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The Role and Application of Enterococci in Food and Health

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The Role and Application of Enterococci in Food and Health International Journal of Food Microbiology 106 (2006) 1 – 24 www.elsevier.com/locate/ijfoodmicro Review The role and application of enterococci in food and health M.R. Foulquie´ Moreno a,1, P. Sarantinopoulos b,1,2, E. Tsakalidou b, L. De Vuyst a,* a Research Group of Industrial Microbiology, Fermentation Technology and Downstream Processing (IMDO), Department of Applied Biological Sciences and Engineering, Vrije Universiteit Brussel (VUB), Pleinlaan 2, B-1050 Brussels, Belgium b Laboratory of Dairy Research, Department of Food Science and Technology, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece Received 19 February 2005; accepted 5 June 2005 Abstract The genus Enterococcus is the most controversial group of lactic acid bacteria. Studies on the microbiota of many traditional cheeses in the Mediterranean countries have indicated that enterococci play an important role in the ripening of these cheeses, probably through proteolysis, lipolysis, and citrate breakdown, hence contributing to their typical taste and flavour. Enterococci are also present in other fermented foods, such as sausages and olives. However, their role in these products has not been fully elucidated. Furthermore, the production of bacteriocins by enterococci is well documented. Moreover, enterococci are nowadays used as probiotics. At the same time, however, enterococci have been associated with a number of human infections. Several virulence factors have been described and the number of vancomycin-resistant enterococci is increasing. The controversial nature of enterococci has prompted an enormous increase in scientific papers and reviews in recent years, where researchers have been divided into two groups, namely pro and contra enterococci. To the authors’ impression, the negative traits have been focused on very extensively. The aim of the present review is to give a balanced overview of both beneficial and virulence features of this divisive group of microorganisms, because it is only acquaintance with both sides that may allow their safe exploitation as starter cultures or co-cultures. D 2005 Elsevier B.V. All rights reserved. Keywords: Enterococcus; Food; Health; Functional properties; Pathogenesis Contents 1. The genus Enterococcus ........................................................ 2 2. Functional properties of enterococci .................................................. 2 2.1. Bacteriocin production by enterococci.............................................. 2 2.2. Citrate metabolism by enterococci................................................ 3 2.3. Proteolysis and lipolysis by enterococci ............................................. 5 2.3.1. Proteolysis ....................................................... 5 2.3.2. Lipolysis ........................................................ 6 2.4. Enterococci as probiotics .................................................... 7 3. Pathogenesis of enterococci....................................................... 8 3.1. Cytolytic activity of enterococci ................................................. 8 3.2. Antibiotic resistance of enterococci ............................................... 9 3.3. Virulence factors of enterococci ................................................. 9 * Corresponding author. Tel.: +32 2 6293245; fax: +32 2 6292720. E-mail address: [email protected] (L. De Vuyst). 1 M.R. Foulquie´ Moreno and P. Sarantinopoulos have equally contributed to this manuscript. 2 Current address: DSM Food Specialties, Research and Development, Process Technology Department, P.O. Box 1, 2600 MA, Delft, The Netherlands. 0168-1605/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.ijfoodmicro.2005.06.026 2 M.R. Foulquie´ Moreno et al. / International Journal of Food Microbiology 106 (2006) 1–24 3.3.1. Aggregation substance................................................. 10 3.3.2. Gelatinase ....................................................... 10 3.3.3. Extracellular surface protein .............................................. 10 3.4. Opsonophagocytic assay to assess the safety of potential enterococcal pathogens ....................... 10 4. Enterococci in food .......................................................... 10 4.1. Cheese products ........................................................ 10 4.1.1. Presence of enterococci in cheese ........................................... 11 4.1.2. Applicability of enterococci as starter or adjunct cultures in cheese ......................... 12 4.1.3. Applicability of bacteriocinogenic enterococci and/or their enterocins in cheese ................... 12 4.2. Meat products ......................................................... 14 4.2.1. Presence of enterococci in meat ............................................ 14 4.2.2. Applicability of bacteriocinogenic enterococci and/or their enterocins in meat products ............... 15 4.3. Vegetables and olives...................................................... 15 5. Conclusions .............................................................. 16 Acknowledgments ............................................................. 16 References ................................................................. 16 1. The genus Enterococcus columbae grow poorly or not at all in the presence of 6.5% NaCl (Devriese et al., 1990, 1993; Vancanneyt et al., 2004). The genus Enterococcus belongs to a group of micro- Most enterococcal species can hydrolyse aesculin in the organisms known as lactic acid bacteria (LAB). Enterococci presence of 40% bile salts. Enterococcal species possess the are Gram-positive, non-sporeforming, catalase-negative, ox- Lancefield group D antigen with the exception of E. idase-negative, facultative anaerobic cocci that occur singly, cecorum, E. columbae, E. dispar, E. pseudoavium, E. in pairs, or in chains. From a taxonomic point of view, the saccharolyticus and E. sulfureus (Hardie and Whiley, genus Enterococcus has been reviewed several times 1997). E. mundtii and E. casseliflavus are yellow-pigmented, (Schleifer and Kilpper-Ba¨lz, 1987; Stackebrandt and Teuber, and E. gallinarum and E. casseliflavus are motile (Schleifer 1988; Devriese and Pot, 1995; Hardie and Whiley, 1997). In and Kilpper-Ba¨lz, 1987). 1984, DNA–DNA hybridisation and 16S rRNA sequencing studies indicated that the species Streptococcus faecium and 2. Functional properties of enterococci S. faecalis were sufficiently distinct from other streptococci, and Schleifer and Kilpper-Ba¨lz (1984) proposed their Studies on the microbiota of traditional cheeses in the transfer to the genus Enterococcus. To date, 28 species, Mediterranean countries, which are mainly produced from namely E. asini, E. avium, E. canis, E. casseliflavus, E. raw ewes’ or goats’ milk, and less commonly from cows’ cecorum, E. columbae, E. dispar, E. durans, E. faecalis, E. milk, have indicated that enterococci play an important role faecium, E. flavescens, E. gallinarum, E. gilvus, E. in the ripening of these cheeses, probably through proteol- haemoperoxidus, E. hirae, E. malodoratus, E. moraviensis, ysis, lipolysis, and citrate breakdown, hence contributing to E. mundtii, E. pallens, E. phoeniculicola, E. pseudoavium, their typical taste and flavour, (Coppola et al., 1990; E. raffinosus, E. ratti, E. saccharolyticus, E. saccharomi- Litopoulou-Tzanetaki and Tzanetakis, 1992; Ledda et al., nimus, E. solitarius, E. sulfureus, and E. villorum, have 1994; Giraffa et al., 1997; Manolopoulou et al., 2003). They been added to the genus on the basis of phylogenetic are also present in other fermented food products, such as evidence strengthened by 16S rRNA DNA sequencing and/ sausages (Franz et al., 1999a, 2003; Giraffa, 2002; Hugas et or DNA–DNA hybridization studies. However, some reclas- al., 2003) and olives (Ferna´ndez-Diaz, 1983; Franz et al., sifications may occur in the near future. For instance, E. 1996, 1999a; Floriano et al., 1998; Ben Omar et al., 2004). flavescens and E. casseliflavus have insufficient differences Enterococci have the ability to produce bacteriocins, the so- to be classified separately (Devriese and Pot, 1995; called enterocins, which are small peptides with antimicro- Descheemaeker et al., 1997), and E. avillorum is an earlier bial activity towards closely related Gram-positive bacteria heterotypic synonym of E. porcinus (De Graef et al., 2003). including spoilage or pathogenic bacteria, such as Listeria Enterococci grow optimally at a temperature of 35 -C, (De Vuyst and Vandamme, 1994). Moreover, enterococci are although most species in the genus will grow at temperatures used in some countries as probiotics (Franz et al., 1999a, ranging from 10 to 45 -C. They can also grow in the 2003). presence of 6.5% NaCl, at pH 9.6, and they survive heating at 60 -C for 30 min. Exceptions include E. dispar and E. 2.1. Bacteriocin production by enterococci sulfureus (Martı´nez-Murcia and Collins, 1991), E. malodor- atus (Collins et al., 1984) and E. moraviensis (Svec et al., The bacteriocins produced by LAB belong to the large 2001), which do not grow at 45 -C, and E. cecorum and E. group of ribosomally synthesised, small, cationic, amphiphilic columbae, which do not grow at 10 -C(Devriese et al., (rather hydrophobic), antimicrobial peptides, naturally pro- 1993). E. avium, E. saccharominimus, E. cecorum and E. duced by microorganisms, which vary in spectrum and mode of M.R. Foulquie´ Moreno et al. / International Journal of Food Microbiology 106 (2006) 1–24 3 activity, molecular
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