The Sortase-Dependent Fimbriome of the Genus Bifidobacterium: Extracellular Structures with Potential To Modulate Microbe-Host Dialogue

Milani, Christian; Mangifesta, Marta; Mancabelli, Leonardo; Lugli, Gabriele Andrea; Mancino, Walter; Viappiani, Alice; Faccini, Andrea; Sinderen, Douwe van; Ventura, Marco; Turroni, Francesca

doi:10.1128/aem.01295-17

Cited by 34 publications

(43 citation statements)

References 67 publications

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“…A very recent study showed these sortase-dependent pili to be ubiquitous in Bifidobacterium spp. and some coded for FimB subunits that were able to bind starch, xylan and pectin, indicative of a luminal location, while others showed interaction with the host [ 18 , 88 ].…”

Section: Resultsmentioning

confidence: 99%

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Comparative genomic analysis of the multispecies probiotic-marketed product VSL#3

et al. 2018

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Several probiotic-marketed formulations available for the consumers contain live lactic acid bacteria and/or bifidobacteria. The multispecies product commercialized as VSL#3 has been used for treating various gastro-intestinal disorders. However, like many other products, the bacterial strains present in VSL#3 have only been characterized to a limited extent and their efficacy as well as their predicted mode of action remain unclear, preventing further applications or comparative studies. In this work, the genomes of all eight bacterial strains present in VSL#3 were sequenced and characterized, to advance insights into the possible mode of action of this product and also to serve as a basis for future work and trials. Phylogenetic and genomic data analysis allowed us to identify the 7 species present in the VSL#3 product as specified by the manufacturer. The 8 strains present belong to the species Streptococcus thermophilus, Lactobacillus acidophilus, Lactobacillus paracasei, Lactobacillus plantarum, Lactobacillus helveticus, Bifidobacterium breve and B. animalis subsp. lactis (two distinct strains). Comparative genomics revealed that the draft genomes of the S. thermophilus and L. helveticus strains were predicted to encode most of the defence systems such as restriction modification and CRISPR-Cas systems. Genes associated with a variety of potential probiotic functions were also identified. Thus, in the three Bifidobacterium spp., gene clusters were predicted to encode tight adherence pili, known to promote bacteria-host interaction and intestinal barrier integrity, and to impact host cell development. Various repertoires of putative signalling proteins were predicted to be encoded by the genomes of the Lactobacillus spp., i.e. surface layer proteins, LPXTG-containing proteins, or sortase-dependent pili that may interact with the intestinal mucosa and dendritic cells. Taken altogether, the individual genomic characterization of the strains present in the VSL#3 product confirmed the product specifications, determined its coding capacity as well as identified potential probiotic functions.

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Section: Resultsmentioning

confidence: 99%

“…A specific set of Tad pili and sortase-dependent pili has been discovered in B . breve that are involved in intestinal persistence and the host-microbe dialogue [ 17 , 18 ]. Surface exopolysaccharides in B .…”

Section: Introductionmentioning

confidence: 99%

Comparative genomic analysis of the multispecies probiotic-marketed product VSL#3

et al. 2018

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“…Pili or fimbriae are proteinaceous extracellular appendages produced by many bacteria, that protrude from the bacterial cell surface and that can be involved in microbe-host interactions promoting adhesion to the intestinal epithelium or facilitating aggregation with other bacterial cells (Scott and Zahner, 2006;Kline et al, 2010;Foroni et al, 2011). Two different types of pili have been described in bifidobacteria, i.e., sortase-dependent pili, and the type IVb pili, both of which are also known as tight adherence pili (Tad pili) (O'Connell Motherway et al, 2011;Milani et al, 2017b). Bifidobacterial sortase-dependent pili are not only responsible for adhesion and interaction with the host, but also are involved in the microbe-microbe interactions and in stimulation/modulation of the host immune system.…”

Section: Pili/fimbriaementioning

confidence: 99%

Microbiota and Cancer: The Emerging Beneficial Role of Bifidobacteria in Cancer Immunotherapy

et al. 2020

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Many intestinal bacteria are believed to be involved in various inflammatory and immune processes that influence tumor etiology because of their metabolic properties and their ability to alter the microbiota homeostasis. Although many functions of the microbiota are still unclear, there is compelling experimental evidence showing that the intestinal microbiota is able to modulate carcinogenesis and the response to anticancer therapies, both in the intestinal tract and other body sites. Among the wide variety of gut-colonizing microorganisms, various species belonging to the Bifidobacterium genus are believed to elicit beneficial effects on human physiology and on the host-immune system. Recent findings, based on preclinical mouse models and on human clinical trials, have demonstrated the impact of gut commensals including bifidobacteria on the efficacy of tumor-targeting immunotherapy. Although the underlying molecular mechanisms remain obscure, bifidobacteria and other microorganisms have become a promising aid to immunotherapeutic procedures that are currently applied to treat cancer. The present review focuses on strategies to recruit the microbiome in order to enhance anticancer responses and develop therapies aimed at fighting the onset and progression of malignancies.

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“…The Bifidobacterium genus currently consists of 56 species and 9 subspecies, members of which have been isolated from human, other mammalian, and certain insect intestinal contents (11,12). Recently, it has been demonstrated that members of the genus Bifidobacterium interact with other bacterial species and the host using extracellular structures, such as sortase-dependent pili and type IVb tight adherence (Tad) pili (13)(14)(15). Furthermore, extracellular anti-inflammatory proteins, such as the serine protease inhibitor (serpin) protein, were identified in several bifidobacterial species (16,17), as well as extracellular macromolecules, like exopolysaccharides (EPSs), which form a glycan slime layer that is loosely attached to the cell (18,19).…”

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Reconstruction of the Bifidobacterial Pan-Secretome Reveals the Network of Extracellular Interactions between Bifidobacteria and the Infant Gut

Lugli

Mancino

Milani

et al. 2018

Appl Environ Microbiol

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The repertoire of secreted proteins decoded by a microorganism represents proteins released from or associated with the cell's surface. In gut commensals, such as bifidobacteria, these proteins are perceived to be functionally relevant as they regulate the interaction with the gut environment. In the current study, we have screened the predicted proteome of over 300 bifidobacterial strains amongst the currently recognized bifidobacterial species to generate a comprehensive database encompassing bifidobacterial extracellular proteins. A glycobiome analysis of this predicted bifidobacterial secretome revealed that a correlation exists between particular bifidobacterial species and their capability to hydrolyze HMOs and intestinal glyconjugates such as mucin. Furthermore, exploration of metatranscriptomic datasets of the infant gut microbiota allowed the evaluation of the expression of bifidobacterial genes encoding extracellular proteins, represented by ABC transporter substrate-binding proteins and glycoside hydrolases enzymes involved in the degradation of human milk oligosaccharides and mucin. Overall, this study provides insights into how bifidobacteria interact with their natural yet highly complex environment, the infant gut. The ecological success of bifidobacteria relies on the activity of extracellular proteins that are involved in the metabolism of nutrients and the interaction with the environment. To date, information on secreted proteins encoded by bifidobacteria are incomplete and just related to few species. In this study, we reconstructed the bifidobacterial pan-secretome, revealing extracellular proteins that modulate the interaction of bifidobacteria with their natural environment. Furthermore, a survey of secretion system between bifidobacterial genomes allowed the identification of a conserved Sec-dependent secretion machinery in all the analyzed genomes and the Tat protein translocation system in the chromosomes of 23 strains belonging to subsp. and .

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The Sortase-Dependent Fimbriome of the Genus Bifidobacterium: Extracellular Structures with Potential To Modulate Microbe-Host Dialogue

Cited by 34 publications

References 67 publications

Comparative genomic analysis of the multispecies probiotic-marketed product VSL#3

Comparative genomic analysis of the multispecies probiotic-marketed product VSL#3

Microbiota and Cancer: The Emerging Beneficial Role of Bifidobacteria in Cancer Immunotherapy

Reconstruction of the Bifidobacterial Pan-Secretome Reveals the Network of Extracellular Interactions between Bifidobacteria and the Infant Gut

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