New perspectives on butyrate assimilation in Rhodospirillum rubrum S1H under photoheterotrophic conditions.


Journal

BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981

Informations de publication

Date de publication:
20 05 2020
Historique:
received: 05 07 2019
accepted: 07 05 2020
entrez: 22 5 2020
pubmed: 22 5 2020
medline: 27 5 2021
Statut: epublish

Résumé

The great metabolic versatility of the purple non-sulfur bacteria is of particular interest in green technology. Rhodospirillum rubrum S1H is an α-proteobacterium that is capable of photoheterotrophic assimilation of volatile fatty acids (VFAs). Butyrate is one of the most abundant VFAs produced during fermentative biodegradation of crude organic wastes in various applications. While there is a growing understanding of the photoassimilation of acetate, another abundantly produced VFA, the mechanisms involved in the photoheterotrophic metabolism of butyrate remain poorly studied. In this work, we used proteomic and functional genomic analyses to determine potential metabolic pathways involved in the photoassimilation of butyrate. We propose that a fraction of butyrate is converted to acetyl-CoA, a reaction shared with polyhydroxybutyrate metabolism, while the other fraction supplies the ethylmalonyl-CoA (EMC) pathway used as an anaplerotic pathway to replenish the TCA cycle. Surprisingly, we also highlighted a potential assimilation pathway, through isoleucine synthesis and degradation, allowing the conversion of acetyl-CoA to propionyl-CoA. We tentatively named this pathway the methylbutanoyl-CoA pathway (MBC). An increase in isoleucine abundance was observed during the early growth phase under butyrate condition. Nevertheless, while the EMC and MBC pathways appeared to be concomitantly used, a genome-wide mutant fitness assay highlighted the EMC pathway as the only pathway strictly required for the assimilation of butyrate. Photoheterotrophic growth of Rs. rubrum with butyrate as sole carbon source requires a functional EMC pathway. In addition, a new assimilation pathway involving isoleucine synthesis and degradation, named the methylbutanoyl-CoA (MBC) pathway, could also be involved in the assimilation of this volatile fatty acid by Rs. rubrum.

Sections du résumé

BACKGROUND
The great metabolic versatility of the purple non-sulfur bacteria is of particular interest in green technology. Rhodospirillum rubrum S1H is an α-proteobacterium that is capable of photoheterotrophic assimilation of volatile fatty acids (VFAs). Butyrate is one of the most abundant VFAs produced during fermentative biodegradation of crude organic wastes in various applications. While there is a growing understanding of the photoassimilation of acetate, another abundantly produced VFA, the mechanisms involved in the photoheterotrophic metabolism of butyrate remain poorly studied.
RESULTS
In this work, we used proteomic and functional genomic analyses to determine potential metabolic pathways involved in the photoassimilation of butyrate. We propose that a fraction of butyrate is converted to acetyl-CoA, a reaction shared with polyhydroxybutyrate metabolism, while the other fraction supplies the ethylmalonyl-CoA (EMC) pathway used as an anaplerotic pathway to replenish the TCA cycle. Surprisingly, we also highlighted a potential assimilation pathway, through isoleucine synthesis and degradation, allowing the conversion of acetyl-CoA to propionyl-CoA. We tentatively named this pathway the methylbutanoyl-CoA pathway (MBC). An increase in isoleucine abundance was observed during the early growth phase under butyrate condition. Nevertheless, while the EMC and MBC pathways appeared to be concomitantly used, a genome-wide mutant fitness assay highlighted the EMC pathway as the only pathway strictly required for the assimilation of butyrate.
CONCLUSION
Photoheterotrophic growth of Rs. rubrum with butyrate as sole carbon source requires a functional EMC pathway. In addition, a new assimilation pathway involving isoleucine synthesis and degradation, named the methylbutanoyl-CoA (MBC) pathway, could also be involved in the assimilation of this volatile fatty acid by Rs. rubrum.

Identifiants

pubmed: 32434546
doi: 10.1186/s12866-020-01814-7
pii: 10.1186/s12866-020-01814-7
pmc: PMC7238569
doi:

Substances chimiques

Acyl Coenzyme A 0
Bacterial Proteins 0
Butyrates 0
Pentanols 0
ethylmalonyl-coenzyme A 0
Isoleucine 04Y7590D77

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

126

Subventions

Organisme : Fonds De La Recherche Scientifique - FNRS
ID : 2877824
Pays : International
Organisme : European Space Agency
ID : MELiSSA
Pays : International
Organisme : Belgian Scientific policy
ID : Prodex
Pays : International

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Auteurs

Quentin De Meur (Q)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium.

Adam Deutschbauer (A)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA.

Matthias Koch (M)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium.

Guillaume Bayon-Vicente (G)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium.

Paloma Cabecas Segura (P)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium.

Ruddy Wattiez (R)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium.

Baptiste Leroy (B)

Laboratory of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Avenue du champs de Mars, 6 (Pentagone 3B), 7000, Mons, Belgium. baptiste.leroy@umons.ac.be.

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Classifications MeSH