Isolation and genomic characterization of<i>Novimethylophilus kurashikiensis</i>gen. nov. sp. nov., a new lanthanide‐dependent methylotrophic species of<i>Methylophilaceae</i>

Lv, Haoxin; Sahin, Nurettin; Tani, Akio

doi:10.1111/1462-2920.14062

Cited by 36 publications

(18 citation statements)

References 85 publications

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“…Since lanthanides are abundant in soil and sediment particles and all methanotrophs reported to date have XoxF-MDH (Keltjens et al, 2014), we assume the existence of lanthanide-dependent methanotrophs in moderate environments. This assumption is supported by previous findings on methanol-oxidizing bacteria (methylotrophs) that show lanthanide dependency (Skovran and Martinez-Gomez, 2015;Lv et al, 2018). Furthermore, the presence of lanthanide-dependent methanotrophs in moderate environments has been deduced from biogeochemical and molecular ecological studies.…”

supporting

confidence: 78%

“…3c). The full growth of strain Ce-a6 required a lower lanthanide concentration than that of the lanthanidedependent strains reported to date, i.e., the thermoacidophilic methanotroph M. fumariolicum SolV (>320 nM) (Pol et al, 2014) and the mesophilic methylotroph Novimethylophilus kurashikiensis La2-4 (>1,000 nM) (Lv et al, 2018). We also evaluated the lanthanide requirements of the type strain of M. sporium (strain DSM17706 T ), the closest relative of strain Ce-a6 (Fig.…”

Section: Growth Properties Of Isolated Methanotrophsmentioning

confidence: 99%

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Isolation and Genomic Characterization of a Proteobacterial Methanotroph Requiring Lanthanides

et al. 2020

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Although the bioavailability of rare earth elements (REEs, including scandium, yttrium, and 15 lanthanides) has not yet been examined in detail, methane-oxidizing bacteria (methanotrophs) were recently shown to harbor specific types of methanol dehydrogenases (XoxF-MDHs) that contain lanthanides in their active site, whereas their well-characterized counterparts (MxaF-MDHs) were Ca 2+-dependent. However, lanthanide dependency in methanotrophs has not been demonstrated, except in acidic environments in which the solubility of lanthanides is high. We herein report the isolation of a lanthanide-dependent methanotroph from a circumneutral environment in which lanthanides only slightly dissolved. Methanotrophs were enriched and isolated from pond sediment using mineral medium supplemented with CaCl 2 or REE chlorides. A methanotroph isolated from the cerium (Ce) chloride-supplemented culture, Methylosinus sp. strain Ce-a6, was clearly dependent on lanthanide. Strain Ce-a6 only required approximately 30 nM lanthanide chloride for its optimal growth and exhibited the ability to utilize insoluble lanthanide oxides, which may enable survival in circumneutral environments. Genome and gene expression analyses revealed that strain Ce-a6 lost the ability to produce functional MxaF-MDH, and this may have been due to a large-scale deletion around the mxa gene cluster. The present results provide evidence for lanthanide dependency as a novel survival strategy by methanotrophs in circumneutral environments.

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supporting

confidence: 78%

Section: Growth Properties Of Isolated Methanotrophsmentioning

confidence: 99%

Isolation and Genomic Characterization of a Proteobacterial Methanotroph Requiring Lanthanides

et al. 2020

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“…Notably, due to their low solubility in most natural environments, REEs have long been considered to have no biological function (Sarkar, 2002). However, the discovery of the wide-spread occurrence of the REE-dependent XoxF-type of PQQ-dependent methanol dehydrogenases (PQQ-MDHs), together with the more recent description of Ln 3+ -dependent ethanol dehydrogenases, has highlighted the important role of REEs for many bacterial species in various environmental compartments (Fitriyanto et al ., 2011a; Fushimi, et al, 2011; Pol et al, 2014; Taubert et al, 2015; Chu and Lidstrom, 2016; Good et al, 2016; Vekeman et al, 2016; Shiller et al, 2017; Wehrmann et al, 2017; Lv et al, 2018; Masuda et al, 2018). While in the absence of Ln 3+ the oxidation of methanol in methylotrophs is driven by Ca 2+ -dependent PQQ-MDHs (MxaF-type), the presence of low amounts of REE ions is usually sufficient to trigger a transcriptional switch to the XoxF-type of PQQ-MDHs.…”

Section: Introductionmentioning

confidence: 99%

The PedS2/PedR2 two-component system is crucial for the rare earth element switch in Pseudomonas putida KT2440

Wehrmann¹,

Berthelot

Billard

et al. 2018

Preprint

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In Pseudomonas putida KT2440, two pyrroloquinoline quinone-dependent ethanol dehydrogenases (PQQ-EDHs) are responsible for the periplasmic oxidation of a broad variety of volatile organic compounds (VOCs). Depending on the availability of rare earth elements (REEs) of the lanthanide series (Ln3+), we have recently described that the transcription of the genes encoding the Ca2+-utilizing enzyme PedE and the Ln3+-utilizing enzyme PedH are inversely regulated. With adaptive evolution experiments, site-specific mutations, transcriptional reporter fusions, and complementation approaches, we herein demonstrate that the PedS2/PedR2 (PP_2671/PP_2672) two-component system (TCS) plays a central role in the observed REE-mediated switch of PQQ-EDHs in P. putida. We provide evidence that in the absence of lanthanum (La3+), the sensor histidine kinase PedS2 phosphorylates its cognate LuxR-type response regulator PedR2, which in turn not only activates pedE gene transcription but is also involved in repression of pedH. Our data further suggests that the presence of La3+ lowers kinase activity of PedS2, either by the direct binding of the metal ions to the periplasmic region of PedS2 or by an uncharacterized indirect interaction, leading to reduced levels of phosphorylated PedR2. Consequently, the fading pedE expression and concomitant alleviation of pedH repression causes – in conjunction with the transcriptional activation of the pedH gene by a yet unknown regulatory module – the Ln3+-dependent transition from PedE to PedH catalysed oxidation of alcoholic VOCs.IMPORTANCEThe function of lanthanides for methano- and methylotrophic bacteria is gaining increasing attention, while knowledge about the role of rare earth elements (REEs) in non-methylotrophic bacteria is still limited. The present study investigates the recently described differential expression of the two PQQ-EDHs of P. putida in response to lanthanides. We demonstrate that a specific TCS is crucial for their inverse regulation and provide evidence for a dual regulatory function of the LuxR-type response regulator involved. Thus, our study represents the first detailed characterization of the molecular mechanism underlying the REE switch of PQQ-EDHs in a non-methylotrophic bacterium and stimulates subsequent investigations for the identification of additional genes or phenotypic traits that might be co-regulated during REE-dependent niche adaptation.

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“…The recent findings regarding the Ln 3+ dependency of XoxF have expanded our knowledge of methylotrophy and generated new questions. First, the wider distribution of xoxF in many bacterial genomes led to the discovery of new methylotrophs of novel genera [20][21][22] and the discovery that certain known microorganisms are methylotrophs [23,24]. Second, bacteria containing both MDHs, including strain AM1, exhibit a phenomenon called the "lanthanide switch".…”

Section: Introductionmentioning

confidence: 99%

Lanthanide-Dependent Methanol and Formaldehyde Oxidation in Methylobacterium aquaticum Strain 22A

et al. 2020

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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.

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Isolation and genomic characterization ofNovimethylophilus kurashikiensisgen. nov. sp. nov., a new lanthanide‐dependent methylotrophic species ofMethylophilaceae

Cited by 36 publications

References 85 publications

Isolation and Genomic Characterization of a Proteobacterial Methanotroph Requiring Lanthanides

Isolation and Genomic Characterization of a Proteobacterial Methanotroph Requiring Lanthanides

The PedS2/PedR2 two-component system is crucial for the rare earth element switch in Pseudomonas putida KT2440

Lanthanide-Dependent Methanol and Formaldehyde Oxidation in Methylobacterium aquaticum Strain 22A

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