Lanthanide-dependent methanol and formaldehyde oxidation in methylobacterium aquaticum strain 22A

Patcha Yanpirat, Yukari Nakatsuji, Shota Hiraga, Yoshiko Fujitani, Terumi Izumi, Sachiko Masuda, Ryoji Mitsui, Tomoyuki Nakagawa, Akio Tani

Research output: Contribution to journalArticle

Abstract

Lanthanides (Ln) are an essential cofactor for XoxF-type methanol dehydrogenases (MDHs) in Gram-negative methylotrophs. The Ln3+ dependency of XoxF has expanded knowledge and raised new questions in methylotrophy, including the differences in characteristics of XoxF-type MDHs, their regulation, and the methylotrophic metabolism including formaldehyde oxidation. In this study, we genetically identified one set of Ln3+-and Ca2+-dependent MDHs (XoxF1 and MxaFI), that are involved in methylotrophy, and an ExaF-type Ln3+-dependent ethanol dehydrogenase, among six MDH-like genes in Methylobacterium aquaticum strain 22A. We also identified the causative mutations in MxbD, a sensor kinase necessary for mxaF expression and xoxF1 repression, for suppressive phenotypes in xoxF1 mutants defective in methanol growth even in the absence of Ln3+. Furthermore, we examined the phenotypes of a series of formaldehyde oxidation-pathway mutants (fae1, fae2, mch in the tetrahydromethanopterin (H4MPT) pathway and hgd in the glutathione-dependent formaldehyde dehydrogenase (GSH) pathway). We found that MxaF produces formaldehyde to a toxic level in the absence of the formaldehyde oxidation pathways and that either XoxF1 or ExaF can oxidize formaldehyde to alleviate formaldehyde toxicity in vivo. Furthermore, the GSH pathway has a supportive role for the net formaldehyde oxidation in addition to the H4MPT pathway that has primary importance. Studies on methylotrophy in Methylobacterium species have a long history, and this study provides further insights into genetic and physiological diversity and the differences in methylotrophy within the plant-colonizing methylotrophs.

Original languageEnglish
Article number822
JournalMicroorganisms
Volume8
Issue number6
DOIs
Publication statusPublished - Jun 2020

Keywords

  • Lanthanide
  • Methanol dehydrogenase
  • Methylobacterium species
  • Methylotroph
  • XoxF

ASJC Scopus subject areas

  • Microbiology
  • Virology
  • Microbiology (medical)

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  • Cite this

    Yanpirat, P., Nakatsuji, Y., Hiraga, S., Fujitani, Y., Izumi, T., Masuda, S., Mitsui, R., Nakagawa, T., & Tani, A. (2020). Lanthanide-dependent methanol and formaldehyde oxidation in methylobacterium aquaticum strain 22A. Microorganisms, 8(6), [822]. https://doi.org/10.3390/microorganisms8060822