Access to novel ecological niches often requires adaptation of metabolic pathways to cope with new environments. For conversion to cellular building blocks, many substrates enter central carbon metabolism via acetyl-coenzyme A (acetyl-CoA). Until now, only two such pathways have been identified: the glyoxylate cycle and the ethylmalonyl-CoA pathway. Prokaryotes in the haloarchaea use a third pathway by which acetyl-CoA is oxidized to glyoxylate via the key intermediate methylaspartate. Glyoxylate condensation with another acetyl-CoA molecule yields malate, the final assimilation product. This cycle combines reactions that originally belonged to different metabolic processes in different groups of prokaryotes, which suggests lateral gene transfer and evolutionary tinkering of acetate assimilation. Moreover, it requires elevated intracellular glutamate concentrations, as well as coupling carbon assimilation with nitrogen metabolism.

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Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by inhibitor studies and membrane potential measurements of aerobically grown M. roseus cells revealed the activity of aerobic respiratory electron transfer chain comprised of respiratory complexes I and IV, and an alternative complex III. Phylogeny reconstruction revealed that oxygen reductases belonged to atypical cc(o/b)o3-type and canonical cbb3–type cytochrome oxidases. Also, two molybdoenzymes of M. roseus were affiliated either with Ttr or Psr/Phs clades, but not with typical respiratory arsenate reductases of the Arr clade. Expression profiling, both at transcripts and protein level, allowed us to assign the role of the terminal respiratory oxidase under atmospheric oxygen concentration for the cc(o/b)o3 cytochrome oxidase, previously proposed to serve for oxygen detoxification only. Transcriptomic analysis revealed the involvement of both molybdoenzymes of M. roseus in As(V) respiration, yet differences in the genomic context of their gene clusters allow to hypothesize about their distinct roles in arsenate metabolism with the ‘Psr/Phs’-type molybdoenzyme being the most probable candidate respiratory arsenate reductase. Basing on multi-omics data, the pathways for aerobic and arsenate respiration were proposed. Our results start to bridge the vigorously increasing gap between homology-based predictions and experimentally verified metabolic processes, what is especially important for understudied microorganisms of novel lineages from deep subsurface environments of Eurasia, which remained separated from the rest of the biosphere for several geological periods.

A novel anaerobic chemoorganotrophic, facultatively alkaliphilic bacterium (strain M17 DMBT) was isolated from a coastal lake (Golubitsckoe, Taman Peninsula, Russia). Cells were motile rods, 1.6–2.1 µm long and 0.45 µm in diameter. The temperature range for growth was 14–42 °C, with an optimum at 30 °C. The pH range for growth was pH 5.5–10.0, with an optimum at pH 8.0–8.5. Growth of strain M17 DMBT was observed at NaCl concentrations of 1–12 % (w/v) with optimum growth at 1.5–2.0 %. Strain M17 MBTutilized glucose, fructose, sucrose, ribose, mannose, raffinose, arabinose, dextrin, yeast extract, peptone, carbon monoxide, vanillic acid and 3,4-dimethoxybenzoic acid. The end products from glucose fermentation were acetate and ethanol. The DNA G+C content of strain M17 DMBT was 39.1 mol%. The closest phylogenetic relative of strain M17 DMBT was Alkalibacter saccharofermentans with 97.8 % 16S rRNA gene sequence similarity. The OrthoANI value between M17 DMBT and A. saccharofermentans was 70.4 %. Based on the phenotypic, genotypic and phylogenetic characteristics of the isolate, strain M17 DMBT is considered to represent a novel species of the genus Alkalibacter for which the name Alkalibacter mobilis sp. nov. is proposed. The type strain of Alkalibacter mobilis is M17 DMBT (=KCTC 15920T=VKM B-3408T).

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