Intergenomic evolution and metabolic cross-talk between rumen and thermophilic autotrophic methanogenic archaea

• Published in: Molecular phylogenetics and evolution Vol. 107; pp. 293 - 304
• Main Authors: Bharathi, M., Chellapandi, P.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.02.2017
• Subjects: Animals; Archaea - genetics; Autotrophic Processes; Comparative genomics; DNA Replication - genetics; Evolution, Molecular; Formate dehydrogenase; Functional markers; Genetic Markers; Genetic Variation; Genome, Archaeal; Metabolic Networks and Pathways - genetics; Methane - metabolism; Methanobacteriaceae - genetics; Methanobrevibacter; Methanogenesis; Methanothermobacter; Molecular evolution; Phylogeny; Rumen - microbiology; Synteny; MTH; Methanothermobacter; hemC; nusA; Comparative genomics; Functional markers; murD; Phylogeny; engA; fusA; aEF-2; TFB; mcrA; Methanobrevibacter; OriC; mtd; leu; ogt; secY; obg/cgtA; rnhB; MMG; nifD; hsp20; cooF1/F2; glyS; infB; mutS; tgtA; polB1/B2; mvhD2; tpiA; rpoB/C; serS; MFC; frhABGDA; ispD; mreB; MRU; dnaG/J; purM; spoVC; Methanogenesis; OriCs; COG; mer; metK; truB; MSI; pyrG; fdhC/D; Molecular evolution; fdhA/B; radA; cdc6; Formate dehydrogenase; porCDABG; GGDC
• ISSN: 1055-7903; 1095-9513
• DOI: 10.1016/j.ympev.2016.11.008

[Display omitted] •We found an intergenomic evolutionary link between Methanobrevibacter and Methanothermobacter.•Metabolic cross-talk with mammalian bacterial origins supported the growth physiology of Methanobrevibacter.•Therapeutic targets discovered in Methanobrevibacter can reduce energy harvest in farm animals and mitigate methane emission globally. Methanobrevibacter ruminantium M1 (MRU) is a rumen methanogenic archaean that can be able to utilize formate and CO2/H2 as growth substrates. Extensive analysis on the evolutionary genomic contexts considered herein to unravel its intergenomic relationship and metabolic adjustment acquired from the genomic content of Methanothermobacter thermautotrophicus ΔH. We demonstrated its intergenomic distance, genome function, synteny homologs and gene families, origin of replication, and methanogenesis to reveal the evolutionary relationships between Methanobrevibacter and Methanothermobacter. Comparison of the phylogenetic and metabolic markers was suggested for its archaeal metabolic core lineage that might have evolved from Methanothermobacter. Orthologous genes involved in its hydrogenotrophic methanogenesis might be acquired from intergenomic ancestry of Methanothermobacter via Methanobacterium formicicum. Formate dehydrogenase (fdhAB) coding gene cluster and carbon monoxide dehydrogenase (cooF) coding gene might have evolved from duplication events within Methanobrevibacter-Methanothermobacter lineage, and fdhCD gene cluster acquired from bacterial origins. Genome-wide metabolic survey found the existence of four novel pathways viz. l-tyrosine catabolism, mevalonate pathway II, acyl-carrier protein metabolism II and glutathione redox reactions II in MRU. Finding of these pathways suggested that MRU has shown a metabolic potential to tolerate molecular oxygen, antimicrobial metabolite biosynthesis and atypical lipid composition in cell wall, which was acquainted by metabolic cross-talk with mammalian bacterial origins. We conclude that coevolution of genomic contents between Methanobrevibacter and Methanothermobacter provides a clue to understand the metabolic adaptation of MRU in the rumen at different environmental niches.