Dietary trehalose enhances virulence of epidemic Clostridium difficile
Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what has driven this emergence. Here we show that two epidemic ribotypes (RT027 and RT078) have acquired unique mechanisms to metabolize low conce...
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Published in | Nature (London) Vol. 553; no. 7688; pp. 291 - 294 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
18.01.2018
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Abstract | Clostridium difficile
disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what has driven this emergence. Here we show that two epidemic ribotypes (RT027 and RT078) have acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose. RT027 strains contain a single point mutation in the trehalose repressor that increases the sensitivity of this ribotype to trehalose by more than 500-fold. Furthermore, dietary trehalose increases the virulence of a RT027 strain in a mouse model of infection. RT078 strains acquired a cluster of four genes involved in trehalose metabolism, including a PTS permease that is both necessary and sufficient for growth on low concentrations of trehalose. We propose that the implementation of trehalose as a food additive into the human diet, shortly before the emergence of these two epidemic lineages, helped select for their emergence and contributed to hypervirulence.
Two hypervirulent ribotypes of the enteric pathogen
Clostridium difficile
, RT027 and RT078, have independently acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose, suggesting a correlation between the emergence of these ribotypes and the widespread adoption of trehalose in the human diet.
The rise of an intestinal epidemic
Clostridium difficile
is an intestinal pathogen and a major cause of antibiotic-associated diarrhoea. In epidemics in recent years, hypervirulent ribotypes that cause severe disease have emerged, but the factors that contribute to their emergence are unclear. In this study, Robert Britton and colleagues show that two phylogenetically distinct hypervirulent ribotypes, RT027 and RT078, have independently acquired mechanisms to metabolize low concentrations of the disaccharide trehalose. The team also show that this ability to metabolize trehalose correlates with disease severity in a humanized mouse model. These data suggest a correlation between the emergence of these ribotypes and the widespread adoption and use of trehalose as a sugar additive in the human diet. |
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AbstractList | Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what has driven this emergence. Here we show that two epidemic ribotypes (RT027 and RT078) have acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose. RT027 strains contain a single point mutation in the trehalose repressor that increases the sensitivity of this ribotype to trehalose by more than 500-fold. Furthermore, dietary trehalose increases the virulence of a RT027 strain in a mouse model of infection. RT078 strains acquired a cluster of four genes involved in trehalose metabolism, including a PTS permease that is both necessary and sufficient for growth on low concentrations of trehalose. We propose that the implementation of trehalose as a food additive into the human diet, shortly before the emergence of these two epidemic lineages, helped select for their emergence and contributed to hypervirulence. Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what has driven this emergence. Here we show that two epidemic ribotypes (RT027 and RT078) have acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose. RT027 strains contain a single point mutation in the trehalose repressor that increases the sensitivity of this ribotype to trehalose by more than 500-fold. Furthermore, dietary trehalose increases the virulence of a RT027 strain in a mouse model of infection. RT078 strains acquired a cluster of four genes involved in trehalose metabolism, including a PTS permease that is both necessary and sufficient for growth on low concentrations of trehalose. We propose that the implementation of trehalose as a food additive into the human diet, shortly before the emergence of these two epidemic lineages, helped select for their emergence and contributed to hypervirulence. Two hypervirulent ribotypes of the enteric pathogen Clostridium difficile , RT027 and RT078, have independently acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose, suggesting a correlation between the emergence of these ribotypes and the widespread adoption of trehalose in the human diet. The rise of an intestinal epidemic Clostridium difficile is an intestinal pathogen and a major cause of antibiotic-associated diarrhoea. In epidemics in recent years, hypervirulent ribotypes that cause severe disease have emerged, but the factors that contribute to their emergence are unclear. In this study, Robert Britton and colleagues show that two phylogenetically distinct hypervirulent ribotypes, RT027 and RT078, have independently acquired mechanisms to metabolize low concentrations of the disaccharide trehalose. The team also show that this ability to metabolize trehalose correlates with disease severity in a humanized mouse model. These data suggest a correlation between the emergence of these ribotypes and the widespread adoption and use of trehalose as a sugar additive in the human diet. Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what has driven this emergence. Here we show two epidemic ribotypes (RT027 and RT078) have acquired unique mechanisms to metabolize low concentrations of the disaccharide trehalose. RT027 strains contain a single point mutation in the trehalose repressor that increases this ribotype’s sensitivity to trehalose by >500 fold. Furthermore, dietary trehalose increases virulence of a RT027 strain in a mouse model of infection. RT078 strains acquired a cluster of four genes involved in trehalose metabolism, including a PTS permease that is both necessary and sufficient for growth on low concentrations of trehalose. We propose that the implementation of trehalose as a food additive into the human diet, shortly before the emergence of these two epidemic lineages, helped select for their emergence and contributed to hypervirulence. |
Audience | Academic |
Author | Collins, J. Auchtung, J. M. Britton, R. A. Danhof, H. Knetsch, C. W. Robinson, C. van Leeuwen, H. C. Lawley, T. D. |
AuthorAffiliation | 1 Baylor College of Medicine, Department of Molecular Virology and Microbiology 3 Leiden University Medical Centre, Department of Medical Microbiology, The Netherlands 2 University of Oregon, Institute for Molecular Biology 4 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, United Kingdom |
AuthorAffiliation_xml | – name: 4 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, United Kingdom – name: 1 Baylor College of Medicine, Department of Molecular Virology and Microbiology – name: 3 Leiden University Medical Centre, Department of Medical Microbiology, The Netherlands – name: 2 University of Oregon, Institute for Molecular Biology |
Author_xml | – sequence: 1 givenname: J. surname: Collins fullname: Collins, J. organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza – sequence: 2 givenname: C. surname: Robinson fullname: Robinson, C. organization: University of Oregon, Institute for Molecular Biology – sequence: 3 givenname: H. surname: Danhof fullname: Danhof, H. organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza – sequence: 4 givenname: C. W. surname: Knetsch fullname: Knetsch, C. W. organization: Department of Medical Microbiology, Leiden University Medical Centre – sequence: 5 givenname: H. C. surname: van Leeuwen fullname: van Leeuwen, H. C. organization: Department of Medical Microbiology, Leiden University Medical Centre – sequence: 6 givenname: T. D. surname: Lawley fullname: Lawley, T. D. organization: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus – sequence: 7 givenname: J. M. surname: Auchtung fullname: Auchtung, J. M. organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza – sequence: 8 givenname: R. A. surname: Britton fullname: Britton, R. A. email: robert.britton@bcm.edu organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, One Baylor Plaza |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29310122$$D View this record in MEDLINE/PubMed |
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References | de Kok (CR26) 2014; 3 Walker (CR8) 2013; 56 Goorhuis (CR5) 2008; 47 Kumar, Stecher, Tamura (CR32) 2016; 33 He (CR1) 2013; 45 Knetsch (CR22) 2011; 157 Holm (CR30) 1979; 6 Gupta, Khanna (CR6) 2014; 7 Dingle, Mulvey, Armstrong (CR35) 2011; 79 Theriot (CR21) 2014; 5 Griffiths (CR31) 2010; 48 Leffler, Lamont (CR20) 2015; 372 Fagan, Fairweather (CR25) 2011; 286 He (CR9) 2010; 107 Smith, Markowitz, Macrina (CR37) 1981; 19 Robinson, Auchtung, Collins, Britton (CR10) 2014; 82 Polivkova, Krutova, Petrlova, Benes, Nyc (CR13) 2016; 40 Bergoz, Bolte, Meyer zum Bueschenfelde (CR16) 1973; 8 Stabler (CR19) 2009; 10 Rupnik (CR14) 2016; 42 Bergoz (CR15) 1971; 60 CR29 Spigaglia (CR2) 2008; 57 Eyre (CR12) 2015; 20 Pfaffl, Dorak (CR27) 2006 Spigaglia, Barbanti, Dionisi, Mastrantonio (CR3) 2010; 48 Higashiyama (CR18) 2002; 74 Collins, Auchtung, Schaefer, Eaton, Britton (CR28) 2015; 3 Popoff, Rubin, Gill, Boquet (CR36) 1988; 56 Bouillaut, Self, Sonenshein (CR23) 2013; 195 Jhung (CR4) 2008; 14 Sievers (CR33) 2011; 7 Roca, Abajian, Vigerust (CR34) 2013; 2 Limbago (CR7) 2009; 47 Oku, Nakamura (CR17) 2000; 54 Lim (CR11) 2014; 58 Ng (CR24) 2013; 8 29345660 - Nature. 2018 Jan 18;553(7688):285-286 29447694 - Cell Host Microbe. 2018 Feb 14;23 (2):156-158 AS Walker (BFnature25178_CR8) 2013; 56 DW Eyre (BFnature25178_CR12) 2015; 20 D Griffiths (BFnature25178_CR31) 2010; 48 TC Dingle (BFnature25178_CR35) 2011; 79 SDe de Kok (BFnature25178_CR26) 2014; 3 S Holm (BFnature25178_CR30) 1979; 6 P Spigaglia (BFnature25178_CR2) 2008; 57 R Bergoz (BFnature25178_CR15) 1971; 60 P Spigaglia (BFnature25178_CR3) 2010; 48 T Oku (BFnature25178_CR17) 2000; 54 S Polivkova (BFnature25178_CR13) 2016; 40 CD Robinson (BFnature25178_CR10) 2014; 82 CM Theriot (BFnature25178_CR21) 2014; 5 J Collins (BFnature25178_CR28) 2015; 3 M He (BFnature25178_CR1) 2013; 45 RP Fagan (BFnature25178_CR25) 2011; 286 CW Knetsch (BFnature25178_CR22) 2011; 157 MR Popoff (BFnature25178_CR36) 1988; 56 F Sievers (BFnature25178_CR33) 2011; 7 RA Stabler (BFnature25178_CR19) 2009; 10 T Higashiyama (BFnature25178_CR18) 2002; 74 A Gupta (BFnature25178_CR6) 2014; 7 M Rupnik (BFnature25178_CR14) 2016; 42 SK Lim (BFnature25178_CR11) 2014; 58 S Kumar (BFnature25178_CR32) 2016; 33 BFnature25178_CR29 A Goorhuis (BFnature25178_CR5) 2008; 47 L Bouillaut (BFnature25178_CR23) 2013; 195 M He (BFnature25178_CR9) 2010; 107 CJ Smith (BFnature25178_CR37) 1981; 19 AI Roca (BFnature25178_CR34) 2013; 2 MA Jhung (BFnature25178_CR4) 2008; 14 DA Leffler (BFnature25178_CR20) 2015; 372 BM Limbago (BFnature25178_CR7) 2009; 47 MW Pfaffl (BFnature25178_CR27) 2006 YK Ng (BFnature25178_CR24) 2013; 8 R Bergoz (BFnature25178_CR16) 1973; 8 |
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Snippet | Clostridium difficile
disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what... Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what... Clostridium difficile disease has recently increased to become a dominant nosocomial pathogen in North America and Europe, although little is known about what... |
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SubjectTerms | 38/44 38/70 45/70 631/326/107 631/326/2565/855 631/326/325/1506 631/326/421 64 64/60 Analysis Animals Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Clostridioides difficile - drug effects Clostridioides difficile - genetics Clostridioides difficile - metabolism Clostridioides difficile - pathogenicity Clostridium Clostridium difficile Clostridium Infections - epidemiology Clostridium Infections - microbiology Dietary Sugars - administration & dosage Dietary Sugars - metabolism Dietary Sugars - pharmacology Emergence Epidemics Female Food additives Gastrointestinal Microbiome Gene mutation Genetic aspects Genomes Health aspects Humanities and Social Sciences Humans Male Metabolism Mice Mice, Inbred C57BL Microbiota multidisciplinary Multigene Family Mutation Nosocomial infection Permease Phosphoenolpyruvate Sugar Phosphotransferase System - genetics Phosphoenolpyruvate Sugar Phosphotransferase System - metabolism Physiological aspects Point Mutation Repressor Proteins - genetics Repressor Proteins - metabolism Ribotyping Science Trehalose Trehalose - administration & dosage Trehalose - metabolism Trehalose - pharmacology Virulence Virulence (Microbiology) Virulence - drug effects |
Title | Dietary trehalose enhances virulence of epidemic Clostridium difficile |
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