Literature DB >> 35289327

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

Craig S Robb1,2, Joanne K Hobbs1, Benjamin Pluvinage1, Greta Reintjes3,4, Leeann Klassen3, Stephanie Monteith3, Greta Giljan4, Carolyn Amundsen3, Chelsea Vickers1,5, Andrew G Hettle1, Rory Hills1, Xiaohui Xing3, Tony Montina6, Wesley F Zandberg7, D Wade Abbott3, Alisdair B Boraston8.   

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.
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.

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Year:  2022        PMID: 35289327     DOI: 10.1038/s41589-022-00983-y

Source DB:  PubMed          Journal:  Nat Chem Biol        ISSN: 1552-4450            Impact factor:   16.174


  46 in total

Review 1.  A sweet new wave: structures and mechanisms of enzymes that digest polysaccharides from marine algae.

Authors:  Jan-Hendrik Hehemann; Alisdair B Boraston; Mirjam Czjzek
Journal:  Curr Opin Struct Biol       Date:  2014-08-17       Impact factor: 6.809

2.  A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan.

Authors:  Lukas Reisky; Aurélie Préchoux; Marie-Katherin Zühlke; Marcus Bäumgen; Craig S Robb; Nadine Gerlach; Thomas Roret; Christian Stanetty; Robert Larocque; Gurvan Michel; Tao Song; Stephanie Markert; Frank Unfried; Marko D Mihovilovic; Anke Trautwein-Schult; Dörte Becher; Thomas Schweder; Uwe T Bornscheuer; Jan-Hendrik Hehemann
Journal:  Nat Chem Biol       Date:  2019-07-08       Impact factor: 15.040

3.  Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota.

Authors:  Jan-Hendrik Hehemann; Gaëlle Correc; Tristan Barbeyron; William Helbert; Mirjam Czjzek; Gurvan Michel
Journal:  Nature       Date:  2010-04-08       Impact factor: 49.962

4.  Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism.

Authors:  Fiona Cuskin; Elisabeth C Lowe; Max J Temple; Yanping Zhu; Elizabeth Cameron; Nicholas A Pudlo; Nathan T Porter; Karthik Urs; Andrew J Thompson; Alan Cartmell; Artur Rogowski; Brian S Hamilton; Rui Chen; Thomas J Tolbert; Kathleen Piens; Debby Bracke; Wouter Vervecken; Zalihe Hakki; Gaetano Speciale; Jose L Munōz-Munōz; Andrew Day; Maria J Peña; Richard McLean; Michael D Suits; Alisdair B Boraston; Todd Atherly; Cherie J Ziemer; Spencer J Williams; Gideon J Davies; D Wade Abbott; Eric C Martens; Harry J Gilbert
Journal:  Nature       Date:  2015-01-08       Impact factor: 49.962

5.  Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria.

Authors:  Elizabeth Ficko-Blean; Aurélie Préchoux; François Thomas; Tatiana Rochat; Robert Larocque; Yongtao Zhu; Mark Stam; Sabine Génicot; Murielle Jam; Alexandra Calteau; Benjamin Viart; David Ropartz; David Pérez-Pascual; Gaëlle Correc; Maria Matard-Mann; Keith A Stubbs; Hélène Rogniaux; Alexandra Jeudy; Tristan Barbeyron; Claudine Médigue; Mirjam Czjzek; David Vallenet; Mark J McBride; Eric Duchaud; Gurvan Michel
Journal:  Nat Commun       Date:  2017-11-22       Impact factor: 14.919

Review 6.  Algae as nutritional and functional food sources: revisiting our understanding.

Authors:  Mark L Wells; Philippe Potin; James S Craigie; John A Raven; Sabeeha S Merchant; Katherine E Helliwell; Alison G Smith; Mary Ellen Camire; Susan H Brawley
Journal:  J Appl Phycol       Date:  2016-11-21       Impact factor: 3.215

7.  Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont.

Authors:  Benjamin Pluvinage; Julie M Grondin; Carolyn Amundsen; Leeann Klassen; Paul E Moote; Yao Xiao; Dallas Thomas; Nicholas A Pudlo; Anuoluwapo Anele; Eric C Martens; G Douglas Inglis; Richard E R Uwiera; Alisdair B Boraston; D Wade Abbott
Journal:  Nat Commun       Date:  2018-03-13       Impact factor: 14.919

8.  Ancient acquisition of "alginate utilization loci" by human gut microbiota.

Authors:  Sophie Mathieu; Mélanie Touvrey-Loiodice; Laurent Poulet; Sophie Drouillard; Renaud Vincentelli; Bernard Henrissat; Gudmund Skjåk-Bræk; William Helbert
Journal:  Sci Rep       Date:  2018-05-23       Impact factor: 4.379

9.  Complex pectin metabolism by gut bacteria reveals novel catalytic functions.

Authors:  Didier Ndeh; Artur Rogowski; Alan Cartmell; Ana S Luis; Arnaud Baslé; Joseph Gray; Immacolata Venditto; Jonathon Briggs; Xiaoyang Zhang; Aurore Labourel; Nicolas Terrapon; Fanny Buffetto; Sergey Nepogodiev; Yao Xiao; Robert A Field; Yanping Zhu; Malcolm A O'Neil; Breeana R Urbanowicz; William S York; Gideon J Davies; D Wade Abbott; Marie-Christine Ralet; Eric C Martens; Bernard Henrissat; Harry J Gilbert
Journal:  Nature       Date:  2017-03-22       Impact factor: 69.504

10.  Insights into the κ/ι-carrageenan metabolism pathway of some marine Pseudoalteromonas species.

Authors:  Andrew G Hettle; Joanne K Hobbs; Benjamin Pluvinage; Chelsea Vickers; Kento T Abe; Orly Salama-Alber; Bailey E McGuire; Jan-Hendrik Hehemann; Joseph P M Hui; Fabrice Berrue; Arjun Banskota; Junzeng Zhang; Eric M Bottos; Jonathan Van Hamme; Alisdair B Boraston
Journal:  Commun Biol       Date:  2019-12-19
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  2 in total

1.  Sulfated glycan recognition by carbohydrate sulfatases of the human gut microbiota.

Authors:  Ana S Luis; Arnaud Baslé; Dominic P Byrne; Gareth S A Wright; James A London; Chunsheng Jin; Niclas G Karlsson; Gunnar C Hansson; Patrick A Eyers; Mirjam Czjzek; Tristan Barbeyron; Edwin A Yates; Eric C Martens; Alan Cartmell
Journal:  Nat Chem Biol       Date:  2022-06-16       Impact factor: 16.174

Review 2.  Sulfatases: Critical Enzymes for Algal Polysaccharide Processing.

Authors:  Andrew G Hettle; Chelsea J Vickers; Alisdair B Boraston
Journal:  Front Plant Sci       Date:  2022-04-28       Impact factor: 6.627

  2 in total

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