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1 Centre for Molecular and Biomolecular Informatics, Radboud University Nijmegen, 6525ED, Nijmegen, The Netherlands
2 Wageningen Centre for Food Sciences, Wageningen, The Netherlands
3 NIZO food research, Ede, The Netherlands
Correspondence
Jos Boekhorst
J.Boekhorst{at}cmbi.ru.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Supplementary tables and figures are available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Servin, 2004). A protective layer of mucus, consisting of a complex mixture of large, highly glycosylated proteins (mucins) (Dekker et al., 2002) and glycolipids, covers the epithelial cells of the intestine and offers an attachment site for the bacteria colonizing the intestine. These bacteria play an important role in maintaining normal gut functionality and in the resistance of the host against pathogenic micro-organisms (Hooper & Gordon, 2001), and some may use mucins as their major carbon and energy source (Aryanta et al., 1991; Bayliss & Houston, 1984; Sonnenburg et al., 2005). Certain strains of LAB may promote health in man and animals (Reid et al., 2003), and many have been shown to adhere to intestinal mucus (Servin, 2004). In most cases, this adhesion has been shown to be mediated by proteins (Coconnier et al., 1992; Conway & Kjelleberg, 1989; Roos & Jonsson, 2002).
An extracellular mucus-binding protein of Lactobacillus reuteri 1063 was identified by Roos & Jonsson (2002). This protein contains two different types of repeats of approximately 200 aa, present in eight and six copies, shown to be responsible for the adherence to intestinal mucus. More recently, Pretzer et al. (2005) have identified a protein of Lactobacillus plantarum WCFS1 that contains a domain similar to the mucus-binding (MUB) domains identified by Roos & Jonsson (2002) and is involved in the adherence to mannose, which is a constituent of mucin glycosylation moieties. This domain is partly similar to the MucBP domain from the Pfam database (Bateman et al., 2004), but is significantly different in size, sequence and phylogenetic distribution.
The mucus-binding proteins of both Lb. plantarum and Lb. reuteri have characteristics typical of cell-surface proteins of Gram-positive bacteria: an N-terminal signal peptide targeting the protein for secretion and a C-terminal sortase recognition site targeting the protein for covalent attachment to the peptidoglycan layer at the outside of the bacterial cell (Ton-That et al., 2004).
The modification and recombination of existing functional modules plays an important role in evolution of protein function (Doolittle & Bork, 1993). Extracellular proteins are often large proteins consisting of many of these modules or domains (Bork, 1991). The identification and characterization of these domains can play an important role in elucidating the function of extracellular proteins. We have searched bacterial genome sequences and the UniProt protein database for potential mucus-binding proteins based on the sequence of the MUB domains of Lb. reuteri and Lb. plantarum. We discuss the properties and variability of the MUB domain and the putative role of the domain as a functional unit.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) and the ERGO database (Overbeek et al., 2003). From the ERGO database we used genome information for Enterococcus faecium DO, Lactobacillus brevis ATCC 367, Lactobacillus casei ATCC 33323, Lactobacillus delbrueckii subsp. bulgaricus ATCCBAA-356, Lactococcus lactis subsp. cremoris SK11, Leuconostoc mesenteroides ATCC 8293, Oenococcus oeni PSU-1 and Pediococcus pentosaceus ATCC 25745. A list of the species present in the NCBI bacterial genome database at the time of this analysis can be found in supplementary Table A (available with the online version of this paper).
Sequence analysis.
Sequence similarity was detected with BLAST (Altschul et al., 1990) while multiple sequence alignments were made with Muscle (Edgar, 2004). The HMMER package (Durbin et al., 1998) was used to construct Hidden Markov models (HMMs) of MUB domains and to scan protein sequences with HMMs. HMMs from the Pfam (Bateman et al., 2004), SMART (Letunic et al., 2004) and Superfam (Gough et al., 2001) databases were used to identify other known domains in proteins with identified MUB domains. HMMs were compared with HHsearch (Soding, 2005).
Sortase recognition sites with LPxTG-type motifs were predicted with a recently developed HMM (Boekhorst et al., 2005). Conserved sequence patterns were identified with MEME and MAST (Bailey & Elkan, 1994). Proline-rich amino acid stretches were identified using simple Python scripts. Protein secondary structure predictions were done with PsiPred (McGuffin et al., 2000). The EMBOSS package (Rice et al., 2000) was used to scan for repetitive DNA sequences. DNA secondary structure predictions were done with MFOLD (Santa Lucia, 1998).
Identifying putative mucus-binding proteins.
An initial set of potential mucus-binding proteins was identified by searching amino acid sequences obtained from the sources mentioned above with an HMM based on the MUB domains of protein Mub of Lb. reuteri (Roos & Jonsson, 2002) and an HMM based on the domains of protein lp_1229 of Lb. plantarum WCFS1 (Kleerebezem et al., 2003; Pretzer et al., 2005). Hits with an e-score of 1e-10 or lower were considered putative MUB-domain proteins. The amino acid sequences of these proteins were scanned for conserved protein motifs with MEME. The exact position of the MUB domains in the identified proteins was determined based on the results of the MEME and HMM analyses, and on multiple sequence alignments of highly similar MUB-domain-containing proteins. Multiple sequence alignments of the individual MUB domains were used to create new HMMs, which were subsequently used to search for additional MUB-domain proteins. This iterative process was repeated until no additional MUB-domain proteins were detected in the bacterial genomes or the UniProt database.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Pretzer et al., 2005; Roos & Jonsson, 2002). This difference in size implies a discrepancy in the definition of the domain boundaries in the Lb. plantarum or Lb. reuteri mucus-binding proteins. To create domains of a uniform size would require either merging of every second repeat of the Lb. plantarum mucus-binding protein with its neighbour or splitting the Lb. reuteri domain in two. However, our sequence analysis suggests that the mucus-binding building blocks of the mucus-binding proteins do in fact vary in size. A multiple sequence alignment of the MUB domains of Lb. reuteri shows that they are 90 % identical in sequence, while the first 100 residues of each domain share less than 15 % sequence identity with the second half of the domain (data not shown). This suggests that the copies of the Lb. reuteri domain have evolved from one large MUB domain, in turn suggesting that the large domain functions as a biological unit. A possible explanation for this difference in size will be discussed below.
This variability in size makes it difficult to determine the boundaries of MUB domains, a problem often encountered in defining protein domains (Ekman et al., 2005). HMM searches with models based on the MUB domains of different proteins suggest contradicting boundaries (see below). This problem is further complicated by the presence of what seem to be partial MUB domains flanking complete MUB domains in the same protein. Ultimately, we were able to define the boundaries of the MUB domain by comparing different sets of sequences of highly similar proteins that differed in their number of MUB domains: (i) protein L39650 from Lc. lactis IL1403 and its orthologue RLCR01214 from Lc. lactis SK11, (ii) two highly similar proteins RLBR01191 and RLBR01264 from Lb. brevis, and (iii) orthologues of lp_1229 from different Lb. plantarum strains (G. Pretzer and others, unpublished data).
Next, we searched the protein databases for MUB domains using domain boundaries derived from multiple sequence alignments of orthologous and paralogous proteins as described above. We identified a total of 48 proteins containing at least one MUB domain in nine different species. Most were lactobacilli that are known inhabitants of the gastrointestinal tract, while others were species commonly used in food fermentations (Altermann et al., 2005; Aryanta et al., 1991; Bolotin et al., 2001; Kleerebezem et al., 2003; Pridmore et al., 2004; Zoetendal et al., 2002). A schematic overview of the 30 proteins with three or more MUB domains is given in Fig. 1. Table 1 lists the species in which proteins containing one or more MUB domains were identified, while a complete list of putative mucus-binding proteins and their predicted features is given in supplementary Table B (available with the online version of this paper). A multiple sequence alignment of selected MUB domains and a predicted secondary structure of the domain can be found in the supplementary Figs A and B (available with the online version of this paper). An HMM based on the complete set of MUB domains identified is given in supplementary File 1 (available with the online version of this paper).
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), encode a smaller number of these proteins. Compared to lactobacilli of the gastrointestinal tract, ‘domesticated’ Lc. lactis strains live in a more restricted habitat (Bolotin et al., 2001), which could explain the presence of only a single MUB-domain-containing protein in this bacterium.
Comparison of MUB and Pfam-MucBP domains
The model MucBP from the Pfam database is similar to part of the MUB domain described in this study. The Pfam model describes a sequence of approximately 50 aa, while we predict the MUB domain to be approximately 200 residues in length.
The MucBP model tends to either leave large gaps between the different copies of the MUB domain in many proteins or predict the presence of multiple instances of the domain in situations where only a single domain is present. Also, the phylogenetic distribution of the Pfam-MucBP domain is much broader than that of the domain described in this study; it is found in many proteins of Listeria monocytogenes and even in a single protein supposedly from Homo sapiens, although the presence in this protein of both a Gram-positive signal peptide and an LPxTG-type sortase anchor suggest that this protein is in fact of bacterial origin. In our opinion, the relatively weak similarity between these domains and the Lb. plantarum MUB domain that has been experimentally shown to have mannose-binding properties or the MUB domains of the protein Mub from Lb. reuteri does not warrant the inclusion of these Listeria proteins in the set of putative MUB proteins discussed here. Many proteins with significant hits to the Pfam-MucBP domain, but with no significant hits to the MUB domain of LAB, contain multiple copies of the leucine-rich repeat domain (a domain thought to be involved in protein–protein interactions; Kobe & Kajava, 2001). This observation does not hold true for the putative MUB proteins we have identified, indicating that they might have different roles.
The difference in size between MUB and MucBP can in part be explained by the distinct N-terminal region of the MUB domain that we have identified; this part is present in 43 of the 48 proteins containing the MUB domain. Fig. 2 shows a multiple alignment of the N terminus of a subset of domains. This part of the domain does not merely act as a spacer or a flexible region since it has numerous conserved residues and is predicted to contain distinct secondary structure elements. As shown in the alignment, in some cases the N-terminal part of the MUB domain is separated from the rest of the domain by a PxxP region (discussed in more detail below). The N-terminal part of the MUB domain is never found without the C-terminal part, showing that it is in fact part of the MUB domain and not functioning as a separate domain.
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; Marcotte et al., 1999). Gene clusters encoding MUB proteins were found to be only conserved over relatively short evolutionary distances: conserved clusters were only detected in Lactobacillus johnsonii, Lactobacillus gasseri and Lactobacillus acidophilus, three species which are closely related (Altermann et al., 2005; Pridmore et al., 2004). This lack of conservation over larger phylogenetic distances is in good agreement with the observation that even bacteria of the same genus, such as Lb. plantarum and Lb. johnsonii, have their own set of extracellular proteins (Boekhorst et al., 2004). Although the exact context of genes encoding MUB-domain proteins is not conserved, these proteins are often encoded in gene clusters together with other putative extracellular proteins (based on the presence of a signal peptide), suggesting that these extracellular proteins have a functional relation. In several cases multiple proteins containing the MUB domain are encoded in a single gene cluster; Fig. 3 shows an example of a cluster of MUB-containing proteins in Lb. acidophilus and a different conserved cluster found in both Lb. gasseri and Lb. johnsonii.
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show that the different MUB domain types can have different adhesion targets, suggesting a broadening of the range of mucus components such a protein can adhere to. In situations where all the copies of the MUB domains in a protein are highly similar, the role of a larger number of domains could be an increased affinity to mucins.
The high variability in the number of MUB domains in related proteins, even in orthologous proteins from closely related species, exemplifies the relative ease with which the domain is duplicated or deleted in evolution. As an example, Fig. 4 displays two orthologous proteins from Lb. plantarum and Lb. brevis, which have 6 and 3 homologous MUB domains, respectively. A possible evolutionary scenario that would explain the tree is an ancestral protein containing three copies of the MUB domain followed by a single duplication of the first MUB domain and two successive duplications of the second MUB domain in the Lb. plantarum version of the ancestral protein. The relatively frequent deletion and duplication of the MUB domain might be explained by repetitive DNA sequence in the boundaries of the domain. However, analysis of the boundaries of the domain did not yield any repetitive structures such as inverted repeats or tandem repeats.
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). A signal peptide is an N-terminal signal sequence that targets a protein to the bacterial cell wall (von Heijne, 1989). For 5 of the residual 11 proteins, originally predicted not to contain a signal peptide, we were able to identify a signal peptide by selecting an alternative translation start site or by the introduction of a single frameshift (see supplementary Table B, available with the online version of this paper). Frameshifts could either be a sequencing artefact or a true frameshift; the latter suggests the gene containing the frameshift does not encode a functional protein. In addition to a signal peptide, most of the proteins with multiple MUB domains contain a C-terminal anchoring motif, called LPxTG, that is recognized by a family of enzymes called sortases for covalent attachment to the peptidoglycan of the bacterial cell wall (Navarre & Schneewind, 1999). The presence or absence of signal peptides and LPxTG-like motifs is summarized in supplementary Table A (available with the online version of this paper). The MUB-domain-containing proteins without an LPxTG anchor or a signal peptide are often encoded next to proteins containing the MUB domain, a signal peptide and an LPxTG-like motif. They could either be non-functional remnants of extracellular proteins or function at the bacterial cell wall through some other mechanism, e.g. interaction with extracellular proteins that do contain a membrane anchor.
PxxP regions
Many MUB proteins contain proline-rich amino acid stretches, designated PxxP regions. In these regions, proline residues are separated by two (in rare cases 1 or 3) non-proline residues. Sequences of at least 13 residues in length containing at least five P residues were considered PxxP regions. About half of the putative mucus-binding proteins we identified contained at least one PxxP region, always inserted in or flanking an MUB domain. In some of the cases where such a region is found inside an MUB domain, only a subset of the MUB domains of a specific protein contain a PxxP region. Combined with the observation that the MUB domains of such a protein are often more similar to each other than to any other MUB domain, this suggests that the insertion or deletion of PxxP regions are quite common events.
It has been suggested that proline residues allow a polypeptide chain to make sharp bends or twists (Fischetti, 2000). In this scenario, the function of the PxxP regions could be to generate flexibility of the protein chain. The presence of a PxxP region between the C-terminal membrane anchor and the last MUB domain of many of the MUB proteins supports this putative function of the PxxP regions (Fig. 1).
In eukaryotes, proline-rich motifs are known to be involved in binding to so-called SH3 domains (described by Pfam entries SH3_1 and SH3_2). In these interactions, the proline-rich sequence forms a polyproline type II helical conformation that fits into the hydrophobic groove of the SH3 domain (Agrawal & Kishan, 2002). The proline-rich motifs bound by the SH3 domain are approximately 13 residues long; the difference in size compared to the PxxP regions found in the MUB proteins, which in some cases reach lengths of over 50 residues, suggests that the bacterial regions could form similar secondary structure elements, but might have a different function.
Identification of other domains of MUB proteins
To gain further insight into the presence and putative function of other domains of mucus-binding proteins, generally preceding the MUB domains, all proteins containing one or more MUB domain were scanned with HMMs from the Pfam, Superfam and SMART databases. In many cases we identified sequences in the N-terminal region of these proteins which are similar to either binding domains or enzymic domains found in other extracellular proteins, such as glucanase and pectin lyase-like domains (supplementary Table B, available with the online version of this paper). However, in most cases these regions scored just below the threshold suggested for the various HMMs, indicating that these potential domains have similar, but not identical, enzymic functions. The similarity to glucanase and pectin lyase-like domains suggests that these putative domains may be involved in degradation of complex polysaccharides or mucus-associated glycosylation moieties.
In addition to domains with similarity to domains with a known function or structure, we identified a previously undescribed domain of approximately 70 aa in size. This domain, which we call MUB-associated domain (Mubad), is present in six of the proteins containing the MUB domain and the number of Mubad domains per protein varies between 1 and 18 (Fig. 1). A multiple sequence alignment of Mubad domains (supplementary Fig. C, available with the online version of this paper) shows that this domain is not highly conserved. However, the presence of Mubad domains only in proteins that contain MUB domains suggests that the association is significant. Comparison of an HMM based on a multiple alignment of the Mubad domain to models from the Pfam and Superfam databases did not detect any known domains homologous to the Mubad domain. Although the function of this Mubad domain remains unclear, it again illustrates the complex domain architecture of the putative mucus-binding proteins.
Concluding remarks
The MUB domain is very variable in size and sequence, making it difficult to determine precise domain boundaries. The use of orthologous proteins with different numbers of MUB domains allowed us to identify putative functional units. The high variability in the number of MUB domains in putative mucus-binding proteins suggests that the MUB domain is often duplicated or deleted in evolution. In contrast to the MucBP domain from the Pfam database, the MUB domain appears to be only present in LAB, with the highest abundance in lactobacilli of the gastrointestinal tract, strongly suggesting that the MUB domain is a functional unit specific to LAB that could fulfil an important function in host–microbe interactions.
The genomes sequenced from intestinal bacteria are presently biased towards LAB, due to the relevance of LAB to food and health. In the future, the ever-increasing number of available genome sequences might lead to the identification of MUB-domain-containing proteins in other species and other types of mucus-binding domains.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
|---|
Altermann, E., Russell, W. M., Azcarate-Peril, M. A. & 11 other authors (2005). Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci U S A 102, 3906–3912.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef][Medline]
Aryanta, R. W., Fleet, G. H. & Buckle, K. A. (1991). The occurrence and growth of microorganisms during the fermentation of fish sausage. Int J Food Microbiol 13, 143–155.[CrossRef][Medline]
Bailey, T. L. & Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2, 28–36.[Medline]
Bairoch, A., Apweiler, R., Wu, C. H. & 12 other authors (2005). The Universal Protein Resource (UniProt). Nucleic Acids Res 33, D154–D159.
Bateman, A., Coin, L., Durbin, R. & 10 other authors (2004). The Pfam protein families database. Nucleic Acids Res 32, D138–D141.
Bayliss, C. E. & Houston, A. P. (1984). Characterization of plant polysaccharide- and mucin-fermenting anaerobic bacteria from human feces. Appl Environ Microbiol 48, 626–632.
Boekhorst, J., Siezen, R. J., Zwahlen, M. C. & 7 other authors (2004). The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. Microbiology 150, 3601–3611.
Boekhorst, J., de Been, M. W., Kleerebezem, M. & Siezen, R. J. (2005). Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs. J Bacteriol 187, 4928–4934.
Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., Ehrlich, S. D. & Sorokin, A. (2001). The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11, 731–753.
Bork, P. (1991). Shuffled domains in extracellular proteins. FEBS Lett 286, 47–54.[CrossRef][Medline]
Coconnier, M. H., Klaenhammer, T. R., Kerneis, S., Bernet, M. F. & Servin, A. L. (1992). Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture. Appl Environ Microbiol 58, 2034–2039.
Conway, P. L. & Kjelleberg, S. (1989). Protein-mediated adhesion of Lactobacillus fermentum strain 737 to mouse stomach squamous epithelium. J Gen Microbiol 135, 1175–1186.[Medline]
Dandekar, T., Snel, B., Huynen, M. & Bork, P. (1998). Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23, 324–328.[CrossRef][Medline]
Dekker, J., Rossen, J. W., Buller, H. A. & Einerhand, A. W. (2002). The MUC family: an obituary. Trends Biochem Sci 27, 126–131.[CrossRef][Medline]
Doolittle, R. F. & Bork, P. (1993). Evolutionarily mobile modules in proteins. Sci Am 269, 50–56.
Durbin, R., Eddy, S., Krogh, A. & Mitchison, G. (1998). Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids. Cambridge: Cambridge University Press.
Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E. & Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science 308, 1635–1638.
Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.[CrossRef][Medline]
Ekman, D., Bjorklund, A. K., Frey-Skott, J. & Elofsson, A. (2005). Multi-domain proteins in the three kingdoms of life: orphan domains and other unassigned regions. J Mol Biol 348, 231–243.[CrossRef][Medline]
Fischetti, V. A. (2000). In Gram-Positive Pathogens, pp. 11–24. Washington, DC: American Society for Microbiology.
Gough, J., Karplus, K., Hughey, R. & Chothia, C. (2001). Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313, 903–919.[CrossRef][Medline]
Hooper, L. V. & Gordon, J. I. (2001). Commensal host–bacterial relationships in the gut. Science 292, 1115–1118.
Kleerebezem, M., Boekhorst, J., van Kranenburg, R. & 17 other authors (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100, 1990–1995.
Kobe, B. & Kajava, A. V. (2001). The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11, 725–732.[CrossRef][Medline]
Letunic, I., Copley, R. R., Schmidt, S., Ciccarelli, F. D., Doerks, T., Schultz, J., Ponting, C. P. & Bork, P. (2004). SMART 4.0: towards genomic data integration. Nucleic Acids Res 32, D142–D144.
Marcotte, E. M., Pellegrini, M., Ng, H. L., Rice, D. W., Yeates, T. O. & Eisenberg, D. (1999). Detecting protein function and protein–protein interactions from genome sequences. Science 285, 751–753.
McGuffin, L. J., Bryson, K. & Jones, D. T. (2000). The PSIPRED protein structure prediction server. Bioinformatics 16, 404–405.
Navarre, W. W. & Schneewind, O. (1999). Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63, 174–229.
Overbeek, R., Larsen, N., Walunas, T. & 19 other authors (2003). The ERGO genome analysis and discovery system. Nucleic Acids Res 31, 164–171.
Pretzer, G., Snel, J., Molenaar, D. & 7 other authors (2005). Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J Bacteriol 187, 6128–6136.
Pridmore, D., Berger, B., Desiere, F. & 12 other authors (2004). The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci U S A 101, 2512–2517.
Reid, G., Sanders, M. E., Gaskins, H. R. & 7 other authors (2003). New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol 37, 105–118.[CrossRef][Medline]
Rice, P., Longden, I. & Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16, 276–277.[CrossRef][Medline]
Roos, S. & Jonsson, H. (2002). A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148, 433–442.
SantaLucia, J., Jr (1998). A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc Natl Acad Sci U S A 95, 1460–1465.
Servin, A. L. (2004). Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28, 405–440.[Medline]
Soding, J. (2005). Protein homology detection by HMM–HMM comparison. Bioinformatics 21, 951–960.
Sonnenburg, J. L., Xu, J., Leip, D. D., Chen, C. H., Westover, B. P., Weatherford, J., Buhler, J. D. & Gordon, J. I. (2005). Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.
Ton-That, H., Marraffini, L. A. & Schneewind, O. (2004). Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694, 269–278.[Medline]
von Heijne, G. (1989). The structure of signal peptides from bacterial lipoproteins. Protein Eng 2, 531–534.
Zoetendal, E. G., von Wright, A., Vilpponen-Salmela, T., Ben-Amor, K., Akkermans, A. D. & de Vos, W. M. (2002). Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68, 3401–3407.
Received 8 August 2005;
revised 21 October 2005;
accepted 21 October 2005.
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-helix. The dashed vertical line indicates the end of the N-terminal part of the domain. The alignment was visualized with CLUSTALX using the default colouring scheme (Thompson et al., 1997
