Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria

Jenny Angelica Laverde Gomez, Indrani Mukhopadhya (Corresponding Author), Sylvia H. Duncan, Petra Louis, Sophie Shaw, Elaina Collie-Duguid, Emmanuelle Crost, Nathalie Juge, Harry J. Flint

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Abstract

Interspecies cross‐feeding is a fundamental factor in anaerobic microbial communities. In the human colon formate is produced by many bacterial species but is normally detected only at low concentrations. Ruminococcus bromii produces formate, ethanol and acetate in approximately equal molar proportions in pure culture on RUM‐RS medium with 0.2% Novelose resistant starch (RS3) as energy source. Batch co‐culturing on starch with the acetogen Blautia hydrogenotrophica however led to the disappearance of formate and increased levels of acetate, which is proposed to occur through the routing of formate via the Wood Ljungdahl pathway of B. hydrogenotrophica. We investigated these inter‐species interactions further using RNAseq to examine gene expression in continuous co‐cultures of R. bromii and B. hydrogenotrophica. Transcriptome analysis revealed upregulation of B. hydrogenotrophica genes involved in the Wood‐Ljungdahl pathway and of a 10 gene cluster responsible for increased branched chain amino acid fermentation in the co‐cultures. Cross‐feeding between formate‐producing species and acetogens may be a significant factor in short chain fatty acid formation in the colon contributing to high rates of acetate production. Transcriptome analysis also indicated competition for the vitamin thiamine and down‐regulation of dissimilatory sulfate reduction and key redox proteins in R. bromii in the co‐cultures, thus demonstrating the wide‐ranging consequences of inter‐species interactions in this model system.
Original languageEnglish
Pages (from-to)259-271
Number of pages13
JournalEnvironmental Microbiology
Volume21
Issue number1
Early online date22 Nov 2018
DOIs
Publication statusPublished - Jan 2019

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formic acid
Ruminococcus bromii
formates
coculture
Coculture Techniques
transcriptomics
cooperatives
acetate
Bacteria
starch
Acetates
bacterium
bacteria
acetates
Gene Expression Profiling
Starch
colon
Colon
gene
Ruminococcus

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title = "Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria",
abstract = "Interspecies cross‐feeding is a fundamental factor in anaerobic microbial communities. In the human colon formate is produced by many bacterial species but is normally detected only at low concentrations. Ruminococcus bromii produces formate, ethanol and acetate in approximately equal molar proportions in pure culture on RUM‐RS medium with 0.2{\%} Novelose resistant starch (RS3) as energy source. Batch co‐culturing on starch with the acetogen Blautia hydrogenotrophica however led to the disappearance of formate and increased levels of acetate, which is proposed to occur through the routing of formate via the Wood Ljungdahl pathway of B. hydrogenotrophica. We investigated these inter‐species interactions further using RNAseq to examine gene expression in continuous co‐cultures of R. bromii and B. hydrogenotrophica. Transcriptome analysis revealed upregulation of B. hydrogenotrophica genes involved in the Wood‐Ljungdahl pathway and of a 10 gene cluster responsible for increased branched chain amino acid fermentation in the co‐cultures. Cross‐feeding between formate‐producing species and acetogens may be a significant factor in short chain fatty acid formation in the colon contributing to high rates of acetate production. Transcriptome analysis also indicated competition for the vitamin thiamine and down‐regulation of dissimilatory sulfate reduction and key redox proteins in R. bromii in the co‐cultures, thus demonstrating the wide‐ranging consequences of inter‐species interactions in this model system.",
author = "{Laverde Gomez}, {Jenny Angelica} and Indrani Mukhopadhya and Duncan, {Sylvia H.} and Petra Louis and Sophie Shaw and Elaina Collie-Duguid and Emmanuelle Crost and Nathalie Juge and Flint, {Harry J.}",
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T1 - Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria

AU - Laverde Gomez, Jenny Angelica

AU - Mukhopadhya, Indrani

AU - Duncan, Sylvia H.

AU - Louis, Petra

AU - Shaw, Sophie

AU - Collie-Duguid, Elaina

AU - Crost, Emmanuelle

AU - Juge, Nathalie

AU - Flint, Harry J.

N1 - © 2018 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

PY - 2019/1

Y1 - 2019/1

N2 - Interspecies cross‐feeding is a fundamental factor in anaerobic microbial communities. In the human colon formate is produced by many bacterial species but is normally detected only at low concentrations. Ruminococcus bromii produces formate, ethanol and acetate in approximately equal molar proportions in pure culture on RUM‐RS medium with 0.2% Novelose resistant starch (RS3) as energy source. Batch co‐culturing on starch with the acetogen Blautia hydrogenotrophica however led to the disappearance of formate and increased levels of acetate, which is proposed to occur through the routing of formate via the Wood Ljungdahl pathway of B. hydrogenotrophica. We investigated these inter‐species interactions further using RNAseq to examine gene expression in continuous co‐cultures of R. bromii and B. hydrogenotrophica. Transcriptome analysis revealed upregulation of B. hydrogenotrophica genes involved in the Wood‐Ljungdahl pathway and of a 10 gene cluster responsible for increased branched chain amino acid fermentation in the co‐cultures. Cross‐feeding between formate‐producing species and acetogens may be a significant factor in short chain fatty acid formation in the colon contributing to high rates of acetate production. Transcriptome analysis also indicated competition for the vitamin thiamine and down‐regulation of dissimilatory sulfate reduction and key redox proteins in R. bromii in the co‐cultures, thus demonstrating the wide‐ranging consequences of inter‐species interactions in this model system.

AB - Interspecies cross‐feeding is a fundamental factor in anaerobic microbial communities. In the human colon formate is produced by many bacterial species but is normally detected only at low concentrations. Ruminococcus bromii produces formate, ethanol and acetate in approximately equal molar proportions in pure culture on RUM‐RS medium with 0.2% Novelose resistant starch (RS3) as energy source. Batch co‐culturing on starch with the acetogen Blautia hydrogenotrophica however led to the disappearance of formate and increased levels of acetate, which is proposed to occur through the routing of formate via the Wood Ljungdahl pathway of B. hydrogenotrophica. We investigated these inter‐species interactions further using RNAseq to examine gene expression in continuous co‐cultures of R. bromii and B. hydrogenotrophica. Transcriptome analysis revealed upregulation of B. hydrogenotrophica genes involved in the Wood‐Ljungdahl pathway and of a 10 gene cluster responsible for increased branched chain amino acid fermentation in the co‐cultures. Cross‐feeding between formate‐producing species and acetogens may be a significant factor in short chain fatty acid formation in the colon contributing to high rates of acetate production. Transcriptome analysis also indicated competition for the vitamin thiamine and down‐regulation of dissimilatory sulfate reduction and key redox proteins in R. bromii in the co‐cultures, thus demonstrating the wide‐ranging consequences of inter‐species interactions in this model system.

UR - http://www.mendeley.com/research/formate-crossfeeding-cooperative-metabolic-interactions-revealed-transcriptomics-cocultures-acetogen

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