Metallomics of two microorganisms relevant to heavy metal bioremediation reveal fundamental differences in metal assimilation and utilization

Lancaster, Andrew; Menon, Angeli; Scott, Israel; Poole, Farris; Vaccaro, Brian; Thorgersen, Michael P.; Geller, Jil; Hazen, Terry C.; Brown, Steven D.; Elias, Dwayne A.; Adams, Michael W. W.

doi:10.1039/c4mt00050a

Title: Metallomics of two microorganisms relevant to heavy metal bioremediation reveal fundamental differences in metal assimilation and utilization

Journal Article · Wed Mar 26 00:00:00 EDT 2014 · Metallomics

DOI:https://doi.org/10.1039/c4mt00050a· OSTI ID:1129620

Lancaster, Andrew ^[1]; Menon, Angeli ^[1]; Scott, Israel ^[1]; Poole, Farris ^[1]; Vaccaro, Brian ^[1]; Thorgersen, Michael P. ^[1]; Geller, Jil ^[2]; Hazen, Terry C. ^[3]; Brown, Steven D. ^[4]; Elias, Dwayne A. ^[4]; Adams, Michael W. W. ^[1]

Univ. of Georgia, Athens, GA (United States)
Lawrence Berkeley National Laboratory (LBNL)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Although as many as half of all proteins are thought to require a metal cofactor, the metalloproteomes of microorganisms remain relatively unexplored. Microorganisms from different environments are likely to vary greatly in the metals that they assimilate, not just among the metals with well-characterized roles but also those lacking any known function. Herein we investigated the metal utilization of two microorganisms that were isolated from very similar environments and are of interest because of potential roles in the immobilization of heavy metals, such as uranium and chromium. The metals assimilated and their concentrations in the cytoplasm of Desulfovibrio vulgaris strain Hildenborough (DvH) and Enterobacter cloacae strain Hanford (EcH) varied dramatically, with a larger number of metals present in Enterobacter. For example, a total of 9 and 19 metals were assimilated into their cytoplasmic fractions, respectively, and DvH did not assimilate significant amounts of zinc or copper whereas EcH assimilated both. However, bioinformatic analysis of their genome sequences revealed a comparable number of predicted metalloproteins, 813 in DvH and 953 in EcH. These allowed some rationalization of the types of metal assimilated in some cases (Fe, Cu, Mo, W, V) but not in others (Zn, Nd, Ce, Pr, Dy, Hf and Th). It was also shown that U binds an unknown soluble protein in EcH but this incorporation was the result of extracellular U binding to cytoplasmic components after cell lysis.

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: AC05-00OR22725

OSTI ID:: 1129620

Journal Information:: Metallomics, Vol. 6, Issue 5; ISSN 1756-5901

Publisher:: Royal Society of Chemistry

Country of Publication:: United States

Language:: English

References (32)

Hazards of heavy metal contamination Järup, Lars British Medical Bulletin, Vol. 68, Issue 1 https://doi.org/10.1093/bmb/ldg032	journal	December 2003
Effect of sulfide on growth physiology and gene expression of Desulfovibrio vulgaris Hildenborough Caffrey, Sean M.; Voordouw, Gerrit Antonie van Leeuwenhoek, Vol. 97, Issue 1 https://doi.org/10.1007/s10482-009-9383-y	journal	October 2009
Genomic Diversity within the Enterobacter cloacae Complex Paauw, Armand; Caspers, Martien P. M.; Schuren, Frank H. J. PLoS ONE, Vol. 3, Issue 8 https://doi.org/10.1371/journal.pone.0003018	journal	August 2008
Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria B., Chardin; A., Dolla; F., Chaspoul Applied Microbiology and Biotechnology, Vol. 60, Issue 3 https://doi.org/10.1007/s00253-002-1091-8	journal	November 2002
Cr(VI) detoxification by Desulfovibrio vulgaris strain Hildenborough: microbe–metal interactions studies Goulhen, Florence; Gloter, Alexandre; Guyot, Francois Applied Microbiology and Biotechnology, Vol. 71, Issue 6 https://doi.org/10.1007/s00253-005-0211-7	journal	November 2005
A Computational Framework for Proteome-Wide Pursuit and Prediction of Metalloproteins using ICP-MS and MS/MS Data Lancaster, W. Andrew; Praissman, Jeremy L.; Poole, Farris L. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-64	journal	February 2011
Temporal Transcriptomic Analysis as Desulfovibrio vulgaris Hildenborough Transitions into Stationary Phase during Electron Donor Depletion Clark, M. E.; He, Q.; He, Z. Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/AEM.00284-06	journal	August 2006
InterProScan - an integration platform for the signature-recognition methods in InterPro Zdobnov, E. M.; Apweiler, R. Bioinformatics, Vol. 17, Issue 9, p. 847-848 https://doi.org/10.1093/bioinformatics/17.9.847	journal	September 2001
Spatial and temporal dynamics of the microbial community in the Hanford unconfined aquifer Lin, Xueju; McKinley, James; Resch, Charles T. The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.26	journal	March 2012
Hexavalent chromium reduction in Desulfovibrio vulgaris Hildenborough causes transitory inhibition of sulfate reduction and cell growth Klonowska, A.; Clark, M. E.; Thieman, S. B. Applied Microbiology and Biotechnology, Vol. 78, Issue 6 https://doi.org/10.1007/s00253-008-1381-x	journal	February 2008
Complete genome of the onion pathogen Enterobacter cloacae EcWSU1 Humann, Jodi L.; Wildung, Mark; Cheng, Chun-Huai Standards in Genomic Sciences, Vol. 5, Issue 3 https://doi.org/10.4056/sigs.2174950	journal	December 2011
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Expression profiling of hypothetical genes in Desulfovibrio vulgaris leads to improved functional annotation Elias, Dwayne A.; Mukhopadhyay, Aindrila; Joachimiak, Marcin P. Nucleic Acids Research, Vol. 37, Issue 9 https://doi.org/10.1093/nar/gkp164	journal	March 2009
Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance Mezzatesta, Maria Lina; Gona, Floriana; Stefani, Stefania Future Microbiology, Vol. 7, Issue 7 https://doi.org/10.2217/fmb.12.61	journal	July 2012
Uranium Reduction Wall, Judy D.; Krumholz, Lee R. Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121357	journal	October 2006
Hydrogenases in sulfate-reducing bacteria function as chromium reductase Chardin, B.; Giudici-Orticoni, M. -T.; De Luca, G. Applied Microbiology and Biotechnology, Vol. 63, Issue 3 https://doi.org/10.1007/s00253-003-1390-8	journal	July 2003
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life Pol, Arjan; Barends, Thomas R. M.; Dietl, Andreas Environmental Microbiology, Vol. 16, Issue 1 https://doi.org/10.1111/1462-2920.12249	journal	September 2013
The Three-Dimensional Structure of [NiFeSe] Hydrogenase from Desulfovibrio vulgaris Hildenborough: A Hydrogenase without a Bridging Ligand in the Active Site in Its Oxidised, “as-Isolated” State Marques, Marta C.; Coelho, Ricardo; De Lacey, Antonio L. Journal of Molecular Biology, Vol. 396, Issue 4 https://doi.org/10.1016/j.jmb.2009.12.013	journal	March 2010
Microbial Community Succession during Lactate Amendment and Electron Acceptor Limitation Reveals a Predominance of Metal-Reducing Pelosinus spp. Mosher, Jennifer J.; Phelps, Tommy J.; Podar, Mircea Applied and Environmental Microbiology, Vol. 78, Issue 7 https://doi.org/10.1128/AEM.07165-11	journal	January 2012
How Saccharomyces cerevisiae copes with toxic metals and metalloids Wysocki, Robert; Tamás, Markus J. FEMS Microbiology Reviews, Vol. 34, Issue 6 https://doi.org/10.1111/j.1574-6976.2010.00217.x	journal	November 2010
Characterization and activity studies of highly heavy metal resistant sulphate-reducing bacteria to be used in acid mine drainage decontamination Martins, Mónica; Faleiro, M. Leonor; Barros, Raúl J. Journal of Hazardous Materials, Vol. 166, Issue 2-3 https://doi.org/10.1016/j.jhazmat.2008.11.088	journal	July 2009
Tungsten in biological systems Kletzin, Arnulf; Adams, Michael W. W. FEMS Microbiology Reviews, Vol. 18, Issue 1 https://doi.org/10.1111/j.1574-6976.1996.tb00226.x	journal	March 1996
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface Zhang, Weiwen; Culley, David E.; Nie, Lei Applied Microbiology and Biotechnology, Vol. 76, Issue 2 https://doi.org/10.1007/s00253-007-1014-9	journal	June 2007
Tungsten and Molybdenum Regulation of Formate Dehydrogenase Expression in Desulfovibrio vulgaris Hildenborough da Silva, S. M.; Pimentel, C.; Valente, F. M. A. Journal of Bacteriology, Vol. 193, Issue 12 https://doi.org/10.1128/JB.00042-11	journal	April 2011
A sulfate-reducing bacterium that can detoxify U(VI) and obtain energy via nitrate reduction Pietzsch, Katja; Babel, Wolfgang Journal of Basic Microbiology, Vol. 43, Issue 4 https://doi.org/10.1002/jobm.200390038	journal	August 2003
The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough Heidelberg, John F.; Seshadri, Rekha; Haveman, Shelley A. Nature Biotechnology, Vol. 22, Issue 5 https://doi.org/10.1038/nbt959	journal	April 2004
Ferric iron reduction by Desulfovibrio vulgaris Hildenborough wild type and energy metabolism mutants Park, Hyung Soo; Lin, Shiping; Voordouw, Gerrit Antonie van Leeuwenhoek, Vol. 93, Issue 1-2 https://doi.org/10.1007/s10482-007-9181-3	journal	June 2007
Performance comparison of benchtop high-throughput sequencing platforms Loman, Nicholas J.; Misra, Raju V.; Dallman, Timothy J. Nature Biotechnology, Vol. 30, Issue 5 https://doi.org/10.1038/nbt.2198	journal	April 2012
Microbial metalloproteomes are largely uncharacterized Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P. Nature, Vol. 466, Issue 7307 https://doi.org/10.1038/nature09265	journal	July 2010
Reduction of molybdate by sulfate-reducing bacteria Biswas, Keka C.; Woodards, Nicole A.; Xu, Huifang BioMetals, Vol. 22, Issue 1 https://doi.org/10.1007/s10534-008-9198-8	journal	January 2009
Global Transcriptional, Physiological, and Metabolite Analyses of the Responses of Desulfovibrio vulgaris Hildenborough to Salt Adaptation He, Z.; Zhou, A.; Baidoo, E. Applied and Environmental Microbiology, Vol. 76, Issue 5 https://doi.org/10.1128/AEM.02141-09	journal	December 2009

Similar Records

Microbial metalloproteomes are largely uncharacterized

Journal Article · Sun Jul 18 00:00:00 EDT 2010 · Nature (London) · OSTI ID:1129620

Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P.; +14 more

Fractionation of sulfur isotopes by Desulfovibrio vulgaris mutants lacking hydrogenases or type I tetraheme cytochrome c3

Journal Article · Tue Jan 01 00:00:00 EST 2013 · Frontiers in Microbiology · OSTI ID:1129620

Sim, Min Sub; Wang, David T.; Zane, Grant M.; +3 more

The Role of the Tetraheme Cytochrome c3 in Desulfovibrio vulgaris Hildenborough Metabolism

Technical Report · Mon May 17 00:00:00 EDT 2010 · OSTI ID:1129620

Semkiw, Elizabeth; Zane, Grant; Wall, Judy

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Title: Metallomics of two microorganisms relevant to heavy metal bioremediation reveal fundamental differences in metal assimilation and utilization

Citation Formats

References (32)

Similar Records

Related Subjects