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Diversification of a Fucosyllactose Transporter within the Genus Bifidobacterium.
Appl Environ Microbiol. 2022 01 25; 88(2):e0143721.AE

Abstract

Human milk oligosaccharides (HMOs), which are natural bifidogenic prebiotics, were recently commercialized to fortify formula milk. However, HMO assimilation phenotypes of bifidobacteria vary by species and strain, which has not been fully linked to strain genotype. We have recently shown that specialized uptake systems, particularly for the internalization of major HMOs (fucosyllactose [FL]), are associated with the formation of a Bifidobacterium-rich gut microbial community. Phylogenetic analysis revealed that FL transporters have diversified into two clades harboring four clusters within the Bifidobacterium genus, but the underpinning functional diversity associated with this divergence remains underexplored. In this study, we examined the HMO consumption phenotypes of two bifidobacterial species, Bifidobacterium catenulatum subsp. kashiwanohense and Bifidobacterium pseudocatenulatum, both of which possess FL-binding proteins that belong to phylogenetic clusters with unknown specificities. Growth assays, heterologous gene expression experiments, and HMO consumption analyses showed that the FL transporter type from B. catenulatum subsp. kashiwanohense JCM 15439T conferred a novel HMO uptake pattern that includes complex fucosylated HMOs (lacto-N-fucopentaose II and lacto-N-difucohexaose I/II). Further genomic landscape analyses of FL transporter-positive bifidobacterial strains revealed that the H-antigen- or Lewis antigen-specific fucosidase gene(s) and FL transporter specificities were largely aligned. These results suggest that bifidobacteria have acquired FL transporters along with the corresponding gene sets necessary to utilize the imported HMOs. Our results provide insight into the species- and strain-dependent adaptation strategies of bifidobacteria in HMO-rich environments. IMPORTANCE The gut of breastfed infants is generally dominated by health-promoting bifidobacteria. Human milk oligosaccharides (HMOs) from breast milk selectively promote the growth of specific taxa such as bifidobacteria, thus forming an HMO-mediated host-microbe symbiosis. While the coevolution of humans and bifidobacteria has been proposed, the underpinning adaptive strategies employed by bifidobacteria require further research. Here, we analyzed the divergence of the critical fucosyllactose (FL) HMO transporter within Bifidobacterium. We have shown that the diversification of the solute-binding proteins of the FL transporter led to uptake specificities of fucosylated sugars ranging from simple trisaccharides to complex hexasaccharides. This transporter and the congruent acquisition of the necessary intracellular enzymes allow bifidobacteria to consume different types of HMOs in a predictable and strain-dependent manner. These findings explain the adaptation and proliferation of bifidobacteria in the competitive and HMO-rich infant gut environment and enable accurate specificity annotation of transporters from metagenomic data.

Authors+Show Affiliations

Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.Faculty of Agriculture, Niigata Universitygrid.260975.f, Niigata, Japan.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.School of Human Cultures, The University of Shiga Prefecture, Hikone, Shiga, Japan.Department of Food and Life Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, Japan.Research Faculty of Agriculture, Hokkaido Universitygrid.39158.36, Sapporo, Hokkaido, Japan.Research Faculty of Agriculture, Hokkaido Universitygrid.39158.36, Sapporo, Hokkaido, Japan.Department of Biotechnology and Bioengineering, Technical University of Denmarkgrid.5170.3, Lyngby, Denmark.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.Graduate School of Biostudies, Kyoto Universitygrid.258799.8, Kyoto, Japan.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

34731055

Citation

Ojima, Miriam N., et al. "Diversification of a Fucosyllactose Transporter Within the Genus Bifidobacterium." Applied and Environmental Microbiology, vol. 88, no. 2, 2022, pp. e0143721.
Ojima MN, Asao Y, Nakajima A, et al. Diversification of a Fucosyllactose Transporter within the Genus Bifidobacterium. Appl Environ Microbiol. 2022;88(2):e0143721.
Ojima, M. N., Asao, Y., Nakajima, A., Katoh, T., Kitaoka, M., Gotoh, A., Hirose, J., Urashima, T., Fukiya, S., Yokota, A., Abou Hachem, M., Sakanaka, M., & Katayama, T. (2022). Diversification of a Fucosyllactose Transporter within the Genus Bifidobacterium. Applied and Environmental Microbiology, 88(2), e0143721. https://doi.org/10.1128/AEM.01437-21
Ojima MN, et al. Diversification of a Fucosyllactose Transporter Within the Genus Bifidobacterium. Appl Environ Microbiol. 2022 01 25;88(2):e0143721. PubMed PMID: 34731055.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Diversification of a Fucosyllactose Transporter within the Genus Bifidobacterium. AU - Ojima,Miriam N, AU - Asao,Yuya, AU - Nakajima,Aruto, AU - Katoh,Toshihiko, AU - Kitaoka,Motomitsu, AU - Gotoh,Aina, AU - Hirose,Junko, AU - Urashima,Tadasu, AU - Fukiya,Satoru, AU - Yokota,Atsushi, AU - Abou Hachem,Maher, AU - Sakanaka,Mikiyasu, AU - Katayama,Takane, Y1 - 2021/11/03/ PY - 2021/11/4/pubmed PY - 2022/3/25/medline PY - 2021/11/3/entrez KW - Bifidobacterium KW - fucosidase KW - fucosyllactose transporter KW - human milk oligosaccharides (HMOs) SP - e0143721 EP - e0143721 JF - Applied and environmental microbiology JO - Appl Environ Microbiol VL - 88 IS - 2 N2 - Human milk oligosaccharides (HMOs), which are natural bifidogenic prebiotics, were recently commercialized to fortify formula milk. However, HMO assimilation phenotypes of bifidobacteria vary by species and strain, which has not been fully linked to strain genotype. We have recently shown that specialized uptake systems, particularly for the internalization of major HMOs (fucosyllactose [FL]), are associated with the formation of a Bifidobacterium-rich gut microbial community. Phylogenetic analysis revealed that FL transporters have diversified into two clades harboring four clusters within the Bifidobacterium genus, but the underpinning functional diversity associated with this divergence remains underexplored. In this study, we examined the HMO consumption phenotypes of two bifidobacterial species, Bifidobacterium catenulatum subsp. kashiwanohense and Bifidobacterium pseudocatenulatum, both of which possess FL-binding proteins that belong to phylogenetic clusters with unknown specificities. Growth assays, heterologous gene expression experiments, and HMO consumption analyses showed that the FL transporter type from B. catenulatum subsp. kashiwanohense JCM 15439T conferred a novel HMO uptake pattern that includes complex fucosylated HMOs (lacto-N-fucopentaose II and lacto-N-difucohexaose I/II). Further genomic landscape analyses of FL transporter-positive bifidobacterial strains revealed that the H-antigen- or Lewis antigen-specific fucosidase gene(s) and FL transporter specificities were largely aligned. These results suggest that bifidobacteria have acquired FL transporters along with the corresponding gene sets necessary to utilize the imported HMOs. Our results provide insight into the species- and strain-dependent adaptation strategies of bifidobacteria in HMO-rich environments. IMPORTANCE The gut of breastfed infants is generally dominated by health-promoting bifidobacteria. Human milk oligosaccharides (HMOs) from breast milk selectively promote the growth of specific taxa such as bifidobacteria, thus forming an HMO-mediated host-microbe symbiosis. While the coevolution of humans and bifidobacteria has been proposed, the underpinning adaptive strategies employed by bifidobacteria require further research. Here, we analyzed the divergence of the critical fucosyllactose (FL) HMO transporter within Bifidobacterium. We have shown that the diversification of the solute-binding proteins of the FL transporter led to uptake specificities of fucosylated sugars ranging from simple trisaccharides to complex hexasaccharides. This transporter and the congruent acquisition of the necessary intracellular enzymes allow bifidobacteria to consume different types of HMOs in a predictable and strain-dependent manner. These findings explain the adaptation and proliferation of bifidobacteria in the competitive and HMO-rich infant gut environment and enable accurate specificity annotation of transporters from metagenomic data. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/34731055/Diversification_of_a_Fucosyllactose_Transporter_within_the_Genus_Bifidobacterium_ DB - PRIME DP - Unbound Medicine ER -