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Cited by 133Probiotics and Fermented FoodsBacterial Genetics and BiotechnologyPolysaccharides Composition and Applications

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Impact of 4 Lactobacillus plantarum capsular polysaccharide clusters on surface glycan composition and host cell signaling

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Remus, Daniela M, van Kranenburg, Richard, van Swam, Iris I, Taverne, Nico, Bongers, Roger S, Wels, Michiel, Wells, Jerry M, Bron, Peter A, Kleerebezem, Michiel·2012·Microbial Cell Factories
DOI 10.1186/1475-2859-11-149PMC PMC3539956
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Abstract

BACKGROUND: Bacterial cell surface-associated polysaccharides are involved in the interactions of bacteria with their environment and play an important role in the communication between pathogenic bacteria and their host organisms. Cell surface polysaccharides of probiotic species are far less well described. Therefore, improved knowledge on these molecules is potentially of great importance to understand the strain-specific and proposed beneficial modes of probiotic action. RESULTS: The Lactobacillus plantarum WCFS1 genome encodes 4 clusters of genes that are associated with surface polysaccharide production. Two of these clusters appear to encode all functions required for capsular polysaccharide formation (cps2A-J and cps4A-J), while the remaining clusters are predicted to lack genes encoding chain-length control functions and a priming glycosyl-transferase (cps1A-I and cps3A-J). We constructed L. plantarum WCFS1 gene deletion mutants that lack individual (Δcps1A-I, Δcps2A-J, Δcps3A-J and Δcps4A-J) or combinations of cps clusters (Δcps1A-3J and Δcps1A-3I, Δcps4A-J) and assessed the genome wide impact of these mutations by transcriptome analysis. The cps cluster deletions influenced the expression of variable gene sets in the individual cps cluster mutants, but also considerable numbers of up- and down-regulated genes were shared between mutants in cps cluster 1 and 2, as well as between mutant in cps clusters 3 and 4. Additionally, the composition of overall cell surface polysaccharide fractions was altered in each mutant strain, implying that despite the apparent incompleteness of cps1A-I and cps3A-J, all clusters are active and functional in L. plantarum. The Δcps1A-I strain produced surface polysaccharides in equal amounts as compared to the wild-type strain, while the polysaccharides were characterized by a reduced molar mass and the lack of rhamnose. The mutants that lacked functional copies of cps2A-J, cps3A-J or cps4A-J produced decreased levels of surface polysaccharides, whereas the molar mass and the composition of polysaccharides was not affected by these cluster mutations. In the quadruple mutant, the amount of surface polysaccharides was strongly reduced. The impact of the cps cluster mutations on toll-like receptor (TLR)-mediated human nuclear factor (NF)-κB activation in host cells was evaluated using a TLR2 reporter cell line. In comparison to a L. plantarum wild-type derivative, TLR2 activation remained unaffected by the Δcps1A-I and Δcps3A-J mutants but appeared slightly increased after stimulation with the Δcps2A-J and Δcps4A-J mutants, while the Δcps1A-3J and Δcps1A-3J, Δcps4A-J mutants elicited the strongest responses and clearly displayed enhanced TLR2 signaling. CONCLUSIONS: Our study reveals that modulation of surface glycan characteristics in L. plantarum highlights the role of these molecules in shielding of cell envelope embedded host receptor ligands. Although the apparently complete cps clusters (cps2A-J and cps4A-J) contributed individually to this shielding, the removal of all cps clusters led to the strongest signaling enhancement. Our findings provide new insights into cell surface glycan biosynthesis in L. plantarum, which bears relevance in the context of host-cell signaling by probiotic bacteria.

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Figures

Figure 1 Genetic organization of polysaccharide biosynthesis gene clusters in L. plantarum strains. (A) Genetic organization of the L. plantarum WCFS1 polysaccharide biosynthesis gene clusters 1, 2, and 3 (AL935263; lp_1176 through lp_1234) and comparison with the corresponding regions of L. plantarum strains ST-III (NC_014554; LPST_C0945 through LPST_C0997), JDM-1 (NC_012984; JDM1_1015 through JDM1_1041), and ATCC 14917 (ACGZ02000014; HMPREF0531_11685 through HMPREF0531_11729; ACGZ02000010; HMPREF0531_11316 through HMPREF0531_11319). Dark-grey colored connecting blocks indicate regions of high sequence conservation identified in the genomes of the indicated strains. The white area connecting msa homologues gene of ST-III and JDM-1, indicates that this gene is separated on two contigs in the draft genome sequence available for ATCC14917. (B) Genetic organization of the L. plantarum WCFS1 polysaccharide biosynthesis gene cluster 4. The corresponding regions are conserved in L. plantarum ST-III, ATCC 14917, and JDM1 sharing 99%, 99%, and 97% nucleotide identity with WCFS 1, respectively. Arrows indicate predicted promoters with e-value ≤ 10-5[27].
Figure 1 Genetic organization of polysaccharide biosynthesis gene clusters in L. plantarum strains. (A) Genetic organization of the L. plantarum WCFS1 polysaccharide biosynthesis gene clusters 1, 2, and 3 (AL935263; lp_1176 through lp_1234) and comparison with the corresponding regions of L. plantarum strains ST-III (NC_014554; LPST_C0945 through LPST_C0997), JDM-1 (NC_012984; JDM1_1015 through JDM1_1041), and ATCC 14917 (ACGZ02000014; HMPREF0531_11685 through HMPREF0531_11729; ACGZ02000010; HMPREF0531_11316 through HMPREF0531_11319). Dark-grey colored connecting blocks indicate regions of high sequence conservation identified in the genomes of the indicated strains. The white area connecting msa homologues gene of ST-III and JDM-1, indicates that this gene is separated on two contigs in the draft genome sequence available for ATCC14917. (B) Genetic organization of the L. plantarum WCFS1 polysaccharide biosynthesis gene cluster 4. The corresponding regions are conserved in L. plantarum ST-III, ATCC 14917, and JDM1 sharing 99%, 99%, and 97% nucleotide identity with WCFS 1, respectively. Arrows indicate predicted promoters with e-value ≤ 10-5[27].CC BY · PubMed Central
Figure 2 Growth phase dependent gene expression levels of individual cps gene clusters in L. plantarum WCFS1. Data is represented as average expression of cps genes of cluster 1 (circles), 2 (squares), 3 (upward pointing arrowheads) and 4(downward pointing arrowheads). Error bars represent the range of expression between the highest and lowest expressed gene in the different clusters.
Figure 2 Growth phase dependent gene expression levels of individual cps gene clusters in L. plantarum WCFS1. Data is represented as average expression of cps genes of cluster 1 (circles), 2 (squares), 3 (upward pointing arrowheads) and 4(downward pointing arrowheads). Error bars represent the range of expression between the highest and lowest expressed gene in the different clusters.CC BY · PubMed Central
Figure 3 Impact of cps cluster deletion on host cell signaling measured by a luminescence reporter in TLR2-expressing HEK-293 cells. Data is represented as average +/− the range between 2 independently grown bacterial cultures (15 CFU/HEK-293 cell) of the L. plantarum wild-type like derivative (NZ3400Cm) and cps deletion mutants (NZ3548cm/Δcps1A-I, NZ5333ACm/Δcps2A-J, NZ3549Cm/Δcps3A-J, NZ3534Cm/Δcps4A-J, NZ3550Cm/ Δcps1A-3J and NZ3680Cm/Δcps1A-3J, Δcps4A-J).
Figure 3 Impact of cps cluster deletion on host cell signaling measured by a luminescence reporter in TLR2-expressing HEK-293 cells. Data is represented as average +/− the range between 2 independently grown bacterial cultures (15 CFU/HEK-293 cell) of the L. plantarum wild-type like derivative (NZ3400Cm) and cps deletion mutants (NZ3548cm/Δcps1A-I, NZ5333ACm/Δcps2A-J, NZ3549Cm/Δcps3A-J, NZ3534Cm/Δcps4A-J, NZ3550Cm/ Δcps1A-3J and NZ3680Cm/Δcps1A-3J, Δcps4A-J).CC BY · PubMed Central

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Metadata

Authors
Remus, D. M., van Kranenburg, R., van Swam, I. I., Taverne, N., Bongers, R. S., Wels, M., Wells, J. M., Bron, P. A., & Kleerebezem, M.
Affiliations
TiFN (NL)
Corresponding author
Kleerebezem, Michiel
ORCID
Venue
Microbial Cell Factories
Publisher
Springer Science and Business Media LLC
Published
2012-11-21
Volume
11
Issue
1
Pages
149-149
ISSN
1475-2859 (ISSN-L)
DOI
10.1186/1475-2859-11-149
PMC
PMC3539956
OpenAlex
W2097092342
Cited by
131
References
52
Citations by year
2026: 15 · 2025: 10 · 2024: 9 · 2023: 9 · 2022: 15 · 2021: 12 · 2020: 11 · 2019: 8 · 2018: 8 · 2017: 8 · 2016: 10 · 2015: 5 · 2014: 5 · 2013: 5
FWCI
7.38
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Microbial Cell Factories (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Socio-Environmental Systems Modeling (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Polysaccharides Composition and Applications
Keywords
Lactobacillus plantarum WCFS1, capsular polysaccharide, deletion mutants, transcriptome, host cell signaling, NF-κB activation, TLR2, probiotic bacteria, rhamnose, molar mass, host-pathogen interaction
MeSH terms
Bacterial Proteins, Multigene Family, Humans, Mutation, Polysaccharides, Bacterial, Signal Transduction, NF-kappa B, Glycosyltransferases, Gene Deletion, Gene Expression Profiling, Lactobacillus plantarum, Lactiplantibacillus plantarum, Toll-Like Receptor 2, HEK293 Cells

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