Tartrate fermentation with H2 production by a new member of Sporomusaceae enriched from rice paddy soil

Appl Environ Microbiol. 2024 Apr 17;90(4):e0235123. doi: 10.1128/aem.02351-23. Epub 2024 Mar 22.

Abstract

In rice paddies, soil and plant-derived organic matter are degraded anaerobically to methane (CH4), a powerful greenhouse gas. The highest rate of methane emission occurs during the reproductive stage of the plant when mostly dicarboxylic acids are exudated by the roots. The emission of methane at this stage depends largely on the cooperative interaction between dicarboxylic acid-fermenting bacteria and methanogenic archaea in the rhizosphere. The fermentation of tartrate, one of the major acids exudated, has been scarcely explored in rice paddy soils. In this work, we characterized an anaerobic consortium from rice paddy soil composed of four bacterial strains, whose principal member (LT8) can ferment tartrate, producing H2 and acetate. Tartrate fermentation was accelerated by co-inoculation with a hydrogenotrophic methanogen. The assembled genome of LT8 possesses a Na+-dependent oxaloacetate decarboxylase and shows that this bacterium likely invests part of the H2 produced to reduce NAD(P)+ to assimilate C from tartrate. The phylogenetic analysis of the 16S rRNA gene, the genome-based classification as well as the average amino acid identity (AAI) indicated that LT8 belongs to a new genus within the Sporomusaceae family. LT8 shares a few common features with its closest relatives, for which tartrate degradation has not been described. LT8 is limited to a few environments but is more common in rice paddy soils, where it might contribute to methane emissions from root exudates.IMPORTANCEThis is the first report of the metabolic characterization of a new anaerobic bacterium able to degrade tartrate, a compound frequently associated with plants, but rare as a microbial metabolite. Tartrate fermentation by this bacterium can be coupled to methanogenesis in the rice rhizosphere where tartrate is mainly produced at the reproductive stage of the plant, when the maximum methane rate emission occurs. The interaction between secondary fermentative bacteria, such as LT8, and methanogens could represent a fundamental step in exploring mitigation strategies for methane emissions from rice fields. Possible strategies could include controlling the activity of these secondary fermentative bacteria or selecting plants whose exudates are more difficult to ferment.

Keywords: genome-resolved metagenomics; hydrogen-producing bacterium; oxaloacetate decarboxylase; root exudates.

MeSH terms

  • Bacteria
  • Bacteria, Anaerobic / metabolism
  • Base Composition
  • Euryarchaeota* / metabolism
  • Fermentation
  • Firmicutes / metabolism
  • Gram-Negative Bacteria / genetics
  • Methane / metabolism
  • Oryza* / microbiology
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • RNA, Ribosomal, 16S / metabolism
  • Sequence Analysis, DNA
  • Soil / chemistry
  • Tartrates / metabolism

Substances

  • Soil
  • tartaric acid
  • Tartrates
  • RNA, Ribosomal, 16S
  • Methane