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Comparative proteomics of cobalamin-dependent propionate production by the rumen bacterium Xylanibacter ruminicola

ABSTRACT: Xylanibacter ruminicola is an abundant rumen bacterium that produces propionate in a cobalamin-dependent manner. However, the effect of cobalamin supplementation on the expression of propionate pathway enzymes has yet to be investigated. To assess this, comparative transcriptomics and proteomics was carried out on X. ruminicola KHP1 cultures grown in defined media in the presence and absence of cobalamin. Cobalamin supplementation did not affect expression of most propionate pathway proteins, with the only differentially abundant pathway enzyme being the cobalamin-dependent methylmalonyl-CoA mutase, which showed a minor upregulation in the presence of cobalamin. Our results demonstrate expression of the propionate pathway regardless of cobalamin availability, suggesting that cobalamin-dependent induction of propionate production by X. ruminicola is controlled post-translationally.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Bacteria Xylanibacter Ruminicola

SUBMITTER: Sam Mahoney-Kurpe

LAB HEAD: Dr Christina D. Moon

PROVIDER: PXD053273 | Pride | 2024-10-14

REPOSITORIES: pride

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Project description:Diatoms perform about 20% of photosynthesis on earth, play a crucial role in forming the base of the marine food web, and sequester anthropogenic carbon into the deep ocean through the biological pump. In some areas of the ocean, diatom growth is limited by the organic micronutrient cobalamin (vitamin B12). Cobalamin affects phytoplankton growth rate and biomass yield, though the consequences of cobalamin limitation are not well understood on the biochemical level. In a controlled laboratory setting, we grew two diatoms, Thalassiosira pseudonana and Navicula pelliculosa, under cobalamin limited and replete conditions to elucidate changes in metabolite pools under cobalamin limitation. Using targeted and untargeted metabolomics, we show that the cobalamin-dependent T. pseudonana experienced a metabolic cascade under cobalamin limitation that a ects the central methionine cycle, the transsulfuration pathway, and the composition of its osmolyte pools. N. pelliculosa, a cobalamin-independent diatom, also showed evidence for changes in the methionine cycle when grown without cobalamin, though to a lesser extent than what we observed in T. pseudonana. In both diatoms the concentration of 5'-methylthioadenosine decreased when limited for cobalamin, suggesting a disruption in the diatoms' polyamine biosynthesis. Furthermore, two acylcarnitines and adenosyl cobalamin accumulated in T. pseudonana under cobalamin limitation, suggesting the use of an adenosylcobalamin-dependent enzyme, methylmalonyl CoA mutase. Overall, these changes in metabolite pools yield insight into the metabolic consequences of cobalamin limitation in diatoms and suggest that cobalamin starvation may have consequences for microbial interactions that are based on metabolite production by phytoplankton. Navicula pelliculosa protocols and data are reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS708' rel='noopener noreferrer' target='_blank'>MTBLS708</a>. Thalassiosira pseudonana protocols and data are reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS703' rel='noopener noreferrer' target='_blank'>MTBLS703</a>.

Project description:Diatoms perform about 20% of photosynthesis on earth, play a crucial role in forming the base of the marine food web, and sequester anthropogenic carbon into the deep ocean through the biological pump. In some areas of the ocean, diatom growth is limited by the organic micronutrient cobalamin (vitamin B12). Cobalamin affects phytoplankton growth rate and biomass yield, though the consequences of cobalamin limitation are not well understood on the biochemical level. In a controlled laboratory setting, we grew two diatoms, Thalassiosira pseudonana and Navicula pelliculosa, under cobalamin limited and replete conditions to elucidate changes in metabolite pools under cobalamin limitation. Using targeted and untargeted metabolomics, we show that the cobalamin-dependent T. pseudonana experienced a metabolic cascade under cobalamin limitation that a ects the central methionine cycle, the transsulfuration pathway, and the composition of its osmolyte pools. N. pelliculosa, a cobalamin-independent diatom, also showed evidence for changes in the methionine cycle when grown without cobalamin, though to a lesser extent than what we observed in T. pseudonana. In both diatoms the concentration of 5'-methylthioadenosine decreased when limited for cobalamin, suggesting a disruption in the diatoms' polyamine biosynthesis. Furthermore, two acylcarnitines and adenosyl cobalamin accumulated in T. pseudonana under cobalamin limitation, suggesting the use of an adenosylcobalamin-dependent enzyme, methylmalonyl CoA mutase. Overall, these changes in metabolite pools yield insight into the metabolic consequences of cobalamin limitation in diatoms and suggest that cobalamin starvation may have consequences for microbial interactions that are based on metabolite production by phytoplankton. Thalassiosira pseudonana protocols and data are reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS703' rel='noopener noreferrer' target='_blank'>MTBLS703</a>. Navicula pelliculosa protocols and data are reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS708' rel='noopener noreferrer' target='_blank'>MTBLS708</a>.

Project description:Propionate is a common three-carbon intermediate produced from the breakdown of propiogenic substrates, such as branched-chain amino acids and odd-numbered fatty acids, and by gut bacteria. Propionate can chemically modify proteins, and if this involves histones, it may underpin a disease-relevant link between short-chain acyls and gene expression in the heart. Here, we sought to characterize how propionate-dependent modifications to histones affect cardiac gene expression and contractile function in a mouse model producing elevated levels of propionate/propionyl-CoA. An adult mouse model of propionic acidaemia (PA) was used to investigate how propionate affects histones and gene expression in the heart, an organ strongly affected in PA patients. Mass spectrometry confirmed elevated plasma propionate in 8-week PA mice, reaching levels detected in PA patient serum. Metabolomic analyses confirmed a metabolic signature of PA, but male mice had enhanced propionate processing towards -alanine. Female PA hearts had expanded end-diastolic and end-systolic volumes, and weaker systolic contractions, without major electrocardiographic changes. Ca2+ signals were deranged in female PA mice (raised diastolic Ca2+), consistent with contractile dysfunction. Differentially-expressed genes (DEGs) included Pde9a and Mme, previously linked to cardiac dysfunction. These DEGs also responded to 48-h culture of wild-type myocytes with propionate as well as butyrate, an HDAC inhibitor, suggesting a role for increased histone acetylation alongside propionylation in inducing these genes. Indeed, histone acetylation (H3K27ac) and propionylation were elevated genome-wide in the PA heart and at the promoters of Pde9a and Mme. These propionate-associated epigenetic responses were more pronounced in female PA mice. The greater prominence of epigenetic, transcriptional, and functional responses in female PA mice, despite a mostly sex-indiscriminate overall metabolic milieu, argues that histone acylation plays a defining role in the cardiac phenotype. We conclude that perturbed propionate metabolism in vivo alters histone acylation and gene expression, which impacts cardiac contractile function.

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Comparative proteomics of cobalamin-dependent propionate production by the rumen bacterium Xylanibacter ruminicola

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