Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A
Lanthanides (Ln) are an essential cofactor for XoxF-type methanol dehydrogenases (MDHs) in Gram-negative methylotrophs. The Ln<sup>3+</sup> dependency of XoxF has expanded knowledge and raised new questions in methylotrophy, including the differences in characteristics of XoxF-type MDHs,...
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MDPI AG
2020-05-01
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| Online Access: | https://www.mdpi.com/2076-2607/8/6/822 |
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| author | Patcha Yanpirat Yukari Nakatsuji Shota Hiraga Yoshiko Fujitani Terumi Izumi Sachiko Masuda Ryoji Mitsui Tomoyuki Nakagawa Akio Tani |
| author_facet | Patcha Yanpirat Yukari Nakatsuji Shota Hiraga Yoshiko Fujitani Terumi Izumi Sachiko Masuda Ryoji Mitsui Tomoyuki Nakagawa Akio Tani |
| author_sort | Patcha Yanpirat |
| collection | DOAJ |
| description | Lanthanides (Ln) are an essential cofactor for XoxF-type methanol dehydrogenases (MDHs) in Gram-negative methylotrophs. The Ln<sup>3+</sup> 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 Ln<sup>3+</sup>- and Ca<sup>2+</sup>-dependent MDHs (XoxF1 and MxaFI), that are involved in methylotrophy, and an ExaF-type Ln<sup>3+</sup>-dependent ethanol dehydrogenase, among six MDH-like genes in <i>Methylobacterium aquaticum</i> strain 22A. We also identified the causative mutations in MxbD, a sensor kinase necessary for <i>mxaF</i> expression and <i>xoxF1</i> repression, for suppressive phenotypes in <i>xoxF1</i> mutants defective in methanol growth even in the absence of Ln<sup>3+</sup>. Furthermore, we examined the phenotypes of a series of formaldehyde oxidation-pathway mutants (<i>fae1</i>, <i>fae2</i>, <i>mch</i> in the tetrahydromethanopterin (H<sub>4</sub>MPT) pathway and <i>hgd</i> 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 H<sub>4</sub>MPT pathway that has primary importance. Studies on methylotrophy in <i>Methylobacterium</i> 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. |
| first_indexed | 2024-03-10T19:29:53Z |
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| language | English |
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| spelling | doaj.art-a29baabf46464a388d9b6c9ba79aaf102023-11-20T02:15:57ZengMDPI AGMicroorganisms2076-26072020-05-018682210.3390/microorganisms8060822Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22APatcha Yanpirat0Yukari Nakatsuji1Shota Hiraga2Yoshiko Fujitani3Terumi Izumi4Sachiko Masuda5Ryoji Mitsui6Tomoyuki Nakagawa7Akio Tani8Institute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanDepartment of Biochemistry, Faculty of Science, Okayama University of Science, Okayama 700-8530, JapanThe United Graduate School of Agricultural Science, Gifu University, Gifu 501-1193, JapanInstitute of Plant Science and Resources, Okayama University, Okayama 710-0046, JapanLanthanides (Ln) are an essential cofactor for XoxF-type methanol dehydrogenases (MDHs) in Gram-negative methylotrophs. The Ln<sup>3+</sup> 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 Ln<sup>3+</sup>- and Ca<sup>2+</sup>-dependent MDHs (XoxF1 and MxaFI), that are involved in methylotrophy, and an ExaF-type Ln<sup>3+</sup>-dependent ethanol dehydrogenase, among six MDH-like genes in <i>Methylobacterium aquaticum</i> strain 22A. We also identified the causative mutations in MxbD, a sensor kinase necessary for <i>mxaF</i> expression and <i>xoxF1</i> repression, for suppressive phenotypes in <i>xoxF1</i> mutants defective in methanol growth even in the absence of Ln<sup>3+</sup>. Furthermore, we examined the phenotypes of a series of formaldehyde oxidation-pathway mutants (<i>fae1</i>, <i>fae2</i>, <i>mch</i> in the tetrahydromethanopterin (H<sub>4</sub>MPT) pathway and <i>hgd</i> 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 H<sub>4</sub>MPT pathway that has primary importance. Studies on methylotrophy in <i>Methylobacterium</i> 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.https://www.mdpi.com/2076-2607/8/6/822lanthanidemethylotrophXoxFmethanol dehydrogenase<i>Methylobacterium</i> species |
| spellingShingle | Patcha Yanpirat Yukari Nakatsuji Shota Hiraga Yoshiko Fujitani Terumi Izumi Sachiko Masuda Ryoji Mitsui Tomoyuki Nakagawa Akio Tani Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A Microorganisms lanthanide methylotroph XoxF methanol dehydrogenase <i>Methylobacterium</i> species |
| title | Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A |
| title_full | Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A |
| title_fullStr | Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A |
| title_full_unstemmed | Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A |
| title_short | Lanthanide-Dependent Methanol and Formaldehyde Oxidation in <i>Methylobacterium aquaticum</i> Strain 22A |
| title_sort | lanthanide dependent methanol and formaldehyde oxidation in i methylobacterium aquaticum i strain 22a |
| topic | lanthanide methylotroph XoxF methanol dehydrogenase <i>Methylobacterium</i> species |
| url | https://www.mdpi.com/2076-2607/8/6/822 |
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