Novel genomic determinants of respiratory metabolism in extremophilic prokaryotes

Background: Extremophilic prokaryotes are thriving at physico-chemical boundaries of life – temperatures up to 122°C, pH 0-12, 5-molar salinity. Many extremophiles represent deep phylogenetic lineages most closely related to the last common ancestor and could possess the most ancient as well as the most stable enzymes driving the key metabolic processes.
Objectives: Identification and description of novel determinants of anaerobic and aerobic respiration from extremophiles of various phylogenetic lineages.
Methods: Genomes of our several extremophilic isolates were screened for target genes using previously described strategies (doi:10.1111/1462-2920.12067); functions of target genes were evidenced at transcript or protein level, symbiotic interactions - by CARD-FISH.
Results: We have evidenced differential involvement of three novel c-type multihemes in Fe(III) respiration and electrogenesis of a thermophilic bacterium Carboxydothermus ferrireducens. For the first time, c-type multihemes determining Fe(III)-reduction were identified in hyperthermophilic archaea of Pyrobaculum genus. Three novel molybdopterin oxidoreductases were revealed in the genome of Halanaeroarchaeum sulfurireducens, determining sulfur respiration with acetate – a unique process for Archaea. Function of the enzymes was confirmed at transcript level. In a hyperacidophile Cuniculiplasma divulgatum, genes of A1-type heme-copper oxidase were identified. Phylogeny reconstruction and genomic context analysis put them into a separate cluster rooted to the ancestor form of all the modern A-type oxygen reductases. Genome analysis of putative C.divulgatum’s symbiont – a nanoarchaeon of ‘DPANN’ superphylum, revealed a cytochrome bd-oxidase to be its only candidate respiratory oxygen reductase, with the host cell being the most probable source of hemes and reduced quinones for the enzyme.