Dataset Information

Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi.

ABSTRACT: Euryarchaeal lineages have been believed to have a methanogenic last common ancestor. However, members of euryarchaeal Archaeoglobi have long been considered nonmethanogenic and their evolutionary history remains elusive. Here, three high-quality metagenomic-assembled genomes (MAGs) retrieved from high-temperature oil reservoir and hot springs, together with three newly assembled Archaeoglobi MAGs from previously reported hot spring metagenomes, are demonstrated to represent a novel genus of Archaeoglobaceae, "Candidatus Methanomixophus." All "Ca Methanomixophus" MAGs encode an M methyltransferase (MTR) complex and a traditional type of methyl-coenzyme M reductase (MCR) complex, which is different from the divergent MCR complexes found in "Ca Polytropus marinifundus." In addition, "Ca Methanomixophus dualitatem" MAGs preserve the genomic capacity for dissimilatory sulfate reduction. Comparative phylogenetic analysis supports a laterally transferred origin for an MCR complex and vertical heritage of the MTR complex in this lineage. Metatranscriptomic analysis revealed concomitant in situ activity of hydrogen-dependent methylotrophic methanogenesis and heterotrophic fermentation within populations of "Ca Methanomixophus hydrogenotrophicum" in a high-temperature oil reservoir.IMPORTANCE Current understanding of the diversity, biology, and ecology of Archaea is very limited, especially considering how few of the known phyla have been cultured or genomically explored. The reconstruction of "Ca Methanomixophus" MAGs not only expands the known range of metabolic versatility of the members of Archaeoglobi but also suggests that the phylogenetic distribution of MCR and MTR complexes is even wider than previously anticipated.

SUBMITTER: Liu YF

PROVIDER: S-EPMC7380581 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi.

Liu Yi-Fan YF Chen Jing J Zaramela Livia S LS Wang Li-Ying LY Mbadinga Serge Maurice SM Hou Zhao-Wei ZW Wu Xiao-Lin XL Gu Ji-Dong JD Zengler Karsten K Mu Bo-Zhong BZ

mSystems 20200317 2

Euryarchaeal lineages have been believed to have a methanogenic last common ancestor. However, members of euryarchaeal Archaeoglobi have long been considered nonmethanogenic and their evolutionary history remains elusive. Here, three high-quality metagenomic-assembled genomes (MAGs) retrieved from high-temperature oil reservoir and hot springs, together with three newly assembled Archaeoglobi MAGs from previously reported hot spring metagenomes, are demonstrated to represent a nove ...[more]

PMID: 32184369

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Project description:UnlabelledPyruvate, a central intermediate in the carbon fixation pathway of methanogenic archaea, is rarely used as an energy source by these organisms. The sole exception to this rule is a genetically uncharacterized Methanosarcina barkeri mutant capable of using pyruvate as a sole energy and carbon source (the Pyr(+) phenotype). Here, we provide evidence that suggests that the Pyr(+) mutant is able to metabolize pyruvate by overexpressing pyruvate ferredoxin oxidoreductase (por) and mutating genes involved in central carbon metabolism. Genomic analysis showed that the Pyr(+) strain has two mutations localized to Mbar_A1588, the biotin protein ligase subunit of the pyruvate carboxylase (pyc) operon, and Mbar_A2165, a putative transcriptional regulator. Mutants expressing the Mbar_A1588 mutation showed no growth defect compared to the wild type (WT), yet the strains lacked pyc activity. Recreation of the Mbar_A2165 mutation resulted in a 2-fold increase of Por activity and gene expression, suggesting a role in por transcriptional regulation. Further transcriptomic analysis revealed that Pyr(+) strains also overexpress the gene encoding phosphoenolpyruvate carboxylase, indicating the presence of a previously uncharacterized route for synthesizing oxaloacetate in M. barkeri and explaining the unimpaired growth in the absence of Pyc. Surprisingly, stringent repression of the por operon was lethal, even when the media were supplemented with pyruvate and/or Casamino Acids, suggesting that por plays an unidentified essential function in M. barkeri.ImportanceThe work presented here reveals a complex interaction between anabolic and catabolic pathways involving pyruvate metabolism in Methanosarcina barkeri Fusaro. Among the unexpected findings were an essential role for the enzyme pyruvate-ferredoxin oxidoreductase and an alternate pathway for synthesis of oxaloacetate. These results clarify the mechanism of methanogenic catabolism of pyruvate and expand our understanding of carbon assimilation in methanogens.

Project description:BackgroundStreptococcus agalactiae is a major cause of bovine mastitis, which is the dominant health disorder affecting milk production within the dairy industry and is responsible for substantial financial losses to the industry worldwide. However, there is considerable evidence for host adaptation (ecotypes) within S. agalactiae, with both bovine and human sourced isolates showing a high degree of distinctiveness, suggesting differing ability to cause mastitis. Here, we (i) generate RNAseq data from three S. agalactiae isolates (two putative bovine adapted and one human) and (ii) compare publicly available whole genome shotgun sequence data from an additional 202 isolates, obtained from six host species, to elucidate possible genetic factors/adaptations likely important for S. agalactiae growth and survival in the bovine mammary gland.ResultsTests for differential expression showed distinct expression profiles for the three isolates when grown in bovine milk. A key finding for the two putatively bovine adapted isolates was the up regulation of a lactose metabolism operon (Lac.2) that was strongly correlated with the bovine environment (all 36 bovine sourced isolates on GenBank possessed the operon, in contrast to only 8/151 human sourced isolates). Multi locus sequence typing of all genome sequences and phylogenetic analysis using conserved operon genes from 44 S. agalactiae isolates and 16 additional Streptococcus species provided strong evidence for acquisition of the operon via multiple lateral gene transfer events, with all Streptococcus species known to be major causes of mastitis, identified as possible donors. Furthermore, lactose fermentation tests were only positive for isolates possessing Lac.2. Combined, these findings suggest that lactose metabolism is likely an important adaptation to the bovine environment. Additional up regulation in the bovine adapted isolates included genes involved in copper homeostasis, metabolism of purine, pyrimidine, glycerol and glucose, and possibly aminoglycoside antibiotic resistance.ConclusionWe detected several genetic factors likely important in S. agalactiae's adaptation to the bovine environment, in particular lactose metabolism. Of concern is the up regulation of a putative antibiotic resistance gene (GCN5-related N-acetyltransferase) that might reflect an adaptation to the use of aminoglycoside antibiotics within this environment.

Dataset Information

Genomic and Transcriptomic Evidence Supports Methane Metabolism in Archaeoglobi.

Publications

Genomic and Transcriptomic Evidence Supports Methane Metabolism in <i>Archaeoglobi</i>.

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