Wageningen Academic

Beneficial Microbes, 2010; 1(1): 61-66 P u b l i s h e r s

Biodiversity of mannose-specific adhesion in Lactobacillus plantarum revisited:

strain-specific domain composition of the mannose-adhesin

G. Gross1,2, J. Snel1, J. Boekhorst3, M.A. Smits2 and M. Kleerebezem1,4

1 NIZO Food Research, Health and Safety, P.O. Box 20, 6710 BA Ede, the Netherlands; 2Animal Breeding and Genomics
Centre, Animal Sciences Group of Wageningen UR, P.O. Box 65, 8200 AB Lelystad, the Netherlands; 3Center for Molecular
and Biomolecular Informatics, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, the
Netherlands; 4Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, the Netherlands;
michiel.kleerebezem@nizo.nl

Received: 27 November 2008 / Accepted: 24 February 2009

© 2009 Wageningen Academic Publishers

Abstract

Recently, we have identified the mannose-specific adhesin encoding gene (msa) of Lactobacillus plantarum. In the
current study, structure and function of this potentially probiotic effector gene were further investigated, exploring
genetic diversity of msa in L. plantarum in relation to mannose adhesion capacity. The results demonstrate that
there is considerable variation in quantitative in vitro mannose adhesion capacity, which is paralleled by msa gene
sequence variation. The msa genes of different L. plantarum strains encode proteins with variable domain composition.
Construction of L. plantarum 299v mutant strains revealed that the msa gene product is the key-protein for mannose
adhesion, also in a strain with high mannose adhering capacity. However, no straightforward correlation between
adhesion capacity and domain composition of Msa in L. plantarum could be identified. Nevertheless, differences in
Msa sequences in combination with variable genetic background of specific bacterial strains appears to determine
mannose adhesion capacity and potentially affects probiotic properties. These findings exemplify the strain-specificity
of probiotic characteristics and illustrate the need for careful and molecular selection of new candidate probiotics.

Keywords: Lactobacillus plantarum, mannose-specific adhesin (Msa), domain composition

1. Introduction et al., 1988). Additionally, also Lactobacillus plantarum,

The human intestinal tract is inhabited by a complex
community of bacterial species. Association of the
endogenous microbiota with the epithelial surface
or the mucus layer is essential for persistence in the
intestine. Likewise, attachment of pathogens to epithelial
glycoconjugates can be crucial for the development of
intestinal infections (Karlsson, 2001; Savage, 2006). One
mechanism of bacterial adhesion is based on the binding
to mannose-containing receptor sites on epithelial cells.
Several pathogenic species are known to specifically
adhere to mannose, including enterotoxigenic Escherichia
coli, Salmonella enteritidis, and Pseudomonas aeruginosa
(Aslanzadeh and Paulissen, 1992; Imberty et al., 2004; Wold
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ISSN 1876-2833 print, ISSN 1876-2891 online, DOI 10.3920/BM2008.1006
a member of the endogenous microbiota with probiotic
features, has been shown to bind to mannose-residues
(Adlerberth et al., 1996; Ahrné et al., 1998; Pretzer et al.,
2005). The capacity to recognise the same receptor sites
has been proposed to enable probiotic microorganisms to
inhibit colonisation of pathogens by competitive exclusion,
which might prevent infections in the small intestine (Reid
and Burton, 2002). L. plantarum strain 299v is currently
applied in probiotic food products with proposed consumer
health claims (De Vries et al., 2006; Molin, 2001; Reid, 1999).
Recently, the potentially ‘probiotic gene’ encoding the
mannose-specific adhesin (Msa) of L. plantarum has been
identified, using a biodiversity-based approach including
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G. Gross et al.
phenotype-genotype correlation and mutation analysis
in L. plantarum strain WCFS1 (Pretzer et al., 2005).
Yet, this study did not investigate mannose-adhesion
capacity in different strains of the species L. plantarum
in a quantitative manner. Variations in quantitative levels
of mannose-adhesion capacity in different strains of L.
plantarum could suggest that additional factors besides
Msa contribute to mannose-adhesion. Alternatively, such
variations might be explained by genetic diversity of msa
among L. plantarum strains, leading to different msa
expression levels or distinct Msa protein sequences or
domain compositions in individual strains of the species
with consequently varying mannose-adhesion capacity.
These issues were addressed in the present study.
2. Materials and methods
In vitro determination of mannose-adhesion
Mannose-adherence capacity of several L. plantarum
strains was assessed semi-quantitatively using a yeast
agglutination assay as described previously (Pretzer et
al., 2005). The L. plantarum strains used in this study are
depicted in Figure 1 and encompassed the same selection
of strains as was used previously for identification of msa
(Pretzer et al., 2005). Using L. plantarum cultures that
had been grown overnight in Man-Rogosa-Sharp (MRS)
medium (Merck, Amsterdam, the Netherlands) at 37 °C
without aeration, a range of twofold dilutions of each strain
was tested. The agglutination titre was determined as the
(log2) reciprocal of the highest dilution that still resulted
in visible agglutination of yeast cells. Mean agglutination
titres and corresponding standard deviations (log2±SD)
were calculated from three independent assays.
DNA manipulations in L. plantarum 299v
To evaluate whether other genes contribute to mannose-
adhesion capacity in strains with a higher agglutination titre
as compared to strain WCFS1, gene-specific mutations of
srtA (sortase) and msa were introduced in the exemplary
strain L. plantarum 299v. Molecular biology techniques
were performed essentially according to standard protocols
(Sambrook et al., 1989), with plasmid constructions in
E. coli DH5α as intermediate cloning host (Hanahan,
1983) and plasmid transformation to L. plantarum 299v
by electroporation (Josson et al., 1989). Primers were
purchased from Proligo France SAS (Paris, France).
Since Msa belongs to the sortase-dependent proteins in L.
plantarum WCFS1, correct anchoring of Msa to the cell
wall does not occur in a srtA-deficient derivative of strain
WCFS1, and consequently, this srtA mutant strain was
shown to lack yeast agglutination capacity (Kleerebezem
et al., 2003; Pretzer et al., 2005). To confirm this finding
in strain 299v, a sortase-deficient mutant was constructed
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62
in this strain using the same cat-replacement mutagenesis
vector previously used in strain WCFS1, pNZ7104
(mutagenesis vector containing flanking regions of L.
plantarum WCFS1 srtA (Pretzer et al., 2005)). The resulting
srtA-deletion derivative of strain 299v was designated
NZ7518.
In order to examine more specifically whether also in
strain 299v msa is the sole gene responsible for mannose-
adhesion capacity, the msa gene of this strain was disrupted
by gene replacement with the chloramphenicol resistance
cassette (P32cat) of mutagenesis vector pNZ5319 (vector
for gene replacements in Gram-positive bacteria (Lambert
et al., 2007)). To this end, the msa gene of L. plantarum
299v was amplified with an Elongase Amplification
System (Invitrogen, Breda, the Netherlands) using L.
plantarum 299v chromosomal DNA as a template
and the locus-specific primer combination lp_1229F
(5’-AAGGACAGAAGCGGCCGCCGTGCGAAAGGAT
AGATT-3’) and lp_1229R (5’-ACGGGCCTCGAGGCCCTA
CTCTTTGTGCT-3’) that were based on the sequence of
msa in the sequenced strain WCFS1 (Kleerebezem et al.,
2003). The resulting 3.5 kb PCR-product was subjected
to sequence analysis (BaseClear, Leiden, the Netherlands;
GenBank accession no. EU011788). The msa gene of strain
299v was used as a template for the amplification of selected
parts of the 5’- and 3’-regions of this gene (each approximately
800 bp), using the primer combinations lp_1229F/
lp_1229ARko (5’-CACTTTTGTCTTGGTGGAGT-3’) and
lp_1229BFkoIII (5’-AGAGTCGCAGGCGTTAAGTA-3’)
/1229-midR, respectively. The obtained amplicons were
sequentially cloned into the SwaI- and Ecl136II-sites of
pNZ5319, respectively, in analogy to the construction
strategy described by Lambert et al. (2007). The correct
identity and orientation of the cloned fragments was
confirmed by PCR, restriction and sequence analyses
(data not shown). The resulting vector was designated
pNZ7517, containing a chloramphenicol resistance gene-
cassette flanked by the two fragments of msa of strain
299v. This plasmid was used for the construction of a
stable msa::P32cat derivative of L. plantarum 299v by
double-cross over mutagenesis, using previously described
procedures (Lambert et al., 2007; Pretzer et al., 2005). The
anticipated chromosomal organisation in the mutant strain
was confirmed by PCR and Southern Blot analysis using
standard procedures (data not shown), and the msa::P32cat
derivative of L. plantarum 299v was designated NZ7517
(pNZ5319 derivative containing fragments from the 5´- and
3´-region of L. plantarum 299v msa).
Sequencing of the msa gene in selected L. plantarum strains
The msa genes of individual L. plantarum strains
were amplified in three overlapping parts in PCR
reactions using the primer combinations 1229-ConAF
(5’-ATGTTAAAAAAGGATAATTTT-3’)/1229-ConAR
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 Msa biodiversity in L. plantarum strains

(5’-GTTGATGAGATTTCACTCCC-3’), 1229-midF Msa is the key protein involved in mannose-adhesion of

(5’-GGTAATTTAGGTATTGGTGG-3’)/1229-midR L. plantarum 299v
(5’-TGACACATGCTGCAAATCTG-3’) and 1229-mubF
(5’-GGGTAATAGTCAAGATTTCG-3’)/lp_1229R or To establish whether the msa gene is responsible for the
1229-mubRII_XhoI (5’-GTATTGCTCGAGAAACC observed mannose-specific yeast agglutination of the L.
ACTAAGCGTCAT-3), respectively. All PCR reactions plantarum strains used, this gene was amplified from
generated single amplification products, which were exemplary strain L. plantarum 299v and used for the
subjected to sequence analysis (GenBank accession construction of an msa deletion derivative of this strain
numbers: strain NC8 ‑ EU011785, strain CIP 104452 ‑ (NZ7517). In addition, the previously constructed srtA
EU011786, strain LM3 ‑ EU011787, strain ATCC 14917T ‑ mutagenesis vector (Pretzer et al., 2005) was employed to
EU011789, strain 299 ‑ EU011790). Due to the amplification generate a srtA mutant of strain 299v (NZ7518), which lacks
and sequencing strategy employed, short stretches of a functional sortase encoding gene and is therefore defective
nucleotides at the terminal 5’- and 3’-ends were not in the correct cell-wall anchoring of sortase dependent
determined, and the strain-specific msa gene sequences proteins, including Msa. Both the msa and srtA derivates
were completed with the established sequence of msa in of strain 299v completely lost their ability to agglutinate
strain WCFS1 for reasons of comparability. yeast cells (mean agglutination titre and corresponding
standard deviation (log2±SD) of both strains: 0.0±0.0 vs.
3. Results 6.7±0.6 for 299v wild type strain).

Mannose-adhesion varies among L. plantarum strains
Mannose-adhesion capacity was determined for the
individual L. plantarum strains using a yeast agglutination
assay; mean agglutination titres are depicted in Figure 1. The
L. plantarum strains varied remarkably in their quantitative
ability to induce yeast agglutination, with substantial
differences reflected in agglutination titres ranging from
0 to 7.7±0.6. For all positive strains, agglutination could be
inhibited by the addition of α-methylmannoside to the assay
buffer, confirming a mannose-specific binding mechanism
(data not shown).
The 3’-regions of msa in selected L. plantarum strains vary
in encoded MUB domain and PxxP-repeat composition
The biodiversity of msa gene domain composition among
L. plantarum strains was explored in a subset of selected
L. plantarum strains with varying mannose-adhesion
capacity, additionally to strain WCFS1 and 299v. The strains
selected for this purpose were 299, ATCC 14917T, LM3,
NC8 and CIP 104452, which previously had been shown
to agglutinate yeast cells and to contain a homologue of
msa as revealed by comparative genome hybridisation
analysis (Molenaar et al., 2005; Pretzer et al., 2005).
Sequence analysis revealed the presence of two versions,

9
Mean agglutination titer (log2±SD)

8
7
6
5
4
3
2
1
0
40

41

50

51

14

S1

80

9V

52
NC

LM

91

29
44

44

44

44

80

LP

44
CF

29
14
10

10

10

10

10
C

C
C
P

P
C
AT
CI

CI

CI

CI

CI
AT

Figure 1. Mean agglutination titres and corresponding standard deviations of L. plantarum strains determined with the yeast
agglutination assay, as calculated from three independent experiments (log2±SD). L. plantarum strains used [original designation
(NIZO culture collection; reference)]: CIP 104440 (B1838; Gasser and Sebald, 1966); CIP 104441 (B2256; Gasser and Sebald, 1966);
CIP 104450 (B2257; Gasser and Sebald, 1966); CIP 104451 (B2258; Gasser and Sebald, 1966); ATCC 8014 (B1843; Mayo et al.,
1997); WCFS1 (B1836; Kleerebezem et al., 2003); NC8 (B2261; Derzelle et al., 2000); LM3 (B2262; Muscariello et al., 2001); ATCC
14917T (B1317; Mayo et al., 1997); LP80 (B2263; Bringel et al., 2001); 299v (B2260; Johansson et al., 1993); 299 (B1837; Molin et
al., 1993); CIP 104452 (B2259; Bringel et al., 2001).
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G. Gross et al.
type I and II, of a domain with similarity to mucus-binding
domains (MUB) originally identified in a Lactobacillus
reuteri mucus-binding protein (Boekhorst et al., 2006; Roos
and Jonsson, 2002) (Figure 2). In analogy with previous
results from L. plantarum WCFS1 (Pretzer et al., 2005),
additionally a domain similar to the ConA-like lectins that
are found in SasA of Staphylococcus aureus (Robinson and
Enright, 2004; Velloso et al., 2002) could be recognised in
the Msa sequences.
Comparison of the strain-specific Msa sequences revealed
that their N-terminal parts containing the ConA-like
domain (residue 263-517), directly followed by a modified
type I MUB domain, were virtually identical up to residue
718 of Msa in all strains analysed (Figure 2). In contrast,
remarkable strain-specific differences were observed in
the 3’-region of the msa genes that include the sequences
encoding the MUB type II domains. Different numbers of
MUB type II domains and cognate PxxP-repeats (Boekhorst
et al., 2006) were found in the encoded Msa proteins of
the strains tested, ranging from one to four MUB domain
copies and from seven to twenty PxxP-units, as indicated
in Figure 2. Besides differences in the numbers of repeated
MUB-units encoded within these strain-specific msa genes,
only a few single nucleotide substitutions were detected
(data not shown). No straightforward correlation between
yeast agglutination titre and domain composition of the
C-terminal region of Msa could be detected.
4. Discussion
This study gives first insights into the structure and function
of the mannose-specific adhesin encoding gene (msa) of
L. plantarum, which might be involved in a probiotic
function of this species. The presented finding that
Number of amino acids
0 250
LM3
299
299V
NC8
ATCC 14917
WCFS1
CIP 104452
ConA-like domain
12
MUB domain type I
Figure 2. Domain composition within Msa as determined by sequencing of the msa gene in a subset of L. plantarum strains,
highlighting the variation in numbers of MUB domains and PxxP-repeats. Locations of domains were determined using the hidden
Markov model package (Durbin et al., 1998), the MUB model described by Boekhorst et al. (2006), and the ConA model from the
Superfam database (Gough et al., 2001).
64
mannose-adhesion varies among L. plantarum strains is
in agreement with previously obtained results (Tallon et al.,
2007). Apparently, strains with higher mean agglutination
titres can bind more effectively to mannose-residues and,
according to the competitive exclusion concept, would
potentially be more efficacious as a probiotic to inhibit
mannose adhesion-dependent infection of pathogens.
Corresponding with previous results from similar mutant
derivatives of L. plantarum WCFS1 (Pretzer et al., 2005), the
msa and srtA derivatives of strain 299v had completely lost
their ability to agglutinate yeast cells, indicating that also in
strain L. plantarum 299v the msa gene product represents
the key-protein involved in mannose-specific adhesion.
Other studies also indicate that one or more sortase-
dependent and mucus-binding proteins, respectively, are
involved in adhesion of lactobacilli to human epithelial cells
(Buck et al., 2005; Van Pijkeren et al., 2006). Notably, despite
the fact that mannose-specific adherence capacity of L.
plantarum 299v wild type is considerably higher than that of
strain WCFS1 (Figure 1), msa-deletion completely abolished
mannose-adhesion capacity also in this strain background.
Therefore, these results suggest that the quantitative
diversity in mannose-adhesion among L. plantarum strains
might be explained by variations in msa expression (resulting
in different levels of the encoded protein molecules) or
domain composition (resulting in a different structure of
the encoded protein molecules) rather than by the presence
or absence of additional factors involved in the process of
mannose-adherence.
To further characterise the postulated relationship between
variation in domain-composition of the msa gene and
mannose-adhesion capacity, the biodiversity of msa among
L. plantarum strains was further explored. Previous in
500 750 1000 1,250
12
16
16
20
12
7
12
MUB domain type II LP×TG-type cleavage site
PxxP region (with signal peptide cleavage site
repeat number)
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 Msa biodiversity in L. plantarum strains
silico analysis of the msa gene product in strain WCFS1
revealed a characteristic multidomain structure for cell
surface proteins of L. plantarum (Kleerebezem et al., 2003;
Pretzer et al., 2005). Notably, two domains were identified in
Msa that might be directly involved in mannose-recognition
and adhesion, i.e. a mucus-binding MUB domain and a
ConA-like domain. The two versions of MUB domains that
could be distinguished are comparable to MUB and MUB-
associated domains as described by Boekhorst et al. (2006).
MUB domains are abundant in lactobacilli that inhabit the
gastrointestinal tract, supporting a role of this domain in
adhesion capacity (Boekhorst et al., 2006). Moreover, a
larger copy-number of highly similar MUB domains in a
particular protein has been suggested to play a role in mucus
affinity, whereas the PxxP-repeats possibly have an impact
on protein flexibility (Boekhorst et al., 2006). Analogously,
the finding that a previously constructed L. plantarum
WCFS1 derivative, overexpressing msa, displayed only
a slight enhancement of its yeast agglutination capacity
as compared to the wild type strain, suggests that the
quantitative degree of yeast agglutination is not strictly
determined by msa expression level (Pretzer et al., 2005).
Moreover, the agglutination titre of this overexpression
strain was quantitatively lower than that of some of the L.
plantarum strains used in the present study. Therefore,
the variable MUB domain repeats in the Msa proteins of
different L. plantarum strains could potentially explain
the variation in mannose-adhering capacity observed in
these strains. However, the current study revealed no
straightforward correlation between yeast agglutination
titre and domain composition of the C-terminal region
of Msa. Nevertheless, our previous work, as well as this
study, strongly suggest that diversity in yeast agglutination
capacity among L. plantarum strains corresponds to genetic
variation in the msa gene. Possibly, subtle differences in
msa sequence might be involved in diverging mannose-
adhesion capacity such as variations in specific encoded
amino acid residues, whose identification would require
a more extensive and detailed study. In addition, strain-
specific genetic background, e.g. leading to different cell
wall structural features, could contribute to more or less
optimal functioning of Msa. Further experiments, including
msa domain-exchange and expression of different msa
derivatives in an identical background, could give further
insights into the role of structural differences and variation
in expression of msa in relation to mannose-adhesion
capacity.
5. Conclusions
In conclusion, the current study demonstrates that Msa
is the sole factor responsible for mannose-adhesion
capacity in both poorly and strongly adhering L. plantarum
strains. The results presented here suggest that diversity of
mannose-adhesion capacity among L. plantarum strains
extends beyond the simple presence and absence of the
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msa gene. This diversity can not solely be explained by
variations in msa expression and apparently corresponds
with strain-specific Msa sequence variation and domain
composition. These findings illustrate the strain-specificity
of candidate probiotic characteristics and indicate that
probiotic bacteria have to be selected with care since
even closely related strains can differ in ‘probiotic gene’
sequence and the corresponding functional trait. However,
the conditions for bacterial binding to the intestinal surface
in vivo are more complex than represented in the mannose-
specific yeast agglutination assay in vitro. Therefore, the
impact of msa on probiotic functionality such as in vivo
adherence, and eventually competitive exclusion, requires
further investigation. At present, the msa-derivative of L.
plantarum 299v is employed to evaluate the functional
relevance of mannose-adhesion and msa as a potential
‘probiotic gene’ for bacterial persistence and competitive
exclusion of pathogens in the intestine.
Acknowledgements
The authors would like to thank Roger Bongers and Jolanda
Lambert for excellent technical support in the molecular
genetics activities. This project was supported by the Centre
for Human Nutrigenomics, the Netherlands.
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