Abstract

BackgroundThe 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.ResultsIn 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.ConclusionPhotoheterotrophic 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.

Highlights

  • The great metabolic versatility of the purple non-sulfur bacteria is of particular interest in green technology

  • Growth of Rs. rubrum S1H under photoheterotrophic conditions with butyrate as carbon source To obtain unbiased proteomic data, it is crucial to harvest cells grown under different conditions in similar growth phases

  • We observed three successive growth arrests in the growth curve that were concomitant with halted butyrate assimilation and that could all be released by the addition of extra bicarbonate

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Summary

Introduction

The great metabolic versatility of the purple non-sulfur bacteria is of particular interest in green technology. Purple non-sulfur bacteria (PNSB) are known for their remarkable metabolic versatility. They represent a promising resource for biotechnology such as biofuel and. De Meur et al BMC Microbiology (2020) 20:126 anoxygenic conditions, Rs. rubrum is known to grow photoheterotrophically, using light as an energy source and VFAs as carbon and electron sources. In photoheterotrophic conditions with light as the energy source, the assimilated organic carbon compounds are used to supply the biosynthesis of anabolic precursors. These precursors are mainly intermediates of the citric acid cycle and must be continuously replenished through anaplerotic pathways. Among the alternative pathways recently proposed for Icl-negative organisms, the ethylmalonyl-CoA pathway was demonstrated to be a key acetate assimilation route in Rhodobacter sphaeroides [6], Methylobacterium extorquens [7,8,9] and Rs. rubrum [10]

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