Lanpepsy is a novel lanthanide-binding protein involved in the lanthanide response of the obligate methylotroph Methylobacillus flagellatus

Hemmann, Jethro L.; Keller, Philipp; Hemmerle, Lucas; Vonderach, Thomas; Ochsner, Andrea M.; Bortfeld‐Miller, Miriam; Günther, Detlef; Vorholt, Julia A.

doi:10.1016/j.jbc.2023.102940

Cited by 13 publications

(11 citation statements)

References 59 publications

(92 reference statements)

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“…In addition, the Vorholt group recently discovered a 19‐kDa‐periplasmic protein, which contains two PepSY domains in Methylobacillus flagellatus . This protein is associated with lanthanide utilization and has been found to have multiple lanthanide binding sites that exhibit high selectivity for lanthanides over calcium ions (Hemmann et al, 2023). A homologous protein is encoded in the genome of strain CH1.…”

Section: Resultsmentioning

confidence: 99%

Active coexistence of the novel gammaproteobacterial methanotroph ‘Ca.Methylocalor cossyra’ CH1 and verrucomicrobial methanotrophs in acidic, hot geothermal soil

Liu,

Schmitz,

Pol

et al. 2024

Environmental Microbiology

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Terrestrial geothermal ecosystems are hostile habitats, characterized by large emissions of environmentally relevant gases such as CO2, CH4, H2S and H2. These conditions provide a niche for chemolithoautotrophic microorganisms. Methanotrophs of the phylum Verrucomicrobia, which inhabit these ecosystems, can utilize these gases and grow at pH levels below 1 and temperatures up to 65°C. In contrast, methanotrophs of the phylum Proteobacteria are primarily found in various moderate environments. Previously, novel verrucomicrobial methanotrophs were detected and isolated from the geothermal soil of the Favara Grande on the island of Pantelleria, Italy. The detection of pmoA genes, specific for verrucomicrobial and proteobacterial methanotrophs in this environment, and the partially overlapping pH and temperature growth ranges of these isolates suggest that these distinct phylogenetic groups could coexist in the environment. In this report, we present the isolation and characterization of a thermophilic and acid‐tolerant gammaproteobacterial methanotroph (family Methylococcaceae) from the Favara Grande. This isolate grows at pH values ranging from 3.5 to 7.0 and temperatures from 35°C to 55°C, and diazotrophic growth was demonstrated. Its genome contains genes encoding particulate and soluble methane monooxygenases, XoxF‐ and MxaFI‐type methanol dehydrogenases, and all enzymes of the Calvin cycle. For this novel genus and species, we propose the name ‘Candidatus Methylocalor cossyra’ CH1.

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Section: Resultsmentioning

confidence: 99%

Active coexistence of the novel gammaproteobacterial methanotroph ‘Ca.Methylocalor cossyra’ CH1 and verrucomicrobial methanotrophs in acidic, hot geothermal soil

Liu,

Schmitz,

Pol

et al. 2024

Environmental Microbiology

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“…Lanmodulin was the first known lanthanide-binding protein (except PQQ ADHs) (26). We meanwhile know three more: the periplasmic Ln-binding protein LutD; supposed to be associated with the LutAEF ABC transporter (27), a ubiquitin ligase from plant chloroplasts (30), and most recently lanpepsy (31) from Methylobacillus flagellatus . Lanmodulin is not essential for lanthanide-dependent methylotrophy in M. extorquens (25).…”

Section: Discussionmentioning

confidence: 99%

“…LanM is a homolog of the wellcharacterized calcium-binding protein calmodulin (26), which features high affinities for lanthanides and application potential for lanthanide detection and recovery (27)(28)(29). Few other lanthanide-binding proteins have been identified, including most recently lanpepsy from Methylobacillus flagellatus (27,30,31). Intracellular accumulation of lanthanides was shown for M. extorquens AM1 (25) and Beijerinckiaceae bacterium RH AL1 (32).…”

Section: Introductionmentioning

confidence: 99%

Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph

Gorniak

Bechwar

Westermann

et al. 2023

Preprint

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Lanthanides are the most recently described life metals and are central to methylotrophy in diverse taxa. We recently characterized a novel, lanthanide-dependent, and lanthanide-accumulating methylotroph, Beijerinckiaceae bacterium RH AL1, that utilizes lighter lanthanides (La, Ce, Nd) for methanol oxidation. We show that lanthanum concentration and different lanthanide (Ln) elements strongly affect gene expression and intracellular lanthanide accumulation. Differential gene expression analysis based on incubations with either La (50 nM or 1 µM), Nd (1 µM), or a lanthanide cocktail ([La, Ce, Nd, Dy, Ho, Er, Yb], equimolarly pooled, 1 µM), revealed that up to 41% of the encoded genes were differentially expressed. The effects of lanthanum concentration and Ln elements were not limited to lanthanide-dependent methanol oxidation but reached into many aspects of metabolism. We observed that lanthanides control the flagellar and chemotactic machinery and that they affect polyhydroxyalkanoate (PHA) biosynthesis. Secretion and various uptake systems, and carbohydrate metabolism were highly responsive. The most differentially expressed genes encode various unknown or hypothetical proteins, but alsolanM, coding for the well-characterized lanthanide-binding protein lanmodulin, and a glucose dehydrogenase gene linked to the conversion of β-D-glucose to gluconolactone, a known metal chelator. Electron microscopy, together with RNAseq, suggested different and potentially selective mechanisms for the uptake and accumulation of individual Ln elements. Mechanisms for discriminating lanthanides and links between lanthanides and various aspects of metabolism underline a broader functional role for lanthanides, possibly by functioning as calcium complements or antagonists.ImportanceSince its discovery, lanthanide-dependent metabolism in bacteria attracted a lot of attention due to its bio-metallurgical application potential regarding lanthanide recycling and circular economy. The physiological role of lanthanides is mostly studied dependent on presence and absence. Comparisons of how different (utilizable) lanthanides affect metabolism have rarely been done. Our research shows that strain RH AL1 distinguishes different lanthanide elements and that the effect of lanthanides reaches into many aspects of physiology, for instance, motility and polyhydroxyalkanoate metabolism. Numerous differentially expressed genes coding for unknown or hypothetical proteins might hide so far unknown lanthanide-binding proteins. Our findings regarding lanthanide accumulation suggest different mechanisms for dealing with individual lanthanide elements and provide insights relating to intracellular lanthanide homeostasis. Understanding comprehensively how microbes distinguish and handle different lanthanide elements is key for turning knowledge into application regarding lanthanide-centered biometallurgy.

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“…The characterized LanMs display a diversity of mechanisms to discriminate between light and heavy lanthanides, ,, including metal-sensitive dimerization, but share to-date unmatched, high affinity and selectivity for trivalent lanthanides and actinides. The relevance of LanMs and biomolecules with similar properties is underscored by the discovery of two other lanthanide-binding proteins , and the recent observation that Am 3+ , and to a lesser extent Cm 3+ , can activate the key bacterial lanthanide-dependent enzyme methanol dehydrogenase in vitro and in vivo on the basis of those elements’ similar ionic radii to Nd 3+ and Sm 3+ . Therefore, the unique metal-binding properties of the LanM family, other proteins, and peptides associated with lanthanide-dependent metabolism may play an important role in the partitioning of trivalent lanthanides and actinides in the environment.…”

Section: Introductionmentioning

confidence: 99%

Impact of a Biological Chelator, Lanmodulin, on Minor Actinide Aqueous Speciation and Transport in the Environment

Deblonde,

Morrison,

Mattocks

et al. 2023

Environ. Sci. Technol.

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Minor actinides are major contributors to the long-term radiotoxicity of nuclear fuels and other radioactive wastes. In this context, understanding their interactions with natural chelators and minerals is key to evaluating their transport behavior in the environment. The lanmodulin family of metalloproteins is produced by ubiquitous bacteria and Methylorubrum extorquens lanmodulin (LanM) was recently identified as one of nature’s most selective chelators for trivalent f-elements. Herein, we investigated the behavior of neptunium, americium, and curium in the presence of LanM, carbonate ions, and common minerals (calcite, montmorillonite, quartz, and kaolinite). We show that LanM’s aqueous complexes with Am(III) and Cm(III) remain stable in carbonate-bicarbonate solutions. Furthermore, the sorption of Am(III) to these minerals is strongly impacted by LanM, while Np(V) sorption is not. With calcite, even a submicromolar concentration of LanM leads to a significant reduction in the Am(III) distribution coefficient (K d, from >104 to ∼102 mL/g at pH 8.5), rendering it even more mobile than Np(V). Thus, LanM-type chelators can potentially increase the mobility of trivalent actinides and lanthanide fission products under environmentally relevant conditions. Monitoring biological chelators, including metalloproteins, and their biogenerators should therefore be considered during the evaluation of radioactive waste repository sites and the risk assessment of contaminated sites.

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Lanpepsy is a novel lanthanide-binding protein involved in the lanthanide response of the obligate methylotroph Methylobacillus flagellatus

Cited by 13 publications

References 59 publications

Active coexistence of the novel gammaproteobacterial methanotroph ‘Ca.Methylocalor cossyra’ CH1 and verrucomicrobial methanotrophs in acidic, hot geothermal soil

Active coexistence of the novel gammaproteobacterial methanotroph ‘Ca.Methylocalor cossyra’ CH1 and verrucomicrobial methanotrophs in acidic, hot geothermal soil

Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph

Impact of a Biological Chelator, Lanmodulin, on Minor Actinide Aqueous Speciation and Transport in the Environment

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