Critical roles of a housekeeping sortase of probiotic Bifidobacterium bifidum in bacterium–host cell crosstalk

Ishikawa, Eiji; Yamada, Tetsuya; Yamaji, Kazuaki; Serata, Masaki; Fujii, Daichi; Umesaki, Yoshinori; Tsuji, Hirokazu; Nomoto, Koji; Ito, Masahiro; Okada, Nobuhiko; Nagaoka, Masato; Gomi, A.

doi:10.1016/j.isci.2021.103363

Cited by 3 publications

(7 citation statements)

References 62 publications

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“…The pilus shaft components encoded by fimA and fimP are polymerized and assembled with pilus tip components (encoded by fimB and fimQ) by an adjacent class C sortase (srtC). A further class of sortase enzymes [sortase E (srtE)] has also recently been found to be critical for bifidobacterial adhesion (Ishikawa et al, 2021). It is clear, therefore, that specific sortase enzymes may contribute to the adherence phenotypes observed in this study.…”

Section: Mining Of Bifidobacterial Sequences For Colonization-related...mentioning

confidence: 65%

“…In general, the adhesion of B. bifidum in vitro is exceptionally strong among probiotics (Shibahara-Sone et al, 2016) and therefore the high levels of adherence observed in this study may be expected. Such characteristics might arise from the vast array of proteins specific to B. bifidum as described in a recent study (Ishikawa et al, 2021). The survey of the bacterial genomes for colonisation-related factors revealed a number of components that bacteria can potentially interact with to adhere to mucus and epithelial surface glycans, e.g., outer-membrane proteins, adhesins, capsules and appendages such as pili, flagella, and fimbriae (Paone and Cani, 2020).…”

Section: Discussionmentioning

confidence: 97%

“…Scientific literature databases including PubMed, Web of Science, UCC library, and Google Scholar were searched for studies providing mechanistic insight into probiotic colonization and survival in the gastrointestinal tract. A list of probiotic (Lactobacillus and Bifidobacterium genera) colonisation-related features (Supplementary Table S3) was then compiled from these studies which included gene-trait matching, transcriptomic, proteomic, and knock-out studies (Tanaka et al, 2000;Walter et al, 2005Walter et al, , 2007Walter et al, , 2008Bron et al, 2007;Guglielmetti et al, 2008;Shkoporov et al, 2008;Gueimonde et al, 2009;Kankainen et al, 2009;Foroni et al, 2011;Frese et al, 2011Frese et al, , 2013O'Connell Motherway et al, 2011;Sims et al, 2011;Fanning et al, 2012;González-Rodríguez et al, 2012;Turroni et al, 2013;Christiaen et al, 2014;Goh and Klaenhammer, 2014;Liu et al, 2014;Wilson et al, 2014;Call et al, 2015;Ganesh et al, 2018;Ishikawa et al, 2021). A Blast search was then performed (e-value cutoff of 1e-5, query cover cutoff of 50%) of the database against the bifidobacterial genomes of interest.…”

Section: Prediction Of Colonisation Capabilitiesmentioning

confidence: 99%

“…These sortase-enzymes work by covalently attaching specific sortase-dependent proteins (SDPs) to the cell-wall of gram-positive organisms by recognizing a conserved C-terminal motif. Therefore, to understand if variances in SDPs could account for variances in adherence of the strains studied here, the bifidobacterial proteomes were searched for proteins with a signal peptide at the N-terminus, the srtC (LPXTG) or srtE ([L/I/V][S/A]XTG) recognition motif, followed by a stretch of hydrophobic amino acids and a positively charged C-terminus as previously described (Call and Klaenhammer, 2013;Ishikawa et al, 2021). We found nine such proteins in B. breve M-16 V (Supplementary Figure S2; Supplementary Table S4), 13 in B. infantis R0033 (Supplementary Figure S2; Supplementary Table S5), and 10 in B. infantis M-63 (Supplementary Figure S2; Supplementary Table S6).…”

Section: Mining Of Bifidobacterial Sequences For Colonization-related...mentioning

confidence: 99%

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HMO-primed bifidobacteria exhibit enhanced ability to adhere to intestinal epithelial cells

Walsh,

Owens,

Bottacini

et al. 2023

Front. Microbiol.

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The ability of gut commensals to adhere to the intestinal epithelium can play a key role in influencing the composition of the gut microbiota. Bifidobacteria are associated with a multitude of health benefits and are one of the most widely used probiotics for humans. Enhanced bifidobacterial adhesion may increase host-microbe, microbe-nutrient, and/or microbe-microbe interactions, thereby enabling consolidated health benefits to the host. The objective of this study was to determine the ability of human milk oligosaccharides (HMOs) to enhance bifidobacterial intestinal adhesion in vitro. This study assessed the colonisation-promoting effects of HMOs on four commercial infant-associated Bifidobacterium strains (two B. longum subsp. infantis strains, B. breve and B. bifidum). HT29-MTX cells were used as an in vitro intestinal model for bacterial adhesion. Short-term exposure of four commercial infant-associated Bifidobacterium strains to HMOs derived from breastmilk substantially increased the adherence (up to 47%) of these probiotic strains. Interestingly, when strains were incubated with HMOs as a four-strain combination, the number of viable bacteria adhering to intestinal cells increased by >90%. Proteomic analysis of this multi-strain bifidobacterial mixture revealed that the increased adherence resulting from exposure to HMOs was associated with notable increases in the abundance of sortase-dependent pili and glycosyl hydrolases matched to Bifidobacterium bifidum. This study suggests that HMOs may prime infant gut-associated Bifidobacterium for colonisation to intestinal epithelial cells by influencing the expression of various colonization factors.

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Section: Mining Of Bifidobacterial Sequences For Colonization-related...mentioning

confidence: 65%

Section: Discussionmentioning

confidence: 97%

Section: Prediction Of Colonisation Capabilitiesmentioning

confidence: 99%

Section: Mining Of Bifidobacterial Sequences For Colonization-related...mentioning

confidence: 99%

See 2 more Smart Citations

HMO-primed bifidobacteria exhibit enhanced ability to adhere to intestinal epithelial cells

Walsh,

Owens,

Bottacini

et al. 2023

Front. Microbiol.

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“…However, the mechanisms involved in their colonization and survival in the intestine have not been fully established. Several factors are involved in their colonization and survival: type IVb tight adherence pili [ 2 ], surface exopolysaccharides [ 3 ], and the luxS autoinducer-2-producing gene [ 4 ] in Bifidobacterium breve UCC2003; sortase-dependent pili [ 5 ], the SiaBb2 sialidase [ 6 ], and a housekeeping sortase [ 7 ] in Bifidobacterium bifidum ; and several housekeeping proteins in the extracellular vesicles of Bifidobacterium longum NCC2705 [ 8 ].…”

Section: Introductionmentioning

confidence: 99%

Development of an improved colonization system for human-derived <i>Bifidobacterium longum</i> subsp. <i>longum</i> in conventional mice through the feeding of raffinose or 1-kestose

SHIMADA,

KAWASE,

SONOYAMA

et al. 2024

Bioscience of Microbiota, Food and Health

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How bifidobacteria colonize and survive in the intestine is not fully understood. The administration of bifidobacteria to conventional mice can be used to evaluate their ability to colonize the intestine in the presence of endogenous gut microbiota. However, human-derived bifidobacteria do not readily colonize the intestines of conventional mice, and although colonization by Bifidobacterium breve UCC2003 has been achieved, the viability of such populations requires improvement. Therefore, we aimed to establish a colonization system with human-derived bifidobacteria of high viability in conventional mice using Bifidobacterium longum subsp. longum 105-A. Lactose, raffinose, and 1-kestose were identified as the preferred carbohydrate sources for the growth of this strain in culture. The administration of B. longum 105-A to conventional BALB/c mice fed these carbohydrates showed that diets containing 6% (w/w) raffinose or 1-kestose facilitated colonization with >10 8 colony-forming units/g feces for 2 weeks. The population of this strain was more stable in the raffinose-fed group than in the 1-kestose-fed group. The ingestion of these prebiotics had a greater impact on the composition of the microbiota than the administration of B. longum 105-A. The ingestion of these prebiotics also increased the fecal concentrations of organic acids, which was indicative of greater intestinal fermentation. Collectively, we established a colonization system for B. longum 105-A with high viability in conventional mice by feeding the mice raffinose or 1-kestose. This system should be useful for elucidation of the mechanisms of colonization and survival of bifidobacteria in the intestines in the presence of the endogenous gut microbiota.

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Bacterial Enzyme Assay for Mucin Glycan Degradation

Katoh,

Ashida

2024

Methods in Molecular Biology

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Critical roles of a housekeeping sortase of probiotic Bifidobacterium bifidum in bacterium–host cell crosstalk

Cited by 3 publications

References 62 publications

HMO-primed bifidobacteria exhibit enhanced ability to adhere to intestinal epithelial cells

HMO-primed bifidobacteria exhibit enhanced ability to adhere to intestinal epithelial cells

Development of an improved colonization system for human-derived <i>Bifidobacterium longum</i> subsp. <i>longum</i> in conventional mice through the feeding of raffinose or 1-kestose

Bacterial Enzyme Assay for Mucin Glycan Degradation

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