Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease

Crohn’s disease (CD) results from a complex interplay between host genetic factors and endogenous microbial communities. In the current study, we used Ion Torrent sequencing to characterize the gut bacterial microbiota (bacteriome) and fungal community (mycobiome) in patients with CD and their nondi...

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Main Authors: G. Hoarau, P. K. Mukherjee, C. Gower-Rousseau, C. Hager, J. Chandra, M. A. Retuerto, C. Neut, S. Vermeire, J. Clemente, J. F. Colombel, H. Fujioka, D. Poulain, B. Sendid, M. A. Ghannoum
Format: Article
Language:English
Published: American Society for Microbiology 2016-09-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/7/5/e01250-16
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spelling doaj-475842e273674ada846de9d0690fb7d62021-07-02T03:35:24ZengAmerican Society for MicrobiologymBio2150-75112016-09-0175e01250-1610.1128/mBio.01250-16Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s DiseaseG. HoarauP. K. MukherjeeC. Gower-RousseauC. HagerJ. ChandraM. A. RetuertoC. NeutS. VermeireJ. ClementeJ. F. ColombelH. FujiokaD. PoulainB. SendidM. A. GhannoumCrohn’s disease (CD) results from a complex interplay between host genetic factors and endogenous microbial communities. In the current study, we used Ion Torrent sequencing to characterize the gut bacterial microbiota (bacteriome) and fungal community (mycobiome) in patients with CD and their nondiseased first-degree relatives (NCDR) in 9 familial clusters living in northern France-Belgium and in healthy individuals from 4 families living in the same area (non-CD unrelated [NCDU]). Principal component, diversity, and abundance analyses were conducted, and CD-associated inter- and intrakingdom microbial correlations were determined. Significant microbial interactions were identified and validated using single- and mixed-species biofilms. CD and NCDR groups clustered together in the mycobiome but not in the bacteriome. Microbiotas of familial (CD and NCDR) samples were distinct from those of nonfamilial (NCDU) samples. The abundance of Serratia marcescens and Escherichia coli was elevated in CD patients, while that of beneficial bacteria was decreased. The abundance of the fungus Candida tropicalis was significantly higher in CD than in NCDR (P = 0.003) samples and positively correlated with levels of anti-Saccharomyces cerevisiae antibodies (ASCA). The abundance of C. tropicalis was positively correlated with S. marcescens and E. coli, suggesting that these organisms interact in the gut. The mass and thickness of triple-species (C. tropicalis plus S. marcescens plus E. coli) biofilm were significantly greater than those of single- and double-species biofilms. C. tropicalis biofilms comprised blastospores, while double- and triple-species biofilms were enriched in hyphae. S. marcescens used fimbriae to coaggregate or attach with C. tropicalis/E. coli, while E. coli was closely apposed with C. tropicalis. Specific interkingdom microbial interactions may be key determinants in CD.http://mbio.asm.org/cgi/content/full/7/5/e01250-16
collection DOAJ
language English
format Article
sources DOAJ
author G. Hoarau
P. K. Mukherjee
C. Gower-Rousseau
C. Hager
J. Chandra
M. A. Retuerto
C. Neut
S. Vermeire
J. Clemente
J. F. Colombel
H. Fujioka
D. Poulain
B. Sendid
M. A. Ghannoum
spellingShingle G. Hoarau
P. K. Mukherjee
C. Gower-Rousseau
C. Hager
J. Chandra
M. A. Retuerto
C. Neut
S. Vermeire
J. Clemente
J. F. Colombel
H. Fujioka
D. Poulain
B. Sendid
M. A. Ghannoum
Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
mBio
author_facet G. Hoarau
P. K. Mukherjee
C. Gower-Rousseau
C. Hager
J. Chandra
M. A. Retuerto
C. Neut
S. Vermeire
J. Clemente
J. F. Colombel
H. Fujioka
D. Poulain
B. Sendid
M. A. Ghannoum
author_sort G. Hoarau
title Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
title_short Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
title_full Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
title_fullStr Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
title_full_unstemmed Bacteriome and Mycobiome Interactions Underscore Microbial Dysbiosis in Familial Crohn’s Disease
title_sort bacteriome and mycobiome interactions underscore microbial dysbiosis in familial crohn’s disease
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2016-09-01
description Crohn’s disease (CD) results from a complex interplay between host genetic factors and endogenous microbial communities. In the current study, we used Ion Torrent sequencing to characterize the gut bacterial microbiota (bacteriome) and fungal community (mycobiome) in patients with CD and their nondiseased first-degree relatives (NCDR) in 9 familial clusters living in northern France-Belgium and in healthy individuals from 4 families living in the same area (non-CD unrelated [NCDU]). Principal component, diversity, and abundance analyses were conducted, and CD-associated inter- and intrakingdom microbial correlations were determined. Significant microbial interactions were identified and validated using single- and mixed-species biofilms. CD and NCDR groups clustered together in the mycobiome but not in the bacteriome. Microbiotas of familial (CD and NCDR) samples were distinct from those of nonfamilial (NCDU) samples. The abundance of Serratia marcescens and Escherichia coli was elevated in CD patients, while that of beneficial bacteria was decreased. The abundance of the fungus Candida tropicalis was significantly higher in CD than in NCDR (P = 0.003) samples and positively correlated with levels of anti-Saccharomyces cerevisiae antibodies (ASCA). The abundance of C. tropicalis was positively correlated with S. marcescens and E. coli, suggesting that these organisms interact in the gut. The mass and thickness of triple-species (C. tropicalis plus S. marcescens plus E. coli) biofilm were significantly greater than those of single- and double-species biofilms. C. tropicalis biofilms comprised blastospores, while double- and triple-species biofilms were enriched in hyphae. S. marcescens used fimbriae to coaggregate or attach with C. tropicalis/E. coli, while E. coli was closely apposed with C. tropicalis. Specific interkingdom microbial interactions may be key determinants in CD.
url http://mbio.asm.org/cgi/content/full/7/5/e01250-16
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