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Genomics and Biochemistry of Metabolic Pathways for the C1 Compounds Utilization in Colorless Sulfur Bacterium Beggiatoa leptomitoformis D-402

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Abstract

The metabolic pathways of one-carbon compounds utilized by colorless sulfur bacterium Beggiatoa leptomitoformis D-402 were revealed based on comprehensive analysis of its genomic organization, together with physiological, biochemical and molecular biological approaches. Strain D-402 was capable of aerobic methylotrophic growth with methanol as a sole source of carbon and energy and was not capable of methanotrophic growth because of the absence of genes of methane monooxygenases. It was established that methanol can be oxidized to CO2 in three consecutive stages. On the first stage methanol was oxidized to formaldehyde by the two PQQ (pyrroloquinolinequinone)-dependent methanol dehydrogenases (MDH): XoxF and Mdh2. Formaldehyde was further oxidized to formate via the tetrahydromethanopterin (H4MPT) pathway. And on the third stage formate was converted to CO2 by NAD+-dependent formate dehydrogenase Fdh2. Finally, it was established that endogenous CO2, formed as a result of methanol oxidation, was subsequently assimilated for anabolism through the Calvin–Benson–Bassham cycle. The similar way of one-carbon compounds utilization also exists in representatives of another freshwater Beggiatoa species—B. alba.

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Acknowledgements

The authors would like to express sincere gratitude to Alexey Fomenkov, Tamas Vincze, Brian P. Anton and Richard J. Roberts for their help with genome sequencing.

Funding

This work was supported by Russian Foundation for Basic Research (Grant 18-04-00556).

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Authors and Affiliations

  1. Department of Biochemistry and Cell Physiology, Voronezh State University, Universitetskaya pl., 1, Voronezh, Russia, 394018

    Maria V. Orlova, Eugenia I. Kulinchenko & Margarita Y. Grabovich

  2. All-Russian Collection of Microorganisms (VKM), G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region, Russia, 142290

    Sergey V. Tarlachkov

  3. Federal State Institution “Federal Research Centre “Fundamentals of Biotechnology” of the Russian Academy of Sciences”, Moscow, Russia, 117312

    Galina A. Dubinina

  4. Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, Russia, 142290

    Maria N. Tutukina

  5. Center for Data-Intensive Biomedicine and Biotechnology, Skolkovo Institute of Science and Technology, Moscow, Russia, 143028

    Maria N. Tutukina

Authors
  1. Maria V. Orlova
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  2. Sergey V. Tarlachkov
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  3. Eugenia I. Kulinchenko
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  4. Galina A. Dubinina
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  5. Maria N. Tutukina
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  6. Margarita Y. Grabovich
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Corresponding author

Correspondence to Margarita Y. Grabovich.

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Table S1

. The final concentration of additional components in the cultivation medium in different growth conditions. Table S2. Primers used in this work with their annealing temperatures. Table S3. Metabolic genes of Beggiatoa leptomitoformis D-402 that are discussed in the manuscript. Genes are organized based on their relevance to pathways. Table S4. Identity between proteins of two PQQ-dependent dehydrogenases of methanol/ethanol family of B. leptomitoformis D-402 and B. alba and typical methylotrophs. Table S5. Identity between proteins of the Pqq-clusters of B. leptomitoformis D-402 and Methylobacterium extorquens AM1 and Beggiatoa alba B18LD. Table S6. Identity between proteins which take part in formaldehyde oxidation to CO2 of B. leptomitoformis D-402 and Methylobacterium extorquens AM1 and Beggiatoa alba B18LD (PDF 195 kb)

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Orlova, M.V., Tarlachkov, S.V., Kulinchenko, E.I. et al. Genomics and Biochemistry of Metabolic Pathways for the C1 Compounds Utilization in Colorless Sulfur Bacterium Beggiatoa leptomitoformis D-402. Indian J Microbiol 58, 415–422 (2018). https://doi.org/10.1007/s12088-018-0737-x

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