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Metabolism of Oligosaccharides and Starch in Lactobacilli: a Review

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Metabolism of Oligosaccharides and Starch in Lactobacilli: a Review REVIEW ARTICLE published: 26 September 2012 doi: 10.3389/fmicb.2012.00340 Metabolism of oligosaccharides and starch in lactobacilli: a review Michael G. Gänzle* and Rainer Follador † Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada Edited by: Oligosaccharides, compounds that are composed of 2–10 monosaccharide residues, are Kostas Koutsoumanis, Aristotle major carbohydrate sources in habitats populated by lactobacilli. Moreover, oligosaccharide University, Greece metabolism is essential for ecological fitness of lactobacilli. Disaccharide metabolism by Reviewed by: Eva Van Derlinden, Katholieke lactobacilli is well understood; however, few data on the metabolism of higher oligosac- Universiteit Leuven, Belgium charides are available. Research on the ecology of intestinal microbiota as well as the com- Alexandra Lianou, Aristotle University mercial application of prebiotics has shifted the interest from (digestible) disaccharides to of Thessaloniki, Greece (indigestible) higher oligosaccharides.This review provides an overview on oligosaccharide *Correspondence: metabolism in lactobacilli. Emphasis is placed on maltodextrins, isomalto-oligosaccharides, Michael G. Gänzle, Department of Agricultural, Food and Nutritional fructo-oligosaccharides, galacto-oligosaccharides, and raffinose-family oligosaccharides. Science, University of Alberta, 4-10 Starch is also considered. Metabolism is discussed on the basis of metabolic studies Ag/For Centre, Edmonton, AB, related to oligosaccharide metabolism, information on the cellular location and substrate Canada T6G 2P5. specificity of carbohydrate transport systems, glycosyl hydrolases and phosphorylases, e-mail: [email protected] and the presence of metabolic genes in genomes of 38 strains of lactobacilli. Metabolic †Present address: Rainer Follador, Microsynth AG, pathways for disaccharide metabolism often also enable the metabolism of tri- and tetrasac- Balgach, Switzerland. charides. However, with the exception of amylase and levansucrase, metabolic enzymes for oligosaccharide conversion are intracellular and oligosaccharide metabolism is limited by transport. This general restriction to intracellular glycosyl hydrolases differentiates lac- tobacilli from other bacteria that adapted to intestinal habitats, particularly Bifidobacterium spp. Keywords: Lactobacillus, metabolism, isomalto-oligosaccharides, starch, fructo-oligosaccharides, galacto-oligosaccharides, raffinose-family oligosaccharides, prebiotic INTRODUCTION use of the term “oligosaccharides” in the current scientific lit- Lactobacilli have complex nutritional requirements for fer- erature, however, differs from this definition in a number of mentable carbohydrates, amino acids, nucleic acids and other cases. For example, the term “fructo-oligosaccharides” is gen- substrates, and derive metabolic energy from homofermentative erally used to include b-(1 ! 2) linked fructo-oligosaccharides, or heterofermentative carbohydrate fermentation (Hammes and excluding the digestible disaccharide sucrose; the term “galacto- Hertel, 2006). Habitats of lactobacilli are nutrient-rich and often oligosaccharides” generally includes the (indigestible) b-(1 ! 3 or acidic and include plants, milk and meat, and mucosal surfaces 6) linked disaccharides and a-galactosyllactose but excludes the of humans and animals (Hammes and Hertel, 2006). Intestinal disaccharide lactose, which is also indigestible in a majority of microbiota are characterized by a high proportion of lactobacilli humans, and melibiose; the term“isomalto-oligosaccharides”gen- particularly in animals harboring non-secretory epithelia in the erally includes the digestible disaccharide isomaltose (Roberfroid upper intestinal tract, including the crop of poultry, the pars et al., 1998; MacFarlane et al., 2008; Seibel and Buchholz, 2010). esophagus of swine, and the forestomach or rodents and mem- This paper will use the IUPAC definition of oligosaccharides to bers of the Equidae family (Walter, 2008). Lactobacilli are also include the corresponding disaccharides. dominant in fermentation microbiota of a majority of food fer- Oligosaccharide metabolism is essential for ecological fitness mentations, and are applied as probiotic cultures to benefit host of lactobacilli in most of their food-related and intestinal habi- health (Hammes and Hertel, 2006). Owing to their association tats (de Vos and Vaughan, 1994; Bron et al., 2004; Gänzle et al., with humans, food animals, and food as well as their economic 2007; Walter, 2008; Tannock et al., 2012). Oligosaccharides are the importance, they have been studied for more than a century and major carbohydrate sources in cereals, milk, fruits, and the upper the physiology and genetics of their monosaccharide metabolism intestine of animals. The metabolism of mono- and disaccharides is well understood (Orla-Jensen, 1919; Kandler, 1983; de Vos and is well understood; however, few data are available on the metab- Vaughan, 1994; Axelsson, 2004; Makarova et al., 2006; Gänzle et al., olism of higher oligosaccharides which are equally abundant in 2007). many habitats. Moreover, interest in the intestinal microbial ecol- Oligosaccharides are defined as compounds that are composed ogy as well as the widespread commercial application of prebiotic of few (2–10) monosaccharide residues (Anonymous, 1982). The oligosaccharide preparations has shifted the research interest from www.frontiersin.org September 2012 | Volume 3 | Article 340 | 1 Gänzle and Follador Oligosaccharide metabolism in lactobacilli (digestible) disaccharides to (indigestible) higher oligosaccharides milk, meat, cereal fermentations, vegetable fermentations, and (Barrangou et al., 2003; Kaplan and Hutkins, 2003; Walter, 2008; intestinal habitats. Data were obtained from NCBI GenBank Seibel and Buchholz, 2010). However, the sound description of the (ftp://ftp.ncbi.nih.gov/genomes/Bacteria/) on 9 September 2011 metabolism of higher oligosaccharides is challenging. First, the (Table 1). For each species and its associated plasmids, coding in silico assignment of the specificity of carbohydrate transport sequences were extracted, translated, and a BLAST database was systems or glycosyl hydrolases is unreliable (see e.g., Thompson built using “makeblastdb” of the NCBI Standalone BLASTC soft- et al., 2008; Francl et al., 2010) and often results in question- ware package (version 2.2.25; Camacho et al., 2009). The query able assignments of gene function. Second, few of the relevant sequences were searched in each database using “blastp” of the higher oligosaccharides are available in purified form for use as BLASTC software package with the standard settings and the best substrate. However, the determination of the growth of lactobacilli match was reported. Additionally, a Smith–Waterman alignment on poorly described substrates provided little relevant information of the query sequence with the highest match was performed using on the capacity of lactobacilli to utilize oligosaccharides as carbon a BLOSUM62 substitution matrix. The score of this alignment was source. The lack of reference compounds also impedes identifica- divided by the score of the alignment of the query sequence to itself tion and quantification of individual compounds in a mixture of resulting in a score ratio. An enzyme was marked as present in a oligosaccharides with chromatographic methods. Only few studies given genome or plasmid if the score ratio is above a threshold of characterized oligosaccharide preparations with regards to com- 0.3–0.4. position,linkage type,and degree of polymerization,or monitored The bioinformatic analysis of genes contributing to oligosac- the metabolism of individual compounds during growth of lac- charide metabolism allows an assessment of the frequency of alter- tobacilli (Gopal et al., 2001; Kaplan and Hutkins, 2003; Saulnier native pathways for oligosaccharide metabolism, identifies genes et al., 2007; Ketabi et al., 2011; Teixeira et al., 2012). Despite the that occur together to form a functional metabolic pathway, and importance of oligosaccharide metabolism for the performance delineates major and convergent or divergent metabolic strategies of lactobacilli in food fermentations and in intestinal habitats, of lactobacilli for niche adaptation by specialized oligosaccha- our understanding of oligosaccharide metabolism in lactobacilli ride metabolism. However, it does not account for silent genes remains thus limited. Particularly the delineation of metabolism or orphan genes that are not expressed or not functional (Obst of disaccharides and higher oligosaccharides is unclear, and a et al., 1992). Moreover, carbohydrate fermentation is highly vari- comprehensive description of metabolic pathways is currently not able within strains of the same species due to the loss of plasmid available. encoded traits (de Vos and Vaughan, 1994) and gene acquisition This review aims to provide an overview on oligosaccharide by lateral gene transfer (Barrangou et al., 2003). For example, gene metabolism by lactobacilli. Hydrolysis of starch, the only poly- cassettes coding for carbohydrate utilization in L. plantarum are saccharide hydrolyzed by extracellular enzymes of lactobacilli, is highly variable and were designated as “lifestyle cassettes” that also discussed. Oligosaccharide fermentation is discussed on the may be added or deleted according to the requirements of specific basis of metabolic studies, the cellular location, and substrate ecological niches
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