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Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting Pelotomaculum thermopropionicum and Hydrogenotrophic Methanocella conradii.

ABSTRACT: Microbial syntrophy is a thermodynamically-based cooperation between microbial partners that share the small amounts of free energy for anaerobic growth. To gain insights into the mechanism by which syntrophic microorganisms coordinate their metabolism, we constructed cocultures of propionate-oxidizing Pelotomaculum thermopropionicum and hydrogenotrophic Methanocella conradii and compared them to monocultures. Transcriptome analysis was performed on these cultures using strand-specific mRNA sequencing (RNA-Seq). The results showed that in coculture both P. thermopropionicum and M. conradii significantly upregulated the expression of genes involved in catabolism but downregulated those for anabolic biosynthesis. Specifically, genes coding for the methylmalonyl-CoA pathway in P. thermopropionicum and key genes for methanogenesis in M. conradii were substantially upregulated in coculture compared to monoculture. The putative flavin-based electron bifurcation/confurcation systems in both organisms were also upregulated in coculture. Formate dehydrogenase encoding genes in both organisms were markedly upregulated, indicating that formate was produced and utilized by P. thermopropionicum and M. conradii, respectively. The inhibition of syntrophic activity by formate and 2-bromoethanesulphonate (2-BES) but not H2/CO2 also suggested that formate production was used by P. thermopropionicum for the recycling of intracellular redox mediators. Finally, flagellum-induced signal transduction and amino acids exchange was upregulated for syntrophic interactions. Together, our study suggests that syntrophic organisms employ multiple strategies including global metabolic shift, utilization of electron bifurcation/confurcation and employing formate as an alternate electron carrier to optimize their metabolisms for syntrophic growth.

SUBMITTER: Liu P

PROVIDER: S-EPMC6046458 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting Pelotomaculum thermopropionicum and Hydrogenotrophic Methanocella conradii.

Liu Pengfei P Lu Yahai Y

Frontiers in microbiology 20180709

Microbial syntrophy is a thermodynamically-based cooperation between microbial partners that share the small amounts of free energy for anaerobic growth. To gain insights into the mechanism by which syntrophic microorganisms coordinate their metabolism, we constructed cocultures of propionate-oxidizing Pelotomaculum thermopropionicum and hydrogenotrophic Methanocella conradii and compared them to monocultures. Transcriptome analysis was performed on these cultures using strand-spec ...[more]

PMID: 30038609

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Project description:BACKGROUND: Methanocellales contributes significantly to anthropogenic methane emissions that cause global warming, but few pure cultures for Methanocellales are available to permit subsequent laboratory studies (physiology, biochemistry, etc.). METHODOLOGY/PRINCIPAL FINDINGS: By combining anaerobic culture and molecular techniques, a novel thermophilic methanogen, strain HZ254(T) was isolated from a Chinese rice field soil located in Hangzhou, China. The phylogenetic analyses of both the 16S rRNA gene and mcrA gene (encoding the ? subunit of methyl-coenzyme M reductase) confirmed its affiliation with Methanocellales, and Methanocella paludicola SANAE(T) was the most closely related species. Cells were non-motile rods, albeit with a flagellum, 1.4-2.8 µm long and by 0.2-0.3 µm in width. They grew at 37-60 °C (optimally at 55 °C) and salinity of 0-5 g NaCl l(-1) (optimally at 0-1 g NaCl l(-1)). The pH range for growth was 6.4-7.2 (optimum 6.8). Under the optimum growth condition, the doubling time was 6.5-7.8 h, which is the shortest ever observed in Methanocellales. Strain HZ254(T) utilized H(2)/CO(2) but not formate for growth and methane production. The DNA G+C content of this organism was 52.7 mol%. The sequence identities of 16S rRNA gene and mcrA gene between strain HZ254(T) and SANAE(T) were 95.0 and 87.5% respectively, and the genome based Average Nucleotide Identity value between them was 74.8%. These two strains differed in phenotypic features with regard to substrate utilization, possession of a flagellum, doubling time (under optimal conditions), NaCl and temperature ranges. Taking account of the phenotypic and phylogenetic characteristics, we propose strain HZ254(T) as a representative of a novel species, Methanocella conradii sp. nov. The type strain is HZ254(T) ( = CGMCC 1.5162(T) = JCM 17849(T) = DSM 24694(T)). CONCLUSIONS/SIGNIFICANCE: Strain HZ254(T) could potentially serve as an excellent laboratory model for studying Methanocellales due to its fast growth and consistent cultivability.

Dataset Information

Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting Pelotomaculum thermopropionicum and Hydrogenotrophic Methanocella conradii.

Publications

Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting <i>Pelotomaculum thermopropionicum</i> and Hydrogenotrophic <i>Methanocella conradii</i>.

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