation in fermented dairy products (Anderson et al.1991).Collins et al.(2003a)provided evidence for the relationship between the extent of starter cell autolysis and the level of lipolysis during cheddar cheese ripening.They measured lipolysis by monitoring the accumulation of free fatty acids (FFA)such as butyric (C4:0),caprylic (C8:0),myristic (C14:0),palmitic (C16:0),stearic (C18:0),oleic (C18:1),and linoleic (C18:3)in the cheese matrix.A correlation was established between the FFA levels in cheese and the starter cultures used for cheese manufacture (Collins et al.2003a).Lipases in the cheese matrix can also originate from the milk or the added rennet (Collins et al.2003b).The actual aroma formation follows after conversion of the FFA into secondary alcohols,organic acids,and lactones (Molimard &Spinnler 1996).

CYTOSOLIC METABOLIC PATHWAYS AND AMINO ACID DEGRADATION

The production of speci?c ?avor pro?les depends strongly on the conversion of amino acids into various alcohols,aldehydes,acids,esters and sulfur compounds.These conversions depend on the (sequential)activity of a variety of cytoplasmic enzymes (see Smit et al.2005b for a review).

An important priming reaction in ?avor forming pathways is involving pyridoxal-5 -phosphate-dependent aminotransferases that form the amino acid–derived α-ketoacids.The α-ketoacids can be regarded as central intermediates in ?avor forming pathways and can be converted into their corresponding aldehydes,carboxylic acids,and alcohols,and their related (thio)esters (Figure 1).The conversion of amino acids into their cognate alcohols was ?rst analyzed in yeast,more than a century ago,and was designated the Ehrlich pathway (Ehrlich 1907).Table 1lists the most important ?avor compounds derived from speci?c amino acids that are formed via the α-ketoacid pathways.Most of these reactions are catalyzed by speci?c enzymes;however,some chemical interconversions have also been reported,including the formation of benzaldehyde from the phenylalanine-derived phenylpyruvic acid (Nierop Groot &de Bont 1998,1999).The (reactive)aldehydes that are formed are subject to further conversions into alcohols by dehydrogenation or into carboxylic acids by hydrogenation (Figure 1).The carboxylic acids can then be esteri?ed by speci?c esterases,leading to the formation of (thio)esters (Figure 1).These pathways have been reviewed extensively;we refer the reader to Smit et al.(2005a)for one such example.Recent studies have focused on the high-throughput enzyme screening of different LAB strains (Smit et al.2004,O’Flaherty &Klaenhammer 2011),striving to identify strains with high-(or low-)level activity for speci?c enzymes that may be employed to produce fermented products with enhanced ?avor

316

Smid

Kleerebezem

Among the amino acids,the sulfur-containing amino acid methionine is an important sub-strate for the production of several cheese ?avor components such as methanethiol,dimethyldi-sul?de,dimethyltrisu?de,3-methylthio propanal,and thioesters.Methionine conversion into methanethiol can be achieved via the canonical transaminase reaction that generates its corre-sponding α-ketoacid [α-keto methylthio butyric acid (KMBA)](Figure 1).KMBA conversion into methanethiol can take place via a chemical reaction or,alternatively,via KMBA decar-boxylation into the corresponding aldehyde (3-methylthio propanal),which can again lead to methanethiol via an enzyme-independent chemical reaction.The direct conversion of methio-nine into methanethiol can also be catalyzed by cystathionine β-lyase (CBL;see Figure 1),which produces the important cheese ?avor compound methanethiol (Alting et al.1995,Dias &Weimer 1998)that in turn can be converted into dimethyldisul?de and dimethyltrisu?de via oxidation or thioesters via esterase-catalyzed reactions.The CBL encoding gene (metC )in https://www.wendangku.net/doc/2c777664.html,ctis is located in an operon with the cysteine-synthase encoding cysK gene thereby linking sulfur-containing amino acid biosynthetic and interconversion pathways (Fern′a ndez et al.2000).Expression of the metC-cysK operon was shown to be activated by a LysR-type regulator,CmbR.CmbR-mediated transcription activation involves binding to the coactivator O -acetyl-L-serine,which is the sub-strate for CysK (Fern′a ndez et al.2002,Golic et al.2005).Besides regulating the metC-cysK operon,it has been proposed that CmbR also controls the expression of several amino acid transporters in lactococci and streptococci (Kovaleva &Gelfand 2007).A recent in silico analysis using compar-ative genomics has resulted in a gene regulatory network model for the cysteine and methionine metabolic networks in various LAB,an important next step toward the construction of predictive modeling of ?avor-forming pathway activity in dairy starter cultures (Liu et al.2012).As indicated above,it remains essential to pair these predictive models with in situ expression of the most rele-vant enzymes during the actual production of the fermented food products.The newly developed tools that enable such analyses include an ef?cient recombinase-based in situ expression technology system that exploits luciferase-driven expression detection of in situ gene expression (Bachmann et al.2007,2008,2010)and the microcheese fermentation models (Bachmann et al.2009a).

CITRATE METABOLISM

Citrate can be found in fermentable food products such as fruit,vegetables,and bovine milk.The microbial degradation of citrate leads to the formation of compounds such as diacetyl,acetoin,butanediol,and acetaldehyde,all of which can have profound impacts on the aromas of fermented food products.Few LAB species are capable of utilizing citrate (Hugenholtz 1993).Examples of the few LAB species able to utilize citrate are https://www.wendangku.net/doc/2c777664.html,ctis and Leuconostoc mesenteroides ,which cometabolize citrate with fermentable sugars.Citrate utilization leads to elevated intracellular pools of pyruvate and subsequently a diverse range of metabolites (Bandell et al.1998).Only speci?c variants of https://www.wendangku.net/doc/2c777664.html,ctis (i.e.,https://www.wendangku.net/doc/2c777664.html,ctis https://www.wendangku.net/doc/2c777664.html,ctis biovar diacetylactis)are capable of citrate utilization;this property is linked to the possession of a plasmid-encoded citrate transporter gene (Rademaker et al.2007).Citrate utilization in https://www.wendangku.net/doc/2c777664.html,ctis starts with transport of the tricarboxylic acid by a transporter CitP.This secondary transporter catalyzes electrogenic precursor/product exchange of citrate versus L-lactate during citrate-glucose cometabolism (Pudlik &Lolkema 2012b).After transport into the cell,citrate is converted into oxaloacetate and acetate by the enzyme citrate lyase.Oxaloacetate is further converted by oxaloacetate decarboxylase (CitM),yielding pyruvate and carbon dioxide (Hugenholtz 1993).The subsequent dissipation of pyruvate leads to the production of C4aroma compounds such as diacetyl,acetoin,and 2,3butanediol.Therefore,the presence of citrate-degrading LAB in,for instance,unde?ned dairy starter cultures (Erkus et al.2013)is key for optimal aroma formation.

318

Smid

Kleerebezem

α-Ketoacids

Out

CitP

With regard to the mining of biodiversity,recent investigations of the microbial composition of Zambian traditional fermented nonalcoholic beverages revealed the abundance of various species of LAB (Schoustra et al.2013),which potentially possess interesting aroma-forming activities (van Hylckama Vlieg et al.2006).Selected strains can subsequently enhance ?avor formation when used as adjunct cultures that complement metabolic pathways leading to aroma compounds (Ayad et al.2001,Kieronczyk et al.2003).Using a selection of https://www.wendangku.net/doc/2c777664.html,ctis plant isolates as adjunct cultures in a standard Gouda cheese production process,Bachmann (2009)found a large strain-to-strain variation in the concentration of the key aroma compound 3-methyl-butanal in cheeses ripened for six weeks.

Developments such as advanced genome sequencing and comparative genomics analyses have improved our understanding of the natural diversity within species of bacteria and now provide new opportunities to search for strain-speci?c (metabolic)functions such as aroma formation (Siezen et al.2011).However,conclusions about gene presence/absence in relation to strain functionality can be misleading for various reasons.Genes can be either present in a particular strain but not functional (pseudogenes)or they may not be expressed at all under particular experimental conditions.In both theoretical cases,selected strains,depending on their gene contents,may not deliver the predicted functionality.In situ screening systems such as MicroCheese (Bachmann et al.2009a)can be employed to validate predictions about gene-trait matching (Siezen et al.2011).In fact,the role and function of the lactococcal gene bckad ,which encodes a branched-chain α-ketoacid decarboxylase (BcKAD),were investigated using a wildtype strain and knockout mutant (Bachmann 2009).The wildtype strain https://www.wendangku.net/doc/2c777664.html,ctis B1157is known to express high levels of the BcKAD enzyme,which catalyzes the formation of aldehydes from α-ketoacids such as 3-methylbutanal (Smit et al.2005a).Co-occurrence of the gene bckad with a high concentration of the key aroma compound 3-methylbutanal was demonstrated as well as a one-order-of-magnitude lower concentration of the compound when the knockout strain was used as an adjunct (Bachmann 2009).

Recent investigations (de Bok et al.2011)have demonstrated that even small differences in the initial composition of a starter culture can have profound impacts on the pro?le of aroma compounds produced during fermentation.For instance,the impact of the presence of Lactobacillus delbrueckii subsp.bulgaricus on the pro?le of volatile aroma compounds produced in milk that had been fermented by a proteolytic S.thermophilus strain was still detectable even when the lactobacilli were outnumbered by more than four orders of magnitude (de Bok et al.2011).Interestingly,de Bok et al.(2011)also found high levels of aldehydes and particularly 2-pentanone in milk fermented with Lactobacillus plantarum ,but not in milk fermented by L.plantarum in combination with the traditional yogurt starters.This result suggests that cocultivated yogurt starters either affect production of aroma compounds such as 2-pentanone by L.plantarum or consume these compounds while fermenting the milk.

The actual composition of mixed and complex starter cultures is highly dynamic during the process of dairy fermentation and ripening.For instance,during cheesemaking,the most domi-nant https://www.wendangku.net/doc/2c777664.html,ctis genetic lineage in an unde?ned cheese starter culture was found to have the lowest relative abundance after six weeks of cheese ripening (Erkus et al.2013).This shows that in com-plex cultures,many microbe–microbe interactions are operational and thought to be crucial for obtaining the desired product characteristics (Smid &Lacroix 2013).These microbial interactions are mediated through a variety of metabolic and physiological mechanisms.A classic example of a microbial interaction with a huge impact on fermented product functionality is the stimulation of growth of protease-negative variants (prt ?)of https://www.wendangku.net/doc/2c777664.html,ctis in a cheese starter culture by protease-positive (prt +)variants (Hugenholtz et al.1987).In ecological terminology,this interaction is con-sidered commensalistic because the prt +variants do not experience direct harm from supplying

https://www.wendangku.net/doc/2c777664.html, ?Aroma Compounds in Lactic Fermentations

321

peptides and amino acids to the prt ?variants.However,because prolonged cocultivation of the two variants potentially leads to a sharp increase in the relative abundance of the prt ?variant (Bachmann et al.2011),commensalism gradually turns into parasitism (Smid &Lacroix 2013).This type of cooperative behavior is spread widely in microbial populations.By using multiple ex-perimental approaches and modeling population dynamics,Bachmann et al.(2011)demonstrated that the persistence of the proteolytic trait is determined by the fraction of the generated pep-tides that can be captured by the cell before diffusing away from it.This mechanism explains the evolutionary stability of many extracellular substrate-degrading enzymes (Bachmann et al.2011).The examples presented above show that the ?avor (i.e.,aroma and taste)of fermented (dairy)products can be steered in desired directions providing suf?cient knowledge of the (a )culture composition of fermenting LAB,(b )gene contents of the microbes involved,(c )population dy-namics in the culture,(d )time-resolved in situ gene expression during the production process,and ?nally (e )presence of validated in situ screening models.

CONCLUDING REMARKS AND FUTURE PROSPECTS

The formation of aroma compounds in food fermentation processes relies on the concerted action of two different microbial processes:the activities of (a )various enzymes that are mostly secreted in the food matrix by the fermenting microbes and (b )complete metabolic pathways present in intact and metabolically active microbial cells.The technological progress made in high-throughput analysis methods (the omic techniques)(Smid &Hugenholtz 2010,O’Flaherty &Klaenhammer 2011)and the use of genome-scale metabolic models (Flahaut et al.2013)have been driving the development of new approaches to understand,control,and steer aroma formation in (dairy)fermentation processes.This has led to the notion that the strain diversity at the level of gene content,within bacterial species,is very large (Bayjanov et al.2010).Firstly,extensive genome sequencing programs have revealed a large difference in size between the core genome and the pangenome of a species (Broadbent et al.2012,Erkus et al.2013,Hao et al.2011).Niche adaptation combined with a variety of mechanisms enabling horizontal gene transfer (plasmid mobility,insertion sequence elements,phage transduction)is responsible for the process of gene-content diversi?cation.In fermentation processes,employed for centuries,microbes have evolved through domestication,which is demonstrated by genome decay,loss and gain of metabolic pathways,acquisition of genomic elements,and various bene?cial mutations that provide an advantage for the microbes in the nutrient-rich food environments (Douglas &Klaenhammer 2010,Bachmann et al.2012).Second,producers of fermented (dairy)products and starter cultures have increased their efforts to extend culture collections,allowing them to utilize the existing biodiversity.For instance,dairy companies now show great interest in LAB isolated from a variety of nondairy sources such as (decaying)plant material (Siezen et al.2010,2011)and naturally fermented meat.Third,by combining metagenomics,high-throughput DNA ?ngerprinting of isolates,and whole genome sequencing,our knowledge of the composition and function of domesticated complex starter cultures has increased (Erkus et al.2013),allowing us to reconstitute traditional starter cultures and subsequently steer the relative abundance of genetic lineages of fermenting microbes responsible for the production of particular aroma compounds.Finally,knowledge of population dynamics in mixed cultures and underlying mechanisms such as phage-predation related stability (Erkus et al.2013)and exchange of nutrients and metabolites (Sieuwerts et al.2010,Bachmann et al.2011)is crucial for designing stable,high-performance mixed cultures constituting a selection of strains,which in concert and on the basis of their predicted gene contents deliver the required functionalities.

322

Smid

Kleerebezem

DISCLOSURE STATEMENT

The authors are not aware of any af?liations,memberships,funding,or ?nancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This work is associated with the Kluyver Center for Genomics of Industrial Fermentation,which is ?nancially supported by the Netherlands Genomics Initiative.LITERATURE CITED

Alting AC,Engels WJM,Van Schalkwijk S,Exterkate FA.1995.Puri?cation and characterization of cystathio-nine (beta)-lyase from Lactococcus lactis subsp.cremoris B78and its possible role in ?avor development in cheese.Appl.Environ.Microbiol.61:4037–42

Anderson M,Heeschen W,Jellema A,Kuzdzal-Savoie S,Needs EC,et al.1991.Determination of free fatty

acids in milk and milk products.Int.Dairy Fed.Bull.265:3–52Ard ¨o Y.2006.Flavour formation by amino acid catabolism.Biotechnol.Adv.24:238–42

Ayad EH,Verheul A,Engels WJ,Wouters JT,Smit G.2001.Enhanced ?avour formation by combination of

selected lactococci from industrial and artisanal origin with focus on completion of a metabolic pathway.J.Appl.Microbiol.90:59–67

Baankreis R,van Schalkwijk S,Alting AC,Exterkate FA.1995.The occurrence of two intracellular oligoen-dopeptidases in Lactococcus lactis and their signi?cance for peptide conversion in cheese.Appl.Microbiol.Biotechnol.44:386–92

Bachmann H.2009.Regulatory and adaptive responses of Lactococcus lactis in situ.PhD thesis,Wagening.Univ.,

Wageningen,Neth.

Bachmann H,de Wilt L,Kleerebezem M,van Hylckama Vlieg JE.2010.Time-resolved genetic responses

of Lactococcus lactis to a dairy environment.Environ.Microbiol.12:1260–70

Bachmann H,Kleerebezem M,van Hylckama Vlieg JE.2008.High-throughput identi?cation and validation

of in situ-expressed genes of Lactococcus lactis .Appl.Environ.Microbiol.74:4727–36

Bachmann H,Kruijswijk Z,Molenaar D,Kleerebezem M,van Hylckama Vlieg JET.2009a.A high-throughput

cheese manufacturing model for effective cheese starter culture screening.J.Dairy Sci.92:5868–82

Bachmann H,Molenaar D,Kleerebezem M,van Hylckama Vlieg JE.2011.High local substrate availability

stabilizes a cooperative trait.ISME J.5:929–32

Bachmann H,Santos F,Kleerebezem M,van Hylckama Vlieg JE.2007.Luciferase detection during stationary

phase in Lactococcus lactis .Appl.Environ.Microbiol.73:4704–6

Bachmann H,Starrenburg MJ,Dijkstra A,Molenaar D,Kleerebezem M,et al.2009b.Regulatory phenotyping

reveals important diversity within the species Lactococcus lactis .Appl.Environ.Microbiol.75:5687–94

Bachmann H,Starrenburg MJ,Molenaar D,Kleerebezem M,van Hylckama Vlieg JE.2012.Microbial do-mestication signatures of Lactococcus lactis can be reproduced by experimental evolution.Genome Res.22:115–24

Bandell M,Lhotte ME,Marty-Teysset C,Veyrat A,Pr′e vost H,et al.1998.Mechanism of the citrate trans-porters in carbohydrate and citrate cometabolism in Lactococcus and Leuconostoc species.Appl.Environ.

Microbiol.64:1594–600

Bayjanov JR,Siezen RJ,van Hijum SA.2010.PanCGHweb:a web tool for genotype calling in pangenome

CGH data.Bioinformatics 26:1256–57

Broadbent JR,Neeno-Eckwall EC,Stahl B,Tandee K,Cai H,et al.2012.Analysis of the Lactobacillus casei

supragenome and its in?uence in species evolution and lifestyle adaptation.BMC Genomics 13:533

Chaves AC,Fernandez M,Lerayer AL,Mierau I,Kleerebezem M,Hugenholtz J.2002.Metabolic engineering

of acetaldehyde production by Streptococcus thermophilus .Appl.Environ.Microbiol.68:5656–62

Collins YF,McSweeney PL,Wilkinson MG.2003a.Evidence of a relationship between autolysis of starter

bacteria and lipolysis in cheddar cheese during ripening.J.Dairy Res.70:105–13

https://www.wendangku.net/doc/2c777664.html, ?Aroma Compounds in Lactic Fermentations

323

Collins YF,McSweeney PL,Wilkinson MG.2003b.Lipolysis and free fatty acid catabolism in cheese:a review

of current knowledge.Int.Dairy J.13:841–66

de Bok FA,Janssen PW,Bayjanov JR,Sieuwerts S,Lommen A,et al.2011.Volatile compound ?ngerprinting

of mixed-culture fermentations.Appl.Environ.Microbiol.77:6233–39

de Ruyter PG,Kuipers OP,Meijer WC,de Vos WM.1997.Food-grade controlled lysis of Lactococcus lactis

for accelerated cheese ripening.Nat.Biotechnol.15:976–79

Dias B,Weimer B.1998.Conversion of methionine to thiols by lactococci,lactobacilli,and brevibacteria.

Appl.Environ.Microbiol.64:3320–26

Douglas GL,Klaenhammer TR.2010.Genomic evolution of domesticated microorganisms.Annu.Rev.Food

Sci.Technol.1:397–414

Ehrlich F.1907.¨Uber die Bedingungen der Fusel ¨olbindungen und ¨

uber ihnen Zusammenhang mit dem Eiweissaufbau der Hefe.Ber.Deutsch Chem.Gesells.40:1027–47

Engels WJM,Dekker R,de Jong C,Neeter R,Visser S.1997.A comparative study of volatile compounds in

the water-soluble fraction of various types of ripened cheese.Int.Dairy J.7:255–63

Erkus O,de Jager VC,Spus M,van Alen-Boerrigter IJ,van Rijswijck IM,et al.2013.Multifactorial diversity

sustains microbial community stability.ISME J.7:2126–36Fern′a ndez M,Kleerebezem M,Kuipers OP,Siezen RJ,van Kranenburg R.2002.Regulation of the metC-cysK

operon,involved in sulfur metabolism in Lactococcus lactis .J.Bacteriol.184:82–90Fern′a ndez M,van Doesburg W,Rutten GA,Marugg JD,Alting AC,et al.2000.Molecular and functional

analyses of the metC gene of Lactococcus lactis ,encoding cystathionine β-lyase.Appl.Environ.Microbiol.66:42–48

Flahaut NAL,Wiersma A,van de Bunt B,Martens DE,Schaap PJ,et al.2013.Genome-scale metabolic

model for Lactococcus lactis MG1363and its application to the analysis of ?avor formation.Appl.Microbiol.Biotechnol.97:8729–39

Golic N,Schliekelmann M,Fern′a ndez M,Kleerebezem M,van Kranenburg R.2005.Molecular characteriza-tion of the CmbR activator-binding site in the metC-cysK promoter region in Lactococcus lactis .Microbiology

151:439–46

Grif?ths MW,Tellez https://www.wendangku.net/doc/2c777664.html,ctobacillus helveticus :the proteolytic system.Front.Microbiol.4:30

Guldfeldt LU,Sorensen KI,Stroman P,Behrndt H,Williams D,Johansen E.2001.Effect of starter cultures

with a genetically modi?ed peptidolytic or lytic system on cheddar cheese ripening.Int.Dairy J.11:373–82Guo T,Kong J,Zhang L,Zhang C,Hu S.2012.Fine tuning of the lactate and diacetyl production through

promoter engineering in Lactococcus lactis .PLoS One 7:e36296

Hao P,Zheng H,Yu Y,Ding G,Gu W,et https://www.wendangku.net/doc/2c777664.html,plete sequencing and pan-genomic analysis of

Lactobacillus delbrueckii subsp.bulgaricus reveal its genetic basis for industrial yogurt production.PLoS One 6:e15964

Hugenholtz J.1993.Citrate metabolism in lactic acid bacteria.FEMS Microbiol.Rev.12:165–78

Hugenholtz J,Kleerebezem M,Starrenburg M,Delcour J,de Vos W,Hols https://www.wendangku.net/doc/2c777664.html,ctococcus lactis as a cell

factory for high-level diacetyl production.Appl.Environ.Microbiol.66:4112–14

Hugenholtz J,Splint R,Konings WN,Veldkamp H.1987.Selection of protease-positive and protease-negative variants of Streptococcus cremoris .Appl.Environ.Microbiol.53:309–14Imhof R,Gl¨a ttli H,Bosset JO.1995.Volatile organic compounds produced by thermophilic and mesophilic

single strain dairy starter cultures.Lebensm.Wiss.Technol.28:78–86

Kieronczyk A,Skeie S,Langsrud T,Yvon M.2003.Cooperation between Lactococcus lactis and nonstarter

lactobacilli in the formation of cheese aroma from amino acids.Appl.Environ.Microbiol.69:734–39

Kovaleva GY,Gelfand MS.2007.Transcriptional regulation of the methionine and cysteine transport and

metabolism in streptococci.FEMS Microbiol.Lett.276:207–15

Kunji ER,Mierau I,Hagting A,Poolman B,Konings WN.1996.The proteolytic systems of lactic acid

bacteria.Antonie Leeuwenhoek 70:187–221

Lees GJ,Jago GR.1976.Formation of acetaldehyde from threonine by lactic acid bacteria.J.Dairy Res.

43:75–83

Leroy F,de Vuyst https://www.wendangku.net/doc/2c777664.html,ctic acid bacteria as functional starter cultures for the food fermentation industry.

Trends Food Sci.Technol.15:67–78

324

Smid

Kleerebezem

Liu M,Prakash C,Nauta A,Siezen RJ,Francke https://www.wendangku.net/doc/2c777664.html,putational analysis of cysteine and methionine

metabolism and its regulation in dairy starter and related bacteria.J.Bacteriol.194:3522–33

Lortal S,Chapot-Chartier M-P.2005.Role,mechanisms and control of lactic acid bacteria lysis in cheese.

Int.Dairy J.15:857–71

Molimard P,Spinnler HE.1996.Review:Compounds involved in the ?avor of surface mold-ripened cheeses:

origins and properties.J.Dairy Sci.79:169–84

Nauta A,van den Burg B,Karsens H,Venema G,Kok J.1997.Design of thermolabile bacteriophage repressor

mutants by comparative molecular modeling.Nat.Biotechnol.15:980–83

Nierop Groot MN,de Bont JA.1999.Involvement of manganese in conversion of phenylalanine to benzalde-hyde by lactic acid bacteria.Appl.Environ.Microbiol.65:5590–93

Nierop Groot MN,de Bont JAM.1998.Conversion of phenylalanine to benzaldehyde initiated by an amino-transferase in Lactobacillus plantarum .Appl.Environ.Microbiol.64:3009–13

O’Flaherty S,Klaenhammer TR.2011.The impact of omic technologies on the study of food microbes.Annu.

Rev.Food Sci.Technol.2:353–71

Ott A,Fay LB,Chaintreau A.1997.Determination and origin of the aroma impact compounds of yogurt

?avor.J.Agric.Food Chem.45:850–58

Ott A,Germond JE,Chaintreau A.2000.Vicinal diketone formation in yogurt:13C precursors and effect of

branched-chain amino acids.J.Agric.Food Chem.48:724–31

Park EJ,Chun J,Cha CJ,Park WS,Jeon CO,Bae JW.2012.Bacterial community analysis during fermentation

of ten representative kinds of kimchi with barcoded pyrosequencing.Food Microbiol.30:197–204

Prins WA,Botha M,Botes M,de Kwaadsteniet M,Endo A,Dicks https://www.wendangku.net/doc/2c777664.html,ctobacillus plantarum 24,

isolated from the Marula fruit (Sclerocarya birrea ),has probiotic properties and harbors genes encoding the production of three bacteriocins.Curr.Microbiol.61:584–89

Pudlik AM,Lolkema JS.2012a.Rerouting citrate metabolism in Lactococcus lactis to citrate-driven transami-nation.Appl.Environ.Microbiol.78:6665–73

Pudlik AM,Lolkema JS.2012b.Substrate speci?city of the citrate transporter CitP of Lactococcus lactis .

J.Bacteriol.194:3627–35

Pudlik AM,Lolkema JS.2013.Uptake of α-ketoglutarate by citrate transporter CitP drives transamination

in Lactococcus lactis .Appl.Environ.Microbiol.79:1095–101

Rademaker JL,Herbet H,Starrenburg MJ,Naser SM,Gevers D,et al.2007.Diversity analysis of dairy and

nondairy Lactococcus lactis isolates,using a novel multilocus sequence analysis scheme and (GTG)5-PCR ?ngerprinting.Appl.Environ.Microbiol.73:7128–37

Samson JE,Moineau S.2013.Bacteriophages in food fermentations:new frontiers in a continuous arms race.

Annu.Rev.Food Sci.Technol.4:347–68

Savijoki K,Ingmer H,Varmanen P.2006.Proteolytic systems of lactic acid bacteria.Appl.Microbiol.Biotechnol.

71:394–406

Schoustra SE,Kasase C,Toarta C,Kassen R,Poulain AJ.2013.Microbial community structure of three

traditional Zambian fermented products:mabisi,chibwantu and munkoyo.PLoS One 8:e63948

Sieuwerts S,Molenaar D,van Hijum SA,Beerthuyzen M,Stevens MJ,et al.2010.Mixed-culture transcriptome

analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus .Appl.Environ.Microbiol.76:7775–84

Siezen RJ,Bayjanov J,Renckens B,Wels M,van Hijum SA,et https://www.wendangku.net/doc/2c777664.html,plete genome sequence of

Lactococcus lactis https://www.wendangku.net/doc/2c777664.html,ctis KF147,a plant-associated lactic acid bacterium.J.Bacteriol.192:2649–50Siezen RJ,Bayjanov JR,Felis GE,van der Sijde MR,Starrenburg M,et al.2011.Genome-scale diversity

and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays.Microb.Biotechnol.4:383–402

Smid EJ,Driessen AJM,Konings WN.1989.Mechanism and energetics of dipeptide transport in membrane

vesicles of Lactococcus lactis .J.Bacteriol.171:292–98

Smid EJ,Poolman B,Konings WN.1991.Casein utilization by lactococci.Appl.Environ.Microbiol.57:2447–52Smid EJ,Hugenholtz J.2010.Functional genomics for food fermentation processes.Annu.Rev.Food Sci.

Technol.1:497–519

Smid EJ,Lacroix C.2013.Microbe-microbe interactions in mixed culture food fermentations.Curr.Opin.

Biotechnol.24:148–54

https://www.wendangku.net/doc/2c777664.html, ?Aroma Compounds in Lactic Fermentations

325

Smit BA,Engels WJ,Bruinsma J,van Hylckama Vlieg JE,Wouters JT,Smit G.2004.Development of a high

throughput screening method to test ?avour-forming capabilities of anaerobic micro-organisms.J.Appl.Microbiol.97:306–13

Smit BA,van Hylckama Vlieg JE,Engels WJ,Meijer LJ,Wouters T,Smit G.2005a.Identi?cation,cloning,

and characterization of a Lactococcus lactis branched-chain alpha-keto acid decarboxylase involved in ?avor formation.Appl.Environ.Microbiol.71:303–11

Smit G,Smit BA,Engels WJ.2005b.Flavour formation by lactic acid bacteria and biochemical ?avour pro?ling

of cheese products.FEMS Microbiol.Rev.29:591–610

Steele J,Broadbent J,Kok J.2013.Perspectives on the contribution of lactic acid bacteria to cheese ?avor

development.Curr.Opin.Biotechnol.24:135–41

Steen A,Buist G,Horsburgh GJ,Venema G,Kuipers OP,et al.2005.AcmA of Lactococcus lactis is an

N -acetylglucosaminidase with an optimal number of LysM domains for proper functioning.FEBS J.272:2854–68

Sybesma W,Hugenholtz J,de Vos WM,Smid EJ.2006.Safe use of genetically modi?ed lactic acid bacteria

in food.Bridging the gap between consumers,green groups,and industry.Elec.J.Biotechnol.9:424–48Tamime AY,Deeth HC.1980.Yoghurt:technology and biochemistry.J.Food Prot.43:939–77

van Hylckama Vlieg JE,Rademaker JL,Bachmann H,Molenaar D,Kelly WJ,Siezen RJ.2006.Natural

diversity and adaptive responses of Lactococcus lactis .Curr.Opin.Biotechnol.17:183–90

Wegkamp A,Teusink B,de Vos WM,Smid EJ.2010.Development of a minimal growth medium for Lacto-bacillus plantarum .Lett.Appl.Microbiol.50:57–64

326Smid

Kleerebezem

Annual Review of Food Science and Technology Volume 5,2014

Contents

From Tomato King to World Food Prize Laureate

Philip E.Nelson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1Opportunities and Progress

John H.Litch?eld p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 23Body Weight Regulation and Obesity:Dietary Strategies to Improve the Metabolic Pro?le

M.J.M.Munsters and W.H.M.Saris p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 39Delivery of Lipophilic Bioactives:Assembly,Disassembly,and Reassembly of Lipid Nanoparticles

Mingfei Yao,Hang Xiao,and David Julian McClements p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 53Extraction,Evolution,and Sensory Impact of Phenolic Compounds During Red Wine Maceration

L.Federico Casassa and James F.Harbertson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 83Gastric Digestion In Vivo and In Vitro:How the Structural Aspects of Food In?uence the Digestion Process

Gail M.Bornhorst and R.Paul Singh p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111New Developments on the Role of Intramuscular Connective Tissue in Meat Toughness

Peter P.Purslow p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 133Strategies to Mitigate Peanut Allergy:Production,Processing,Utilization,and Immunotherapy Considerations

Brittany L.White,Xiaolei Shi,Caitlin M.Burk,Michael Kulis,

A.Wesley Burks,Timothy H.Sanders,and Jack P.Davis p p p p p p p p p p p p p p p p p p p p p p p p p p p 155Designing Food Structures for Nutrition and Health Bene?ts

Jennifer E.Norton,Gareth A.Wallis,Fotis Spyropoulos,Peter J.Lillford,

and Ian T.Norton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177Nanodelivery of Bioactive Components for Food Applications:

Types of Delivery Systems,Properties,and Their Effect on ADME Pro?les and Toxicity of Nanoparticles

T.Borel and C.M.Sabliov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197

Modern Supercritical Fluid Technology for Food Applications

Jerry W.King p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 215Impact of Diet on Human Intestinal Microbiota and Health

Anne Salonen and Willem M.de Vos p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 239Applications of Power Ultrasound in Food Processing

Sandra Kentish and Hao Feng p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263Nondestructive Measurement of Fruit and Vegetable Quality Bart M.Nicola¨?,Thijs Defraeye,Bart De Ketelaere,Els Herremans,Maarten L.A.T.M.Hertog,Wouter Saeys,Alessandro Torricelli,

Thomas Vandendriessche,and Pieter Verboven p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 285Production of Aroma Compounds in Lactic Fermentations

E.J.Smid and M.Kleerebezem p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 313Phage Therapy in the Food Industry

Lorraine Endersen,Jim O’Mahony,Colin Hill,R.Paul Ross,Olivia McAuliffe,

and Aidan Coffey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 327Public Health Impacts of Foodborne Mycotoxins

Felicia Wu,John D.Groopman,and James J.Pestka p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351Soft Materials Deformation,Flow,and Lubrication Between Compliant Substrates:Impact on Flow Behavior,Mouthfeel,Stability,and Flavor

Nichola Selway and Jason R.Stokes p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 373Metabolic Stimulation of Plant Phenolics for Food Preservation and Health

Dipayan Sarkar and Kalidas Shetty p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 395Indexes

Cumulative Index of Contributing Authors,Volumes 1–5p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415Cumulative Index of Article Titles,Volumes 1–5p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 418Errata

An online log of corrections to Annual Review of Food Science and Technology articles may be found at https://www.wendangku.net/doc/2c777664.html,/errata/food

vi Contents