Bifidobacterium breve UCC2003 exopolysaccharide modulates the early life microbiota by acting as a potential dietary substrate

Deborah Püngel; Agatha Treveil; Matthew J. Dalby; Shabhonam Caim; Ian J Colquhoun; Catherine Booth; Jennifer Ketskemety; Tamas Korcsmaros; Douwe van Sinderen; Melissa AE Lawson; Lindsay J Hall

doi:10.3390/nu12040948

Bifidobacterium breve UCC2003 exopolysaccharide modulates the early life microbiota by acting as a potential dietary substrate

Deborah Püngel, Agatha Treveil, Matthew J. Dalby, Shabhonam Caim, Ian J Colquhoun, Catherine Booth, Jennifer Ketskemety, Tamas Korcsmaros, Douwe van Sinderen, Melissa AE Lawson^*, Lindsay J Hall^*

^*Corresponding author for this work

Microbiology and Infection

Research output: Contribution to journal › Article › peer-review

15 Citations (Scopus)

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Abstract

Background: Bifidobacterium represents an important early life microbiota member. Specific bifidobacterial components, exopolysaccharides (EPS), positively modulate host responses, with purified EPS also suggested to impact microbe–microbe interactions by acting as a nutrient substrate. Thus, we determined the longitudinal effects of bifidobacterial EPS on microbial communities and metabolite profiles using an infant model colon system.

Methods: Differential gene expression and growth characteristics were determined for each strain; Bifidobacterium breve UCC2003 and corresponding isogenic EPS-deletion mutant (B. breve UCC2003del). Model colon vessels were inoculated with B. breve and microbiome dynamics monitored using 16S rRNA sequencing and metabolomics (NMR).

Results: Transcriptomics of EPS mutant vs. B. breve UCC2003 highlighted discrete differential gene expression (e.g., eps biosynthetic cluster), though overall growth dynamics between strains were unaffected. The EPS-positive vessel had significant shifts in microbiome and metabolite profiles until study end (405 h); with increases of Tyzzerella and Faecalibacterium, and short-chain fatty acids, with further correlations between taxa and metabolites which were not observed within the EPS-negative vessel.

Conclusions: These data indicate that B. breve UCC2003 EPS is potentially metabolized by infant microbiota members, leading to differential microbial metabolism and altered metabolite by-products. Overall, these findings may allow development of EPS-specific strategies to promote infant health.

Original language	English
Article number	948
Number of pages	17
Journal	Nutrients
Volume	12
Issue number	4
DOIs	https://doi.org/10.3390/nu12040948
Publication status	Published - 29 Mar 2020

Bibliographical note

Funding Information:
Author Contributions: M.A.E.L. and L.J.H. designed the study. D.P. and M.A.E.L. performed the model colon studies. D.P. performed growth curves, prepared samples for 16S rRNA sequencing, metabolomics, TEM, and graphed figures. J.K. performed the growth curves and prepared samples for RNASeq. A.T. analysed and visualized the RNASeq data. S.C. performed QC and taxonomic profiling of the 16S rRNA amplicon data. M.J.D. analyzed and visualized the 16S rRNA, metabolomics data, and performed the co-occurrence analysis (also with S.C.). I.J.C. performed the NMR metabolomics and identified metabolites. C.B. performed the TEM. D.P., A.T., M.J.D., MAEL and L.J.H. analyzed the data and co-wrote the manuscript along with D.v.S., and T.K. All authors read and approved the final manuscript Funding: This work was part funded by an Erasmus studentship to D.P. M.A.E.L. was funded by the Marie Skłodowska-Curie Individual Fellowship (Project 661594). L.J.H. is funded by a Wellcome Trust Investigator award (100974/C/13/Z) and together with T.K. by a BBSRC ISP grant for Gut Microbes and Health BB/R012490/1 and its constituent project(s), BBS/E/F/000PR10353 and BBS/E/F/000PR10355. T.K. is also funded by the Genomics for Food security CSP grant from the BBSRC (BB/CSP17270/1). A.T. is supported by the BBSRC Norwich Research Park Biosciences Doctoral Training Partnership (grant BB/M011216/1). D.v.S. is supported by Science Foundation Ireland (SFI/12/RC/2273-P1 and SFI/12/RC/2273-P2). The funding bodies did contribute to the design of the study, collection, analysis, and interpretation of data or in writing the manuscript.

Funding Information:
Acknowledgments: We would like to thank the parents for donating their infants’ stool samples for these experiments, the sequencing team at Wellcome Trust Sanger Institute for performing the 16S rRNA and RNA sequencing and Drs Emma Allen-Vercoe and Julie McDonald for their technical support. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster.

Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

16S rRNA profiling
Bifidobacterium
Cross-feeding
Diet
Early life
Exopolysaccharides
Metabolomics
Model colon

ASJC Scopus subject areas

Food Science
Nutrition and Dietetics

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PüngelD2020BifidobacteriumFinal published version, 2.79 MBLicence: Creative Commons: Attribution (CC BY)

Cite this

@article{b797af2f46a84a4881062a9b0fd391ac,

title = "Bifidobacterium breve UCC2003 exopolysaccharide modulates the early life microbiota by acting as a potential dietary substrate",

abstract = "Background: Bifidobacterium represents an important early life microbiota member. Specific bifidobacterial components, exopolysaccharides (EPS), positively modulate host responses, with purified EPS also suggested to impact microbe–microbe interactions by acting as a nutrient substrate. Thus, we determined the longitudinal effects of bifidobacterial EPS on microbial communities and metabolite profiles using an infant model colon system. Methods: Differential gene expression and growth characteristics were determined for each strain; Bifidobacterium breve UCC2003 and corresponding isogenic EPS-deletion mutant (B. breve UCC2003del). Model colon vessels were inoculated with B. breve and microbiome dynamics monitored using 16S rRNA sequencing and metabolomics (NMR). Results: Transcriptomics of EPS mutant vs. B. breve UCC2003 highlighted discrete differential gene expression (e.g., eps biosynthetic cluster), though overall growth dynamics between strains were unaffected. The EPS-positive vessel had significant shifts in microbiome and metabolite profiles until study end (405 h); with increases of Tyzzerella and Faecalibacterium, and short-chain fatty acids, with further correlations between taxa and metabolites which were not observed within the EPS-negative vessel. Conclusions: These data indicate that B. breve UCC2003 EPS is potentially metabolized by infant microbiota members, leading to differential microbial metabolism and altered metabolite by-products. Overall, these findings may allow development of EPS-specific strategies to promote infant health.",

keywords = "16S rRNA profiling, Bifidobacterium, Cross-feeding, Diet, Early life, Exopolysaccharides, Metabolomics, Model colon",

author = "Deborah P{\"u}ngel and Agatha Treveil and Dalby, {Matthew J.} and Shabhonam Caim and Colquhoun, {Ian J} and Catherine Booth and Jennifer Ketskemety and Tamas Korcsmaros and {van Sinderen}, Douwe and Lawson, {Melissa AE} and Hall, {Lindsay J}",

note = "Funding Information: Author Contributions: M.A.E.L. and L.J.H. designed the study. D.P. and M.A.E.L. performed the model colon studies. D.P. performed growth curves, prepared samples for 16S rRNA sequencing, metabolomics, TEM, and graphed figures. J.K. performed the growth curves and prepared samples for RNASeq. A.T. analysed and visualized the RNASeq data. S.C. performed QC and taxonomic profiling of the 16S rRNA amplicon data. M.J.D. analyzed and visualized the 16S rRNA, metabolomics data, and performed the co-occurrence analysis (also with S.C.). I.J.C. performed the NMR metabolomics and identified metabolites. C.B. performed the TEM. D.P., A.T., M.J.D., MAEL and L.J.H. analyzed the data and co-wrote the manuscript along with D.v.S., and T.K. All authors read and approved the final manuscript Funding: This work was part funded by an Erasmus studentship to D.P. M.A.E.L. was funded by the Marie Sk{\l}odowska-Curie Individual Fellowship (Project 661594). L.J.H. is funded by a Wellcome Trust Investigator award (100974/C/13/Z) and together with T.K. by a BBSRC ISP grant for Gut Microbes and Health BB/R012490/1 and its constituent project(s), BBS/E/F/000PR10353 and BBS/E/F/000PR10355. T.K. is also funded by the Genomics for Food security CSP grant from the BBSRC (BB/CSP17270/1). A.T. is supported by the BBSRC Norwich Research Park Biosciences Doctoral Training Partnership (grant BB/M011216/1). D.v.S. is supported by Science Foundation Ireland (SFI/12/RC/2273-P1 and SFI/12/RC/2273-P2). The funding bodies did contribute to the design of the study, collection, analysis, and interpretation of data or in writing the manuscript. Funding Information: Acknowledgments: We would like to thank the parents for donating their infants{\textquoteright} stool samples for these experiments, the sequencing team at Wellcome Trust Sanger Institute for performing the 16S rRNA and RNA sequencing and Drs Emma Allen-Vercoe and Julie McDonald for their technical support. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster. Publisher Copyright: {\textcopyright} 2020 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2020",

month = mar,

day = "29",

doi = "10.3390/nu12040948",

language = "English",

volume = "12",

journal = "Nutrients",

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T1 - Bifidobacterium breve UCC2003 exopolysaccharide modulates the early life microbiota by acting as a potential dietary substrate

AU - Püngel, Deborah

AU - Treveil, Agatha

AU - Dalby, Matthew J.

AU - Caim, Shabhonam

AU - Colquhoun, Ian J

AU - Booth, Catherine

AU - Ketskemety, Jennifer

AU - Korcsmaros, Tamas

AU - van Sinderen, Douwe

AU - Lawson, Melissa AE

AU - Hall, Lindsay J

N1 - Funding Information: Author Contributions: M.A.E.L. and L.J.H. designed the study. D.P. and M.A.E.L. performed the model colon studies. D.P. performed growth curves, prepared samples for 16S rRNA sequencing, metabolomics, TEM, and graphed figures. J.K. performed the growth curves and prepared samples for RNASeq. A.T. analysed and visualized the RNASeq data. S.C. performed QC and taxonomic profiling of the 16S rRNA amplicon data. M.J.D. analyzed and visualized the 16S rRNA, metabolomics data, and performed the co-occurrence analysis (also with S.C.). I.J.C. performed the NMR metabolomics and identified metabolites. C.B. performed the TEM. D.P., A.T., M.J.D., MAEL and L.J.H. analyzed the data and co-wrote the manuscript along with D.v.S., and T.K. All authors read and approved the final manuscript Funding: This work was part funded by an Erasmus studentship to D.P. M.A.E.L. was funded by the Marie Skłodowska-Curie Individual Fellowship (Project 661594). L.J.H. is funded by a Wellcome Trust Investigator award (100974/C/13/Z) and together with T.K. by a BBSRC ISP grant for Gut Microbes and Health BB/R012490/1 and its constituent project(s), BBS/E/F/000PR10353 and BBS/E/F/000PR10355. T.K. is also funded by the Genomics for Food security CSP grant from the BBSRC (BB/CSP17270/1). A.T. is supported by the BBSRC Norwich Research Park Biosciences Doctoral Training Partnership (grant BB/M011216/1). D.v.S. is supported by Science Foundation Ireland (SFI/12/RC/2273-P1 and SFI/12/RC/2273-P2). The funding bodies did contribute to the design of the study, collection, analysis, and interpretation of data or in writing the manuscript. Funding Information: Acknowledgments: We would like to thank the parents for donating their infants’ stool samples for these experiments, the sequencing team at Wellcome Trust Sanger Institute for performing the 16S rRNA and RNA sequencing and Drs Emma Allen-Vercoe and Julie McDonald for their technical support. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster. Publisher Copyright: © 2020 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2020/3/29

Y1 - 2020/3/29

N2 - Background: Bifidobacterium represents an important early life microbiota member. Specific bifidobacterial components, exopolysaccharides (EPS), positively modulate host responses, with purified EPS also suggested to impact microbe–microbe interactions by acting as a nutrient substrate. Thus, we determined the longitudinal effects of bifidobacterial EPS on microbial communities and metabolite profiles using an infant model colon system. Methods: Differential gene expression and growth characteristics were determined for each strain; Bifidobacterium breve UCC2003 and corresponding isogenic EPS-deletion mutant (B. breve UCC2003del). Model colon vessels were inoculated with B. breve and microbiome dynamics monitored using 16S rRNA sequencing and metabolomics (NMR). Results: Transcriptomics of EPS mutant vs. B. breve UCC2003 highlighted discrete differential gene expression (e.g., eps biosynthetic cluster), though overall growth dynamics between strains were unaffected. The EPS-positive vessel had significant shifts in microbiome and metabolite profiles until study end (405 h); with increases of Tyzzerella and Faecalibacterium, and short-chain fatty acids, with further correlations between taxa and metabolites which were not observed within the EPS-negative vessel. Conclusions: These data indicate that B. breve UCC2003 EPS is potentially metabolized by infant microbiota members, leading to differential microbial metabolism and altered metabolite by-products. Overall, these findings may allow development of EPS-specific strategies to promote infant health.

AB - Background: Bifidobacterium represents an important early life microbiota member. Specific bifidobacterial components, exopolysaccharides (EPS), positively modulate host responses, with purified EPS also suggested to impact microbe–microbe interactions by acting as a nutrient substrate. Thus, we determined the longitudinal effects of bifidobacterial EPS on microbial communities and metabolite profiles using an infant model colon system. Methods: Differential gene expression and growth characteristics were determined for each strain; Bifidobacterium breve UCC2003 and corresponding isogenic EPS-deletion mutant (B. breve UCC2003del). Model colon vessels were inoculated with B. breve and microbiome dynamics monitored using 16S rRNA sequencing and metabolomics (NMR). Results: Transcriptomics of EPS mutant vs. B. breve UCC2003 highlighted discrete differential gene expression (e.g., eps biosynthetic cluster), though overall growth dynamics between strains were unaffected. The EPS-positive vessel had significant shifts in microbiome and metabolite profiles until study end (405 h); with increases of Tyzzerella and Faecalibacterium, and short-chain fatty acids, with further correlations between taxa and metabolites which were not observed within the EPS-negative vessel. Conclusions: These data indicate that B. breve UCC2003 EPS is potentially metabolized by infant microbiota members, leading to differential microbial metabolism and altered metabolite by-products. Overall, these findings may allow development of EPS-specific strategies to promote infant health.

KW - 16S rRNA profiling

KW - Bifidobacterium

KW - Cross-feeding

KW - Diet

KW - Early life

KW - Exopolysaccharides

KW - Metabolomics

KW - Model colon

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U2 - 10.3390/nu12040948

DO - 10.3390/nu12040948

M3 - Article

C2 - 32235410

AN - SCOPUS:85082733075

SN - 2072-6643

VL - 12

JO - Nutrients

JF - Nutrients

IS - 4

M1 - 948

ER -

Bifidobacterium breve UCC2003 exopolysaccharide modulates the early life microbiota by acting as a potential dietary substrate

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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