• This record comes from PubMed

A novel in-silico model explores LanM homologs among Hyphomicrobium spp

. 2024 Nov 20 ; 7 (1) : 1539. [epub] 20241120

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
RGPIN-2020-05189 Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (NSERC Canadian Network for Research and Innovation in Machining Technology)

Links

PubMed 39562649
PubMed Central PMC11576760
DOI 10.1038/s42003-024-07258-3
PII: 10.1038/s42003-024-07258-3
Knihovny.cz E-resources

Investigating microorganisms in metal-enriched environments holds the potential to revolutionize the sustainable recovery of critical metals such as lanthanides (Ln3+). We observe Hyphomicrobium spp. as part of a Fe2+/Mn2+-oxidizing consortia native to the ferruginous bottom waters of a Ln3+-enriched lake in Czechia. Notably, one species shows similarities to recently discovered bacteria expressing proteins with picomolar Ln3+ affinity. This finding was substantiated by developing an in-silico ionic competition model and recombinant expression of a homolog protein (Hm-LanM) from Hyphomicrobium methylovorum. Biochemical assays validate Hm-LanM preference for lighter Ln3+ ions (from lanthanum to gadolinium). This is comparable to established prototypes. Bioinformatics analyses further uncover additional H. methylovorum metabolic biomolecules in genomic proximity to Hm-LanM analogously dependent on Ln3+, including an outer membrane receptor that binds Ln3+-chelating siderophores. These combined observations underscore the remarkable strategy of Hyphomicrobium spp. for thriving in relatively Ln3+ enriched zones of metal-polluted environments.

See more in PubMed

Ganguli, R. & Cook, D. R. Rare earths: a review of the landscape. MRS Energy Sustain.5, E9 (2018).

Ascenzi, P. et al. Rare earth elements (REE) in biology and medicine. Rend. Lincei Sci. Fis. Nat.31, 821–833 (2020).

U.S. Geological Survey. Mineral Commodity Summaries; 10.3133/mcs2021 (2021).

Dutta, T. et al. Global demand for rare earth resources and strategies for green mining. Environ. Res.150, 182–190 (2016). PubMed

Balaram, V. Rare earth elements: a review of applications, occurrence, exploration, analysis, recycling, and environmental impact. Geosci. Front.10, 1285–1303 (2019).

Deblonde, G. J.-P. et al. Impact of a biological chelator, lanmodulin, on minor actinide aqueous speciation and transport in the environment. Environ. Sci. Technol.57, 20830–20843 (2023). PubMed

Jung, H., Su, Z., Inaba, Y., West, A. C. & Banta, S. Genetic modification of Acidithiobacillus Ferrooxidans for rare-earth element recovery under acidic conditions. Environ. Sci. Technol.57, 19902–19911 (2023). PubMed

Ye, Q., Jin, X., Zhu, B., Gao, H. & Wei, N. Lanmodulin-functionalized magnetic nanoparticles as a highly selective biosorbent for recovery of rare earth elements. Environ. Sci. Technol.57, 4276–4285 (2023). PubMed

Cotruvo, J. A., Featherston, E. R., Mattocks, J. A., Ho, J. V. & Laremore, T. N. Lanmodulin: a highly selective lanthanide-binding protein from a lanthanide-utilizing bacterium. J. Am. Chem. Soc.140, 15056–15061 (2018). PubMed

Carl-Eric, W. et al. Extracellular and intracellular lanthanide accumulation in the methylotrophic Beijerinckiaceae bacterium RH AL1. Appl. Environ. Microbiol.87, e03144–20 (2021). PubMed PMC

Cook, E. C., Featherston, E. R., Showalter, S. A. & Cotruvo, J. A. Structural basis for rare earth element recognition by Methylobacterium Extorquens lanmodulin. Biochemistry58, 120–125 (2019). PubMed

Drake, S. K., Lee, K. L. & Falke, J. J. Tuning the equilibrium ion affinity and selectivity of the EF-hand calcium binding motif: substitutions at the gateway position. Biochemistry35, 6697–6705 (1996). PubMed

Veenstra, T. D., Gross, M. D., Hunziker, W. & Kumar, R. Identification of metal-binding sites in rat brain calcium-binding protein. J. Biol. Chem.270, 30353–30358 (1995). PubMed

Gutenthaler, S. M. et al. Lanmodulin peptides – unravelling the binding of the EF-hand loop sequences stripped from the structural corset. Inorg. Chem. Front9, 4009–4021 (2022). PubMed PMC

Mattocks, J. A. et al. Enhanced rare-earth separation with a metal-sensitive lanmodulin dimer. Nature618, 87–93 (2023). PubMed PMC

Featherston, E. R. & Cotruvo, J. A. The biochemistry of lanthanide acquisition, trafficking, and utilization. Biochim. Biophys. Acta Mol. Cell Res.1868, 118864 (2021). PubMed

Juma, P. O. et al. Siderophore for lanthanide and iron uptake for methylotrophy and plant growth promotion in Methylobacterium Aquaticum strain 22A. Front. Microbiol.13, 10.3389/fmicb.2022.921635 (2022). PubMed PMC

Sandy, M. & Butler, A. Microbial iron acquisition: marine and terrestrial siderophores. Chem. Rev.109, 4580–4595 (2009). PubMed PMC

Zytnick, A. M. et al. Identification and characterization of a small-molecule metallophore involved in lanthanide metabolism. Proc. Natl Acad. Sci.121, 10.1073/pnas.2322096121 (2024). PubMed PMC

Deng, Y. W., Ro, S. Y. & Rosenzweig, A. C. Structure and function of the lanthanide-dependent methanol dehydrogenase XoxF from the methanotroph Methylomicrobium Buryatense 5GB1C. J. Biol. Inorg. Chem.23, 1037–1047 (2018). PubMed PMC

Groom, J. D., Ford, S. M., Pesesky, M. W. & Lidstrom, M. E. A mutagenic screen identifies a TonB-dependent receptor required for the lanthanide metal switch in the type I methanotroph Methylotuvimicrobium Buryatense 5GB1C. J. Bacteriol.201, 10.1128/JB.00120-19 (2019). PubMed PMC

Ameyama, M., Matsushita, K., Shinagawa, E., Hayashi, M. & Adachi, O. Pyrroloquinoline quinone: excretion by methylotrophs and growth stimulation for microorganisms. Biofactors1, 51–53 (1988). PubMed

Lumpe, H. et al. The earlier the better: structural analysis and separation of lanthanides with pyrroloquinoline quinone. Chem. A Eur. J.26, 10133–10139 (2020). PubMed PMC

Pol, A. et al. Rare earth metals are essential for methanotrophic life in volcanic mudpots. Environ. Microbiol16, 255–264 (2014). PubMed

Shen, Y.-Q. et al. Distribution and properties of the genes encoding the biosynthesis of the bacterial cofactor, pyrroloquinoline quinone. Biochemistry51, 2265–2275 (2012). PubMed PMC

Teizi, U., Kazuya, Y., Hisao, K., Akio, Y. & Chieko, I.-Y. Production of pyrroloquinoline quinone by using methanol-utilizing bacteria. Appl. Environ. Microbiol.58, 3970–3976 (1992). PubMed PMC

Nealson, K. H. The manganese-oxidizing bacteria. In The Prokaryotes 222–231 (Springer New York: New York, NY, 2006).

Petrash, D. A. et al. Aqueous system-level processes and prokaryote assemblages in the ferruginous and sulfate-rich bottom waters of a post-mining lake. Biogeosciences19, 1723–1751 (2022).

Umbría-Salinas, K. et al. Redox-driven geochemical partitioning of metal(Loid)s in the iron-rich anoxic sediments of a recently flooded lignite mine pit: Lake Medard, NW Czechia. J. Hazard. Mater. Adv.3, 100009 (2021).

Garrity, G. M., Bell, J. A. & Lilburn, T. Class I. Alphaproteobacteria Class. Nov. in Bergey’s Manual® of Systematic Bacteriology 1–574 (Springer US: Boston, MA, 2005).

The Prokaryotes; (eds Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E., Thompson, F.) (Springer Berlin Heidelberg: Berlin, Heidelberg, 2014). 10.1007/978-3-642-30197-1.

Keltjens, J. T., Pol, A., Reimann, J. & Op den Camp, H. J. M. PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference. Appl. Microbiol. Biotechnol.98, 6163–6183 (2014). PubMed

Krause, S. M. B. et al. Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions. Proc. Natl Acad. Sci.114, 358–363 (2017). PubMed PMC

Picone, N. & Op den Camp, H. J. M. Role of rare earth elements in methanol oxidation. Curr. Opin. Chem. Biol.49, 39–44 (2019). PubMed

Tanaka, Y., Yoshida, T., Watanabe, K., Izumi, Y. & Mitsunaga, T. Cloning and analysis of methanol oxidation genes in the methylotroph Hyphomicrobium Methylovorum GM2. FEMS Microbiol. Lett.154, 397–401 (1997). PubMed

Palermo, C. & Dittrich, M. Evidence for the biogenic origin of manganese-enriched layers in lake superior sediments. Environ. Microbiol. Rep.8, 179–186 (2016). PubMed

He, S., Barco, R. A., Emerson, D. & Roden, E. E. Comparative genomic analysis of neutrophilic iron(II) oxidizer genomes for candidate genes in extracellular electron transfer. Front. Microbiol.8. 10.3389/fmicb.2017.01584 (2017). PubMed PMC

Cyriaque, V. et al. Metal-induced bacterial interactions promote diversity in river-sediment microbiomes. FEMS Microbiol. Ecol.9610.1093/femsec/fiaa076 (2020). PubMed

Planktonic 16S RRNA Data, Bottom Ferruginous/Sulfate-Rich Water Column of Lake Medard, NW Czechia [Data Set]. European Nucleotide Archive (EMBL-EBI)http://www.ebi.ac.uk/ena/browser/view/PRJEB47217 (2021).

Zhang, Z. et al. Protein sequence similarity searches using patterns as seeds. Nucleic Acids Res.26, 3986–3990 (1998). PubMed PMC

Petrash, D. A., Jan, J., Sirová, D., Osafo, N. O. A. & Borovec, J. Iron and nitrogen cycling, bacterioplankton community composition and mineral transformations involving phosphorus stabilisation in the ferruginous hypolimnion of a post-mining lake. Environ. Sci. Process Impacts20, 1414–1426 (2018). PubMed

Good, N. M. et al. Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function. J. Biol. Chem.295, 8272–8284 (2020). PubMed PMC

Chu, F. & Lidstrom, M. E. XoxF acts as the predominant methanol dehydrogenase in the type I methanotroph Methylomicrobium Buryatense. J. Bacteriol.198, 1317–1325 (2016). PubMed PMC

Schmitz, R. A. et al. Neodymium as metal cofactor for biological methanol oxidation: structure and kinetics of an XoxF1-type methanol dehydrogenase. mBio12, 10.1128/mBio.01708-21 (2021). PubMed PMC

Barona-Gómez, F., Wong, U., Giannakopulos, A. E., Derrick, P. J. & Challis, G. L. Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces Coelicolor M145. J. Am. Chem. Soc.126, 16282–16283 (2004). PubMed

Li, P., Song, L. F. & Merz, K. M. Jr. Parameterization of highly charged metal ions using the 12-6-4 LJ-type nonbonded model in explicit water. J. Phys. Chem. B119, 883–895 (2015). PubMed PMC

Li, P. Bridging the 12-6-4 model and the fluctuating charge model. Front. Chem.9, 721960 (2021). PubMed PMC

Li, Z., Song, L. F., Li, P. & Merz, K. M. Parametrization of trivalent and tetravalent metal ions for the OPC3, OPC, TIP3P-FB, and TIP4P-FB water models. J. Chem. Theory Comput.17, 2342–2354 (2021). PubMed PMC

Kojetin, D. J. et al. Structure, binding interface and hydrophobic transitions of Ca2+-loaded calbindin-D28K. Nat. Struct. Mol. Biol.13, 641–647 (2006). PubMed

Åkerfeldt, K. S., Coyne, A. N., Wilk, R. R., Thulin, E. & Linse, S. Ca2+-binding stoichiometry of calbindin D28k as assessed by spectroscopic analyses of synthetic peptide fragments. Biochemistry35, 3662–3669 (1996). PubMed

Huang, L. et al. 05SAR-PAGE: separation of protein dimerization and modification using a gel with 0.05% sarkosyl. Anal. Chim. Acta1101, 193–198 (2020). PubMed

Hanpaibool, C. et al. Pyrazolones potentiate colistin activity against MCR-1-producing resistant bacteria: computational and microbiological study. ACS Omega8, 8366–8376 (2023). PubMed PMC

Josts, I., Veith, K. & Tidow, H. Ternary structure of the outer membrane transporter FoxA with resolved signalling domain provides insights into TonB-mediated siderophore uptake. eLife8, e48528 (2019). PubMed PMC

Ohnuki, T., Kozai, N., Sakamoto, F., Suzuki, Y. & Yoshida, T. Biological change of chemical states of actinides and lanthanides-effects of organic acids. Energy Procedia39, 175–182 (2013).

Crocket, K. C. et al. Rare earth element distribution in the NE Atlantic: evidence for benthic sources, longevity of the seawater signal, and biogeochemical cycling. Front. Mar. Sci.5, 10.3389/fmars.2018.00147 (2018).

Catts, J. G. & Langmuir, D. Adsorption of Cu, Pb and Zn by ΔMnO2: applicability of the site binding-surface complexation model. Appl. Geochem.1, 255–264 (1986).

Valero, A., Jan, J. & Petrash, D. A. Anaerobic dissolved As(III) removal from metal-polluted waters by cathode-stabilized Fe(III)-oxyhydroxides. Environ. Sci.9, 454–466 (2023).

Hao, X. et al. Recent advances in exploring the heavy metal(loid) resistant microbiome. Comput. Struct. Biotechnol. J.19, 94–109 (2021). PubMed PMC

Tostevin, R. et al. Low-oxygen waters limited habitable space for early animals. Nat. Commun.7, 12818 (2016). PubMed PMC

Moore, R. L. The biology of hyphomicrobium and other prosthecate, budding bacteria. Annu. Rev. Microbiol.35, 567–594 (1981). PubMed

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol.35, 1547–1549 (2018). PubMed PMC

Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol.4, 406–425 (1987). PubMed

Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution39, 783 (1985). PubMed

Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol.16, 111–120 (1980). PubMed

Madhavi Sastry, G., Adzhigirey, M., Day, T., Annabhimoju, R. & Sherman, W. Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J. Comput. Aided Mol. Des.27, 221–234 (2013). PubMed

Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys.79, 926–935 (1983).

Mahoney, M. W. & Jorgensen, W. L. A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J. Chem. Phys.112, 8910–8922 (2000).

Maier, J. A. et al. Ff14SB: improving the accuracy of protein side chain and backbone parameters from Ff99SB. J. Chem. Theory Comput.11, 3696–3713 (2015). PubMed PMC

Li, P., Song, L. F. & Merz, K. M. Systematic parameterization of monovalent ions employing the nonbonded model. J. Chem. Theory Comput.11, 1645–1657 (2015). PubMed

Li, P., Roberts, B. P., Chakravorty, D. K. & Merz, K. M. Rational design of particle mesh ewald compatible lennard-jones parameters for +2 metal cations in explicit solvent. J. Chem. Theory Comput.9, 2733–2748 (2013). PubMed PMC

Bowers, K. J. et al. Scalable algorithms for molecular dynamics simulations on commodity clusters. In SC ’06: Proc. 2006 ACM/IEEE Conference on Supercomputing, 43 (ACM/IEEE: Tampa, FL, USA, 2006).

Evans, D. J. & Holian, B. L. The Nose–Hoover thermostat. J. Chem. Phys.83, 4069–4074 (1985).

Martyna, G. J., Tobias, D. J. & Klein, M. L. Constant pressure molecular dynamics algorithms. J. Chem. Phys.101, 4177–4189 (1994).

Tuckerman, M., Berne, B. J. & Martyna, G. J. Reversible multiple time scale molecular dynamics. J. Chem. Phys.97, 1990–2001 (1992).

Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph.14, 33–38 (1996). PubMed

Almagro Armenteros, J. J. et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol.37, 420–423 (2019). PubMed

Huang, Y., Niu, B., Gao, Y., Fu, L. & Li, W. CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics26, 680–682 (2010). PubMed PMC

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc.10, 845–858 (2015). PubMed PMC

Grosdidier, A., Zoete, V. & Michielin, O. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res39, W270–W277 (2011). PubMed PMC

Irwin, J. J. & Shoichet, B. K. ZINC − a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model.45, 177–182 (2005). PubMed PMC

Huang, J. & MacKerell, A. D. Jr. CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data. J. Comput. Chem.34, 2135–2145 (2013). PubMed PMC

Zoete, V., Cuendet, M. A., Grosdidier, A. & Michielin, O. SwissParam: a fast force field generation tool for small organic molecules. J. Comput. Chem.32, 2359–2368 (2011). PubMed

Li, J. Gmxtools. 10.5281/zenodo.6408973 (2022).

Guy, L., Roat Kultima, J. & Andersson, S. G. E. GenoPlotR: comparative gene and genome visualization in R. Bioinformatics26, 2334–2335 (2010). PubMed PMC

Crooks, G. E., Hon, G., Chandonia, J.-M. & Brenner, S. E. WebLogo: a sequence logo generator: Fig. 1. Genome Res.14, 1188–1190 (2004). PubMed PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...