Discovery and characterization of the first known biological lanthanide chelator

Zytnick, Alexa M.; Good, Nathan; Barber, Colin; Phi, Manh Tri; Gutenthaler, Sophie M.; Zhang, Wenjun; Daumann, Lena J.; Martinez‐Gomez, N. Cecilia

doi:10.1101/2022.01.19.476857

Cited by 22 publications

(34 citation statements)

References 98 publications

(165 reference statements)

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“…Three of these genomes were Bacteroidetes, Sphingomonadales, Acidobacteria (group 1 Acidobacteriia) from the moderately weathered region and the other was for a Acidobacteria (group 4 Blastocatellia) from the soil. We did not observe any systems similar to the lanthanophore cluster of Methylorubum Extorquens AM1 (Zytnick et al 2022).…”

Section: Resultscontrasting

confidence: 55%

“…We also identified Acidobacteria genomes containing both XoxF3 and siderophores systems, although they were encoded in different genomic regions. Despite this, these siderophores may also assist in lanthanide solubilisation and uptake, given that the lanthanide chelation cluster (LCC) of Methylorubrum extorquens AM1 is located distantly from the XoxF machinery (Zytnick et al 2022). The observation of genomes containing siderophore-like BGCs without XoxF systems in our site raises the possibility that some bacteria promote lanthanide phosphate mineral dissolution to access phosphorus, a byproduct of which is the release of lanthanides.…”

Section: Discussionmentioning

confidence: 99%

“…Given that lanthanides in weathered granite are sequestered in highly insoluble minerals, theoretical considerations (Taunton, Welch, and Banfield 2000; Ochsner et al 2019) and recent experimental work (Zytnick et al 2022) suggest that specialised molecules such as siderophores may be required to induce lanthanide release. Siderophores are produced by biosynthetic gene clusters (BGCs) such as non-ribosomal peptide synthetases (NRPSs) and polyketide synthases (PKS) (Barry and Challis 2009).…”

Section: Introductionmentioning

confidence: 99%

“…This organism was shown to upregulate a Lanthanide Chelation Cluster (LCC) when supplied with poorly soluble Nd 2 O 3 in vitro. LCC encodes a NRPS biosynthetic gene cluster containing a TonB dependent receptor and synthesises an aerobactin-like siderophore (Zytnick et al 2022). This LCC is conserved across Methylobacterium species with some components present in other Alphaproteobacteria.…”

Section: Introductionmentioning

confidence: 99%

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Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

Voutsinos

West-Roberts

Sachdeva

et al. 2022

Preprint

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Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals is critical for the release of phosphate to the biosphere, yet the microorganisms involved, and the genes required for lanthanide metabolism, are poorly understood. Here, we sampled weathered granite and associated soil to identify the zones of lanthanide phosphate mineral solubilization and genomically define the organisms implicated in lanthanide utilisation. We reconstructed 136 genomes from 11 bacterial phyla and found gene clusters implicated in lanthanide-based metabolism of methanol (primarily XoxF3 and XoxF5) are surprisingly common in microbial communities in moderately weathered granite where lanthanide phosphate minerals are dissolving. Notably, XoxF3 systems were found in Verrucomicrobia for the first time, and in Acidobacteria, Gemmatimonadetes, and Alphaproteobacteria. The XoxF-containing gene clusters are shared by diverse Acidobacteria and Gemmatimonadetes, and include conserved hypothetical proteins and transporters not associated with the few well studied XoxF systems. Given that siderophore-like molecules that strongly bind lanthanides may be required to solubilize lanthanide phosphates, it is notable that candidate siderophore biosynthesis systems were most prevalent in bacteria in moderately weathered rock, especially in Acidobacteria with lanthanide-based systems. We conclude that the confluence in the zone of moderate weathering of phosphate mineral dissolution, lanthanide utilisation, and methanol oxidation (thus carbonic acid production) may be important during the conversion of granitic rock to soil.

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Section: Resultscontrasting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

Voutsinos

West-Roberts

Sachdeva

et al. 2022

Preprint

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“…This suggests that there are transcriptional modifications to reorganize the Ln transport machinery in evo -HLn with a stronger response for heavy Ln. Additionally, the gene cluster encoding a putative lanthanide chelator, known as the “lanthanide chelation cluster” (LCC), was upregulated in evo -HLn ( Zytnick et al, 2022 ), with the exception of genes 7 and 8 ( Figure 3A ). As seen with the lut genes, expression levels of this lanthanophore-encoding cluster were highest in evo -Gd.…”

Section: Resultsmentioning

confidence: 99%

Hyperaccumulation of Gadolinium by Methylorubrum extorquens AM1 Reveals Impacts of Lanthanides on Cellular Processes Beyond Methylotrophy

et al. 2022

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Lanthanides (Ln) are a new group of life metals, and many questions remain regarding how they are acquired and used in biology. Methylotrophic bacteria can acquire, transport, biomineralize, and use Ln as part of a cofactor complex with pyrroloquinoline quinone (PQQ) in alcohol dehydrogenases. For most methylotrophic bacteria use is restricted to the light Ln, which range from lanthanum to samarium (atomic numbers 57–62). Understanding how the cell differentiates between light and heavy Ln, and the impacts of these metals on the metabolic network, will advance the field of Ln biochemistry and give insights into enzyme catalysis, stress homeostasis, and metal biomineralization and compartmentalization. We report robust methanol growth with the heavy Ln gadolinium by a genetic variant of the model methylotrophic bacterium Methylorubrum extorquens AM1, named evo-HLn, for “evolved for Heavy Lanthanides.” A non-synonymous single nucleotide polymorphism in a cytosolic hybrid histidine kinase/response regulator allowed for sweeping transcriptional alterations to heavy metal stress response, methanol oxidation, and central metabolism. Increased expression of genes for Ln acquisition and uptake, production of the Ln-chelating lanthanophore, PQQ biosynthesis, and phosphate transport and metabolism resulted in gadolinium hyperaccumulation of 36-fold with a trade-off for light Ln accumulation. Gadolinium was hyperaccumulated in an enlarged acidocalcisome-like compartment. This is the first evidence of a bacterial intracellular Ln-containing compartment that we name the “lanthasome.” Carotenoid and toblerol biosynthesis were also upregulated. Due to its unique capabilities, evo-HLn can be used to further magnetic resonance imaging (MRI) and bioremediation technologies. In this regard, we show that gadolinium hyperaccumulation was sufficient to produce MRI contrast in whole cells, and that evo-HLn was able to readily acquire the metal from the MRI contrast agent gadopentetic acid. Finally, hyperaccumulation of gadolinium, differential uptake of light and heavy Ln, increased PQQ levels, and phosphate transport provide new insights into strategies for Ln recovery.

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Minor Actinides Can Replace Essential Lanthanides in Bacterial Life**

et al. 2023

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Certain f‐block elements—the lanthanides—have biological relevance in the context of methylotrophic bacteria. The respective strains incorporate these 4 f elements into the active site of one of their key metabolic enzymes, a lanthanide‐dependent methanol dehydrogenase. In this study, we investigated whether actinides, the radioactive 5 f elements, can replace the essential 4 f elements in lanthanide‐dependent bacterial metabolism. Growth studies with Methylacidiphilum fumariolicum SolV and the Methylobacterium extorquens AM1 ΔmxaF mutant demonstrate that americium and curium support growth in the absence of lanthanides. Moreover, strain SolV favors these actinides over late lanthanides when presented with a mixture of equal amounts of lanthanides together with americium and curium. Our combined in vivo and in vitro results establish that methylotrophic bacteria can utilize actinides instead of lanthanides to sustain their one‐carbon metabolism if they possess the correct size and a +III oxidation state.

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Discovery and characterization of the first known biological lanthanide chelator

Cited by 22 publications

References 98 publications

Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

Hyperaccumulation of Gadolinium by Methylorubrum extorquens AM1 Reveals Impacts of Lanthanides on Cellular Processes Beyond Methylotrophy

Minor Actinides Can Replace Essential Lanthanides in Bacterial Life**

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