Metabolism of a hybrid algal galactan by members of the human gut microbiome

Craig S Robb; Joanne K Hobbs; Benjamin Pluvinage; Greta Reintjes; Leeann Klassen; Stephanie Monteith; Greta Giljan; Carolyn Amundsen; Chelsea Vickers; Andrew G Hettle; Rory Hills; null Nitin; Xiaohui Xing; Tony Montina; Wesley F Zandberg; D Wade Abbott; Alisdair Boraston

doi:10.1038/s41589-022-00983-y

Metabolism of a hybrid algal galactan by members of the human gut microbiome

Craig S Robb, Joanne K Hobbs, Benjamin Pluvinage, Greta Reintjes, Leeann Klassen, Stephanie Monteith, Greta Giljan, Carolyn Amundsen, Chelsea Vickers, Andrew G Hettle, Rory Hills, Nitin, Xiaohui Xing, Tony Montina, Wesley F Zandberg, D Wade Abbott, Alisdair Boraston^*

^*Corresponding author for this work

School of Biology

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

Abstract

Native porphyran is a hybrid of porphryan and agarose. As a common element of edible seaweed, this algal galactan is a frequent component of the human diet. Bacterial members of the human gut microbiota have acquired polysaccharide utilization loci (PULs) that enable the metabolism of porphyran or agarose. However, the molecular mechanisms that underlie the deconstruction and use of native porphyran remains incompletely defined. Here, we have studied two human gut bacteria, porphyranolytic Bacteroides plebeius and agarolytic Bacteroides uniformis, that target native porphyran. This reveals an exo-based cycle of porphyran depolymerization that incorporates a keystone sulfatase. In both PULs this cycle also works together with a PUL-encoded agarose depolymerizing machinery to synergistically reduce native porphyran to monosaccharides. This provides a framework for understanding the deconstruction of a hybrid algal galactan, and insight into the competitive and/or syntrophic relationship of gut microbiota members that target rare nutrients.

Original language	English
Pages (from-to)	501-510
Number of pages	10
Journal	Nature Chemical Biology
Volume	18
Issue number	5
Early online date	14 Mar 2022
DOIs	https://doi.org/10.1038/s41589-022-00983-y
Publication status	Published - 1 May 2022

Keywords

Bacteria/metabolism
Galactans
Gastrointestinal Microbiome
Humans
Polysaccharides/metabolism
Sepharose

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10.1038/s41589-022-00983-y

Structure of the Exo-L-galactose-6-sulfatase BuS1_11 from Bacteroides uniformis
Hobbs , J. (Creator), Protein Data Bank (PDB), 2022
DOI: 10.2210/pdb7lha/pdb, http://dx.doi.org/10.2210/pdb7lj2/pdb and 7 more links, http://dx.doi.org/10.2210/pdb7ljj/pdb, http://dx.doi.org/10.2210/pdb7lk7/pdb, http://dx.doi.org/10.2210/pdb7lnp/pdb, http://dx.doi.org/10.2210/pdb5t98/pdb, http://dx.doi.org/10.2210/pdb5t99/pdb, http://dx.doi.org/10.2210/pdb7lh6/pdb, http://dx.doi.org/10.2210/pdb7lha/pdb (show fewer)
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Robb, C. S., Hobbs, J. K., Pluvinage, B., Reintjes, G., Klassen, L., Monteith, S., Giljan, G., Amundsen, C., Vickers, C., Hettle, A. G., Hills, R., Nitin, Xing, X., Montina, T., Zandberg, W. F., Abbott, D. W., & Boraston, A. (2022). Metabolism of a hybrid algal galactan by members of the human gut microbiome. Nature Chemical Biology, 18(5), 501-510. https://doi.org/10.1038/s41589-022-00983-y

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title = "Metabolism of a hybrid algal galactan by members of the human gut microbiome",

abstract = "Native porphyran is a hybrid of porphryan and agarose. As a common element of edible seaweed, this algal galactan is a frequent component of the human diet. Bacterial members of the human gut microbiota have acquired polysaccharide utilization loci (PULs) that enable the metabolism of porphyran or agarose. However, the molecular mechanisms that underlie the deconstruction and use of native porphyran remains incompletely defined. Here, we have studied two human gut bacteria, porphyranolytic Bacteroides plebeius and agarolytic Bacteroides uniformis, that target native porphyran. This reveals an exo-based cycle of porphyran depolymerization that incorporates a keystone sulfatase. In both PULs this cycle also works together with a PUL-encoded agarose depolymerizing machinery to synergistically reduce native porphyran to monosaccharides. This provides a framework for understanding the deconstruction of a hybrid algal galactan, and insight into the competitive and/or syntrophic relationship of gut microbiota members that target rare nutrients.",

keywords = "Bacteria/metabolism, Galactans, Gastrointestinal Microbiome, Humans, Polysaccharides/metabolism, Sepharose",

author = "Robb, {Craig S} and Hobbs, {Joanne K} and Benjamin Pluvinage and Greta Reintjes and Leeann Klassen and Stephanie Monteith and Greta Giljan and Carolyn Amundsen and Chelsea Vickers and Hettle, {Andrew G} and Rory Hills and Nitin and Xiaohui Xing and Tony Montina and Zandberg, {Wesley F} and Abbott, {D Wade} and Alisdair Boraston",

note = "Funding: This research was supported by Natural Sciences and Engineering Research Council of Canada Discovery Grants (nos. FRN 04355 to A.B.B. and FRN 03929 to W.F.Z.), funding from Agriculture and Agri-Food Canada (project grant no. J-002262 to D.W.A.) and Beef and Cattle Research Council (grant no. FOS.04.17 / J-001973 to D.W.A.). G.R. was supported by funding from the European Union{\textquoteright}s Horizons 2020 research and innovations program under the Marie Sk{\l}odowska-Curie grant agreement no. 840804.",

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month = may,

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doi = "10.1038/s41589-022-00983-y",

language = "English",

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Robb, CS, Hobbs, JK, Pluvinage, B, Reintjes, G, Klassen, L, Monteith, S, Giljan, G, Amundsen, C, Vickers, C, Hettle, AG, Hills, R, Nitin, Xing, X, Montina, T, Zandberg, WF, Abbott, DW & Boraston, A 2022, 'Metabolism of a hybrid algal galactan by members of the human gut microbiome', Nature Chemical Biology, vol. 18, no. 5, pp. 501-510. https://doi.org/10.1038/s41589-022-00983-y

TY - JOUR

T1 - Metabolism of a hybrid algal galactan by members of the human gut microbiome

AU - Robb, Craig S

AU - Hobbs, Joanne K

AU - Pluvinage, Benjamin

AU - Reintjes, Greta

AU - Klassen, Leeann

AU - Monteith, Stephanie

AU - Giljan, Greta

AU - Amundsen, Carolyn

AU - Vickers, Chelsea

AU - Hettle, Andrew G

AU - Hills, Rory

AU - Nitin, null

AU - Xing, Xiaohui

AU - Montina, Tony

AU - Zandberg, Wesley F

AU - Abbott, D Wade

AU - Boraston, Alisdair

N1 - Funding: This research was supported by Natural Sciences and Engineering Research Council of Canada Discovery Grants (nos. FRN 04355 to A.B.B. and FRN 03929 to W.F.Z.), funding from Agriculture and Agri-Food Canada (project grant no. J-002262 to D.W.A.) and Beef and Cattle Research Council (grant no. FOS.04.17 / J-001973 to D.W.A.). G.R. was supported by funding from the European Union’s Horizons 2020 research and innovations program under the Marie Skłodowska-Curie grant agreement no. 840804.

PY - 2022/5/1

Y1 - 2022/5/1

N2 - Native porphyran is a hybrid of porphryan and agarose. As a common element of edible seaweed, this algal galactan is a frequent component of the human diet. Bacterial members of the human gut microbiota have acquired polysaccharide utilization loci (PULs) that enable the metabolism of porphyran or agarose. However, the molecular mechanisms that underlie the deconstruction and use of native porphyran remains incompletely defined. Here, we have studied two human gut bacteria, porphyranolytic Bacteroides plebeius and agarolytic Bacteroides uniformis, that target native porphyran. This reveals an exo-based cycle of porphyran depolymerization that incorporates a keystone sulfatase. In both PULs this cycle also works together with a PUL-encoded agarose depolymerizing machinery to synergistically reduce native porphyran to monosaccharides. This provides a framework for understanding the deconstruction of a hybrid algal galactan, and insight into the competitive and/or syntrophic relationship of gut microbiota members that target rare nutrients.

AB - Native porphyran is a hybrid of porphryan and agarose. As a common element of edible seaweed, this algal galactan is a frequent component of the human diet. Bacterial members of the human gut microbiota have acquired polysaccharide utilization loci (PULs) that enable the metabolism of porphyran or agarose. However, the molecular mechanisms that underlie the deconstruction and use of native porphyran remains incompletely defined. Here, we have studied two human gut bacteria, porphyranolytic Bacteroides plebeius and agarolytic Bacteroides uniformis, that target native porphyran. This reveals an exo-based cycle of porphyran depolymerization that incorporates a keystone sulfatase. In both PULs this cycle also works together with a PUL-encoded agarose depolymerizing machinery to synergistically reduce native porphyran to monosaccharides. This provides a framework for understanding the deconstruction of a hybrid algal galactan, and insight into the competitive and/or syntrophic relationship of gut microbiota members that target rare nutrients.

KW - Bacteria/metabolism

KW - Galactans

KW - Gastrointestinal Microbiome

KW - Humans

KW - Polysaccharides/metabolism

KW - Sepharose

U2 - 10.1038/s41589-022-00983-y

DO - 10.1038/s41589-022-00983-y

M3 - Article

C2 - 35289327

SN - 1552-4450

VL - 18

SP - 501

EP - 510

JO - Nature Chemical Biology

JF - Nature Chemical Biology

IS - 5

ER -

Metabolism of a hybrid algal galactan by members of the human gut microbiome

Abstract

Keywords

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Datasets

Structure of the Exo-L-galactose-6-sulfatase BuS1_11 from Bacteroides uniformis

Cite this