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Regulation of methanol oxidation and carbon dioxide fixation in Xanthobacter strain 25a grown in continuous culture

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Abstract

The regulation of C1-metabolism in Xanthobacter strain 25a was studied during growth of the organism on acetate, formate and methanol in chemostat cultures. No activity of methanol dehydrogenase (MDH), formate dehydrogenase (FDS) or ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisC/O) could be detected in cells grown on acetate alone over a range of dilution rates tested. Addition of methanol or formate to the feed resulted in the immediate induction of MDH and FDH and complete utilization (D=0.10 h-1) of acetate and the C 1-substrates. The activities of these enzymes rapidly dropped at the higher growth rates, which suggests that their synthesis is further controlled via repression by “heterotrophic” substrates such as acetate. Synthesis of RuBisC/O already occurred at low methanol concentrations in the feed, resulting in additive growth yields on acetate/methanol mixtures. The energy generated in the oxidation of formate initially allowed an increased assimilation of acetate (and a decreased dissimilation), resulting in enhanced growth yields on the mixture. RuBisC/O activity could only be detected at the higher formate/acetate ratios in the feed. The data suggest that synthesis of RuBisC/O and CO2 fixation via the Calvin cycle in Xanthobacter strain 25 a is controlled via a (de)repression mechanism, as is the case in other facultatively autotrophic bacteria. Autotrophic CO2 fixation only occurs under conditions with a diminished supply of “heterotrophic” carbon sources and a sufficiently high availability of suitable energy sources. The latter point is further supported by the clearly more pronounced derepressing effect exerted by methanol compared to formate.

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Abbreviations

FDH:

formate dehydrogenase

FBPase:

fructose-1,6-bisphosphatase

ICDH:

isocitrate dehydrogenase

MDH:

methanol dehydrogenase

PQQ:

pyrrolo quinoline quinone

PRK:

phosphoribulokinase

RuBisC/O:

ribulose-1,5-bisphosphate carboxylase/oxygenase

RuMP:

ribulose monophosphate

TCA:

tricarboxylic acid cycle

References

  • DijkhuizenL, HarderW (1979) Regulation of autotrophic and heterotrophic metabolism in Pseudomonas oxalaticus OX1. Growth on mixtures of acetate and formate in continuous culture. Arch Microbiol 123:47–53

    Article  CAS  Google Scholar 

  • DijkhuizenL, HarderW (1984) Current views on the regulation of autotrophic carbon dioxide fixation via the Calvin cycle in bacteria. Antonie van Leeuwenhoek; J Microbiol Serol 50:473–487

    CAS  Google Scholar 

  • DijkhuizenL, KnightM, HarderW (1978) Metabolic regulation in Pseudomonas oxalaticus OX1. Autotrophic and heterotrophic growth on mixed substrates. Arch Microbiol 116:77–83

    Article  CAS  Google Scholar 

  • GibsonJL, TabitaFR (1988) Localization and mapping of CO2 fixation genes within two gene clusters in Rhodobacter sphaeroides. J Bacteriol 170:2153–2158

    Article  CAS  Google Scholar 

  • GoldbergI, RockJS, Ben-BassatA, MatelesRI (1976) Bacterial yields on methanol, methylamine, formaldehyde, and formate. Biotechnol Bioeng 18:1657–1668

    Article  CAS  Google Scholar 

  • GreenwoodJA, JonesCW (1986) Environmental regulation of the methanol oxidase system of Methylophilus methylotrophus. J Gen Microbiol 132:1247–1256

    CAS  Google Scholar 

  • HeijthuijsenJHFG, HansenTA (1989) Betaine fermentation and oxidation by marine Desulfuromonas strains. Appl Environ Microbiol 55:965–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • HusemannM, KlintworthR, BüttcherV, SalnikovJ, WeissenbornC, BowienB (1988) Chromosomally and plasmid-encoded gene clusters for CO2 fixation (cfx genes) in Alcaligenes eutrophus. Mol Gen Genet 214:112–120

    Article  CAS  Google Scholar 

  • JanssenDB, KeuningS, WitholtB (1987) Involvement of a quinoprotein alcohol dehydrogenase and an NAD-dependent aldehyde dehydrogenase in 2-chloroethanol metabolism in Xanthobacter autotrophicus GJ10. J Gen Microbiol 133:85–92

    CAS  Google Scholar 

  • JenniB, AragnoM (1987) Xanthobacter agilis sp. nov., a motile, dinitrogen-fixing, hydrogen-oxidizing bacterium. Syst Appl Microbiol 9:254–257

    Article  CAS  Google Scholar 

  • JenniB, AragnoM, WiegelJKW (1987) Numerical analysis and DNA-DNA hybridization studies on Xanthobacter and emendation of Xanthobacter flavus. Syst Appl Microbiol 9:247–253

    Article  Google Scholar 

  • LaanbroekHJ, AbeeT, VoogdJL (1982) Alcohol conversions by Desulfobulbus propionicus Lindhorst in the presence and absence of sulfate and hydrogen. Arch Microbiol 133: 178–184

    Article  CAS  Google Scholar 

  • LehmickeLG, LidstromME (1985) Organization of genes necessary for growth of the hydrogen-methanol autotroph Xanthobacter sp. strain H4–14 on hydrogen and carbon dioxide. J Bacteriol 162:1244–1249

    CAS  PubMed  PubMed Central  Google Scholar 

  • LeveringPR, DijkhuizenL (1985) Regulation of methylotrophic and heterotrophic metabolism in Arthrobacter P1. Growth on mixtures of methylamine and acetate in batch and continuous culture. Arch Microbiol 142:113–120

    Article  CAS  Google Scholar 

  • MeijerWG, CroesLM, JenniB, LehmickeLG, LidstromME, DijkhuizenL (1990a) Characterization of Xanthobacter strains H4–14 and 25a and enzyme profiles after growth under autotrophic and heterotrophic conditions. Arch Microbiol 153: 360–367

    Article  CAS  Google Scholar 

  • Meijer WG, Arnberg AC, Enequist HG, Terpstra P, Lidstrom ME, Dijkhuizen L (1990b) Identification and organization of carbon dioxide fixation genes in Xanthobacter flavus H4-14. Mol Gen Genet (in press)

  • Meijer WG, Enequist HG, Terpstra P, Dijkhuizen L (1990c) Nucleotide sequences of the genes encoding fructosebisphosphatase and phosphoribulokinase from Xanthobacter flavus H4-14. J Gen Microbiol (in press)

  • RoitschT, StolpH (1985) Overproduction of methanol dehydrogenase in glucose grown cells of a restricted RuMP type methylotroph. Arch Microbiol 142:43–49

    Article  Google Scholar 

  • RoitschT, StolpH (1986) Synthesis of dissimilatory enzymes of serine type methylotrophs under different growth conditions. Arch Microbiol 144:245–247

    Article  CAS  Google Scholar 

  • TabitaFR (1988) Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol Rev 52:155–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • VerseveldHWvan, StouthamerAH (1978) Growth yields and the efficiency of oxidative phosphorylation during autotrophic growth of Paracoccus denitrificans on methanol and formate. Arch Microbiol 118:21–26

    Article  Google Scholar 

  • VriesGEde, HarmsN, MaurerK, PadendrechtA, StouthamerAH (1988) Physiological regulation of Paracoccus denitrificans methanol dehydrogenase synthesis and activity. J Bacteriol 170:3731–3737

    Article  Google Scholar 

  • WeaverCA, LidstromM (1985) Methanol dissimilation in Xanthobacter H4–14: activities, induction and comparison to Pseudomonas AM1 and Paracoccus denitrificans. J Gen Microbiol 131:2183–2197

    CAS  PubMed  Google Scholar 

  • WeaverCA, LidstromME (1987) Isolation, complementation and partial characterization of mutants of the methanol autotroph Xanthobacter H4–14 defective in methanol dissimilation. J Gen Microbiol 133:1721–1731

    CAS  PubMed  Google Scholar 

  • WiegelJKW, SchlegelHG (1984) Genus Xanthobacter Wiegel, Wilke, Baumgarten, Opitz and Schlegel 1978, 573AL. In: KriegNR, HoltJG (eds) Bergey's manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore London, pp 325–333

    Google Scholar 

  • WiegelJ, WilkeD, BaumgartenJ, OpitzR, SchlegelHG (1978) Transfer of the nitrogen-fixing hydrogen bacterium Corynebacterium autotrophicum Baumgarten et al. to Xanthobacter gen. nov. Int J Syst Bacteriol 28:573–581

    Article  Google Scholar 

  • WilkeD (1980) Conjugational gene transfer in Xanthobacter autotrophicus GZ29. J Gen Microbiol 117:431–436

    Google Scholar 

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Croes, L.M., Meijer, W.G. & Dijkhuizen, L. Regulation of methanol oxidation and carbon dioxide fixation in Xanthobacter strain 25a grown in continuous culture. Arch. Microbiol. 155, 159–163 (1991). https://doi.org/10.1007/BF00248611

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