Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A

Sachiko Masuda, Yutaka Suzuki, Yoshiko Fujitani, Ryoji Mitsui, Tomoyuki Nakagawa, Masaki Shintani, Akio Tani

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Methylobacterium species are representative of methylotrophic bacteria. Their genomes usually encode two types of methanol dehydrogenases (MDHs): MxaF and XoxF. The former is a Ca2+-dependent enzyme, and the latter was recently determined to be a lanthanide-dependent enzyme that is necessary for the expression of mxaF. This finding revealed the unexpected and important roles of lanthanides in bacterial methylotrophy. In this study, we performed transcriptome sequencing (RNA-seq) analysis using M. aquaticum strain 22A grown in the presence of different lanthanides. Expression of mxaF and xoxF1 genes showed a clear inverse correlation in response to La3+. We observed downregulation of formaldehyde oxidation pathways, high formaldehyde dehydrogenase activity, and low accumulation of formaldehyde in the reaction with cells grown in the presence of La3+; this might be due to the direct oxidation of methanol to formate by XoxF1. Lanthanides induced the transcription of AT-rich genes, the function of most of which was unknown, and genes possibly related to cellular survival, as well as other MDH homologues. These results revealed not only the metabolic response toward altered primary methanol oxidation, but also the possible targets to be investigated further in order to better understand methylotrophy in the presence of lanthanides. IMPORTANCE Lanthanides have been considered unimportant for biological processes. In methylotrophic bacteria, however, a methanol dehydrogenase (MDH) encoded by xoxF was recently found to be lanthanide dependent, while the classic-type mxaFI is calcium dependent. XoxF-type MDHs are more widespread in diverse bacterial genera, suggesting their importance for methylotrophy. Methylobacterium species, representative methylotrophic and predominating alphaproteobacteria in the phyllosphere, contain both types and regulate their expression depending on the availability of lanthanides. RNA-seq analysis showed that the regulation takes place not only for MDH genes but also the subsequent formaldehyde oxidation pathways and respiratory chain, which might be due to the direct oxidation of methanol to formate by XoxF. In addition, a considerable number of genes of unknown function, including AT-rich genes, were found to be upregulated in the presence of lanthanides. This study provides first insights into the specific reaction of methylotrophic bacteria to the presence of lanthanides, emphasizing the biological relevance of this trace metal.
Original languageEnglish
Article numbere00462-17
Pages (from-to)e00462-17
JournalmSphere
Volume3
Issue number1
DOIs
Publication statusPublished - Feb 7 2018

Fingerprint

Methylobacterium
Lanthanoid Series Elements
formic acid
Formaldehyde
Genes
Methanol
glutathione-independent formaldehyde dehydrogenase
Bacteria
RNA Sequence Analysis
Alphaproteobacteria
Biological Phenomena
Enzymes
Electron Transport
Transcriptome
Down-Regulation

Keywords

  • Lanthanide
  • Methanol dehydrogenase
  • Methylotrophs
  • XoxF

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Masuda, S., Suzuki, Y., Fujitani, Y., Mitsui, R., Nakagawa, T., Shintani, M., & Tani, A. (2018). Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A. mSphere, 3(1), e00462-17. [e00462-17]. https://doi.org/10.1128/mSphere.00462-17

Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A. / Masuda, Sachiko; Suzuki, Yutaka; Fujitani, Yoshiko; Mitsui, Ryoji; Nakagawa, Tomoyuki; Shintani, Masaki; Tani, Akio.

In: mSphere, Vol. 3, No. 1, e00462-17, 07.02.2018, p. e00462-17.

Research output: Contribution to journalArticle

Masuda, S, Suzuki, Y, Fujitani, Y, Mitsui, R, Nakagawa, T, Shintani, M & Tani, A 2018, 'Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A', mSphere, vol. 3, no. 1, e00462-17, pp. e00462-17. https://doi.org/10.1128/mSphere.00462-17
Masuda S, Suzuki Y, Fujitani Y, Mitsui R, Nakagawa T, Shintani M et al. Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A. mSphere. 2018 Feb 7;3(1):e00462-17. e00462-17. https://doi.org/10.1128/mSphere.00462-17
Masuda, Sachiko ; Suzuki, Yutaka ; Fujitani, Yoshiko ; Mitsui, Ryoji ; Nakagawa, Tomoyuki ; Shintani, Masaki ; Tani, Akio. / Lanthanide-dependent regulation of methylotrophy in Methylobacterium aquaticum strain 22A. In: mSphere. 2018 ; Vol. 3, No. 1. pp. e00462-17.
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N2 - Methylobacterium species are representative of methylotrophic bacteria. Their genomes usually encode two types of methanol dehydrogenases (MDHs): MxaF and XoxF. The former is a Ca2+-dependent enzyme, and the latter was recently determined to be a lanthanide-dependent enzyme that is necessary for the expression of mxaF. This finding revealed the unexpected and important roles of lanthanides in bacterial methylotrophy. In this study, we performed transcriptome sequencing (RNA-seq) analysis using M. aquaticum strain 22A grown in the presence of different lanthanides. Expression of mxaF and xoxF1 genes showed a clear inverse correlation in response to La3+. We observed downregulation of formaldehyde oxidation pathways, high formaldehyde dehydrogenase activity, and low accumulation of formaldehyde in the reaction with cells grown in the presence of La3+; this might be due to the direct oxidation of methanol to formate by XoxF1. Lanthanides induced the transcription of AT-rich genes, the function of most of which was unknown, and genes possibly related to cellular survival, as well as other MDH homologues. These results revealed not only the metabolic response toward altered primary methanol oxidation, but also the possible targets to be investigated further in order to better understand methylotrophy in the presence of lanthanides. IMPORTANCE Lanthanides have been considered unimportant for biological processes. In methylotrophic bacteria, however, a methanol dehydrogenase (MDH) encoded by xoxF was recently found to be lanthanide dependent, while the classic-type mxaFI is calcium dependent. XoxF-type MDHs are more widespread in diverse bacterial genera, suggesting their importance for methylotrophy. Methylobacterium species, representative methylotrophic and predominating alphaproteobacteria in the phyllosphere, contain both types and regulate their expression depending on the availability of lanthanides. RNA-seq analysis showed that the regulation takes place not only for MDH genes but also the subsequent formaldehyde oxidation pathways and respiratory chain, which might be due to the direct oxidation of methanol to formate by XoxF. In addition, a considerable number of genes of unknown function, including AT-rich genes, were found to be upregulated in the presence of lanthanides. This study provides first insights into the specific reaction of methylotrophic bacteria to the presence of lanthanides, emphasizing the biological relevance of this trace metal.

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