skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae

Journal Article · · BMC Genomics
 [1];  [2];  [3];  [3];  [4];  [5];  [6];  [7];  [8]
  1. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biology
  2. Univ. of Toronto, ON (Canada). Dept. of Cell and Systems Biology
  3. Georgia Inst. of Technology, Atlanta, GA (United States). School of Civil and Environmental Engineering
  4. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
  5. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  6. Univ. of Toronto, ON (Canada). Dept. of Chemical Engineering and Applied Chemistry
  7. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biology; Georgia Inst. of Technology, Atlanta, GA (United States). School of Civil and Environmental Engineering
  8. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Civil and Environmental Engineering
+ Show Author Affiliations

Background: Geobacter lovleyi is a unique member of the Geobacteraceae because strains of this species share the ability to couple tetrachloroethene (PCE) reductive dechlorination to cis-1,2-dichloroethene (cis-DCE) with energy conservation and growth (i.e., organohalide respiration). Strain SZ also reduces U(VI) to U(IV) and contributes to uranium immobilization, making G. lovleyi relevant for bioremediation at sites impacted with chlorinated ethenes and radionuclides. G. lovleyi is the only fully sequenced representative of this distinct Geobacter clade, and comparative genome analyses identified genetic elements associated with organohalide respiration and elucidated genome features that distinguish strain SZ from other members of the Geobacteraceae. Results: Sequencing the G. lovleyi strain SZ genome revealed a 3.9 Mbp chromosome with 54.7% GC content (i.e., the percent of the total guanines (Gs) and cytosines (Cs) among the four bases within the genome), and average amino acid identities of 53–56% compared to other sequenced Geobacter spp. Sequencing also revealed the presence of a 77 kbp plasmid, pSZ77 (53.0% GC), with nearly half of its encoded genes corresponding to chromosomal homologs in other Geobacteraceae genomes. Among these chromosome-derived features, pSZ77 encodes 15 out of the 24 genes required for de novo cobalamin biosynthesis, a required cofactor for organohalide respiration. A plasmid with 99% sequence identity to pSZ77 was subsequently detected in the PCE-dechlorinating G. lovleyi strain KB-1 present in the PCE-to-ethene-dechlorinating consortium KB-1. Additional PCE-to-cis-DCE dechlorinating G. lovleyi strains obtained from the PCE-contaminated Fort Lewis, WA, site did not carry a plasmid indicating that pSZ77 is not a requirement (marker) for PCE respiration within this species. Chromosomal genomic islands found within the G. lovleyi strain SZ genome encode two reductive dehalogenase (RDase) homologs and a putative conjugative pilus system. Despite the loss of many c-type cytochrome and oxidative-stress-responsive genes, strain SZ retained the majority of Geobacter core metabolic capabilities, including U(VI) respiration. Conclusions: Gene acquisitions have expanded strain SZ’s respiratory capabilities to include PCE and TCE as electron acceptors. Respiratory processes core to the Geobacter genus, such as metal reduction, were retained despite a substantially reduced number of c-type cytochrome genes. pSZ77 is stably maintained within its host strains SZ and KB-1, likely because the replicon carries essential genes including genes involved in cobalamin biosynthesis and possibly corrinoid transport. Lateral acquisition of the plasmid replicon and the RDase genomic island represent unique genome features of the PCE-respiring G. lovleyi strains SZ and KB-1, and at least the latter signifies adaptation to PCE contamination.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1626415
Journal Information:
BMC Genomics, Vol. 13, Issue 1; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English

References (80)

Functional characterization of the trigger factor protein PceT of tetrachloroethene-dechlorinating Desulfitobacterium hafniense Y51 journal April 2009
Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens journal December 2005
Biosynthesis of cobalamin (vitamin B12) journal August 2002
Stimulating the In Situ Activity of Geobacter Species To Remove Uranium from the Groundwater of a Uranium-Contaminated Aquifer journal October 2003
Mechanisms that Contribute to the Stable Segregation of Plasmids journal December 1989
E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI) journal January 2008
Comparative genomic analysis of Polypodiaceae chloroplasts reveals fine structural features and dynamic insertion sequences journal January 2021
Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens: c-type cytochrome accumulates at the electrode surface journal August 2010
Nitrate reduction by Desulfovibrio desulfuricans : A periplasmic nitrate reductase system that lacks NapB, but includes a unique tetraheme c -type cytochrome, NapM journal July 2005
A Comparative Categorization of Protein Function Encoded in Bacterial or Archeal Genomic Islands journal December 2005
Ascorbic acid-induced loss of a pediocin-encoding plasmid in Pediococcus acidilactici CFR K7 journal January 2000
Circular genome visualization and exploration using CGView journal October 2004
Extracellular electron transfer: wires, capacitors, iron lungs, and more journal June 2008
Role of the Extracytoplasmic Function Protein Family Sigma Factor RpoE in Metal Resistance of Escherichia coli journal March 2005
Characterization of Two Tetrachloroethene-Reducing, Acetate-Oxidizing Anaerobic Bacteria and Their Description as Desulfuromonas michiganensis sp. nov journal May 2003
Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments journal December 2003
Characterization and Description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an Aryl-Halorespiring Facultative Anaerobic Myxobacterium journal February 2002
The genome of Geobacter bemidjiensis, exemplar for the subsurface clade of Geobacter species that predominate in Fe(III)-reducing subsurface environments. journal January 2010
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Complete reductive dechlorination of 1,2-dichloropropane by anaerobic bacteria journal July 1997
Diversity of geobacteraceae species inhabiting metal-polluted freshwater lake sediments ascertained by 16S rDNA analyses journal August 2003
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation journal October 2006
Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides: Quantitative PCR of dechlorinating cultures journal December 2006
Site-Specific Mobilization of Vinyl Chloride Respiration Islands by a Mechanism Common in Dehalococcoides journal June 2011
REPuter: the manifold applications of repeat analysis on a genomic scale journal November 2001
Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes journal January 2010
Ori-Finder: A web-based system for finding oriC s in unannotated bacterial genomes journal February 2008
Assay, purification, and characterization of cobaltochelatase, a unique complex enzyme catalyzing cobalt insertion in hydrogenobyrinic acid a,c-diamide during coenzyme B12 biosynthesis in Pseudomonas denitrificans. journal November 1992
Enrichment, Cultivation, and Detection of Reductively Dechlorinating Bacteria book January 2005
Spatial and Temporal Distributions of Geobacter lovleyi and Dehalococcoides spp. during Bioenhanced PCE-NAPL Dissolution journal March 2009
Geobacter lovleyi sp. nov. Strain SZ, a Novel Metal-Reducing and Tetrachloroethene-Dechlorinating Bacterium journal April 2006
Molecular archaeology of the Escherichia coli genome journal August 1998
The genome sequence of Geobacter metallireducens: features of metabolism, physiology and regulation common and dissimilar to Geobacter sulfurreducens journal January 2009
Extracellular electron transfer via microbial nanowires journal June 2005
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis journal January 2009
Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid journal April 2010
Electron donor availability for microbial reductive processes following thermal treatment journal December 2011
Plasmids isolated from marine sediment microbial communities contain replication and incompatibility regions unrelated to those of known plasmid groups journal March 1997
The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-Proteobacteria journal May 2008
Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation journal May 2008
Isolation of Geobacter species from diverse sedimentary environments. journal January 1996
A sand fly salivary protein acts as a neutrophil chemoattractant journal May 2021
Quantifying expression of Geobacter spp. oxidative stress genes in pure culture and during in situ uranium bioremediation journal January 2009
Characterization of a Highly Enriched Dehalococcoides-Containing Culture That Grows on Vinyl Chloride and Trichloroethene journal September 2004
Isolation and characterization of Tn-Dha1, a transposon containing the tetrachloroethene reductive dehalogenase of Desulfitobacterium hafniense strain TCE1 journal January 2005
GenomeViz: visualizing microbial genomes journal January 2004
Comparative genomics of the pIPO2/pSB102 family of environmental plasmids: sequence, evolution, and ecology of pTer331 isolated from Collimonas fungivorans Ter331: Plasmid pTer331 isolated from Collimonas fungivorans Ter331 journal October 2008
Basic local alignment search tool journal October 1990
Fate of TCE in Heated Fort Lewis Soil journal February 2009
MUSCLE: a multiple sequence alignment method with reduced time and space complexity journal August 2004
Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 journal October 2010
Influence of Vitamin B12 and Cocultures on the Growth of Dehalococcoides Isolates in Defined Medium journal March 2007
Interaction of the Initiator Protein DnaA of Escherichia coli with Its DNA Target journal July 1995
The partition system of multidrug resistance plasmid TP228 includes a novel protein that epitomizes an evolutionarily distinct subgroup of the ParA superfamily: Multidrug resistance plasmid partition journal August 2000
Geobacter daltonii sp. nov., an Fe(III)- and uranium(VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination journal August 2009
Replication and Control of Circular Bacterial Plasmids journal June 1998
Localized Plasticity in the Streamlined Genomes of Vinyl Chloride Respiring Dehalococcoides journal November 2009
Characterization of Metabolism in the Fe(III)-Reducing Organism Geobacter sulfurreducens by Constraint-Based Modeling journal February 2006
Evolution from a respiratory ancestor to fill syntrophic and fermentative niches: comparative fenomics of six Geobacteraceae species journal January 2009
Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins journal July 1995
Biochemical and molecular characterization of a tetrachloroethene dechlorinating Desulfitobacterium sp. strain Y51: a review journal June 2005
Factors affecting the isolation of CCC DNA from Streptomyces lividans and Escherichia coli journal July 1984
TonB-dependent receptors—structural perspectives journal October 2002
F factor conjugation is a true type IV secretion system journal July 2003
Isolation and curing of the Klebsiella pneumoniae large indigenous plasmid using sodium dodecyl sulphate journal April 2000
Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism journal September 2011
Plasmid P1 RepA Is Homologous to the F Plasmid RepE Class of Initiators journal November 2003
Dehalogenase genes of Pseudomonas putida PP3 on chromosomally located transposable elements. journal November 1985
Novel Plasmid-Encoded Ceftazidime-Hydrolyzing CTX-M-53 Extended-Spectrum β-Lactamase from Salmonella enterica Serotypes Westhampton and Senftenberg journal March 2009
Graphite Electrode as a Sole Electron Donor for Reductive Dechlorination of Tetrachlorethene by Geobacter lovleyi journal July 2008
Effects of Chloromethanes on Growth of and Deletion of the pce Gene Cluster in Dehalorespiring Desulfitobacterium hafniense Strain Y51 journal September 2006
Detection and Quantification of Geobacter lovleyi Strain SZ: Implications for Bioremediation at Tetrachloroethene- and Uranium-Impacted Sites journal September 2007
Unique Ecophysiology among U(VI)-Reducing Bacteria as Revealed by Evaluation of Oxygen Metabolism in Anaeromyxobacter dehalogenans Strain 2CP-C journal November 2009
Unusual Codon Bias in Vinyl Chloride Reductase Genes of Dehalococcoides Species journal February 2007
Reductive Dehalogenation of Trichloroacetic Acid byTrichlorobacter thiogenes gen. nov., sp. nov journal June 2000
Characterization of the Corrinoid Iron-Sulfur Protein Tetrachloroethene Reductive Dehalogenase of Dehalobacter restrictus journal August 2003
Interactions in the TonB-Dependent Energy Transduction Complex: ExbB and ExbD Form Homomultimers journal November 1998
Functional and Mutational Analysis of Conjugative Transfer Region 2 (Tra2) from the IncHI1 Plasmid R27 journal January 2003
Cytochrome bd Oxidase, Oxidative Stress, and Dioxygen Tolerance of the Strictly Anaerobic Bacterium Moorella thermoacetica journal March 2005
DNA Microarray and Proteomic Analyses of the RpoS Regulon in Geobacter sulfurreducens journal April 2006

Cited By (18)

An integrative overview of genomic, transcriptomic and proteomic analyses in organohalide respiration research journal January 2018
Identification of a multi-protein reductive dehalogenase complex in D ehalococcoides mccartyi strain CBDB1 suggests a protein-dependent respiratory electron transport chain obviating quinone involvement : Respiratory reductive dehalogenase protein complex journal February 2016
Metabolic versatility of toluene-degrading, iron-reducing bacteria in tidal flat sediment, characterized by stable isotope probing-based metagenomic analysis: Metagenomic analysis of toluene-degrading bacteria journal October 2013
Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases journal April 2013
Functional Characterization of Reductive Dehalogenases by Using Blue Native Polyacrylamide Gel Electrophoresis journal November 2012
Identity and Substrate Specificity of Reductive Dehalogenases Expressed in Dehalococcoides-Containing Enrichment Cultures Maintained on Different Chlorinated Ethenes journal May 2015
Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site journal August 2013
A genomic approach to the cryptic secondary metabolome of the anaerobic world journal January 2013
Comparative c-type cytochrome expression analysis in Shewanella oneidensis strain MR-1 and Anaeromyxobacter dehalogenans strain 2CP-C grown with soluble and insoluble oxidized metal electron acceptors journal November 2012
Identification of bacterial communities in sediments of Poyang Lake, the largest freshwater lake in China journal April 2016
Metagenome phylogenetic profiling of microbial community evolution in a tetrachloroethene-contaminated aquifer responding to enhanced reductive dechlorination protocols journal December 2016
Biodegradation of Volatile Organic Compounds and Their Effects on Biodegradability under Co-Existing Conditions journal January 2017
Ecogenomics of microbial communities in bioremediation of chlorinated contaminated sites journal January 2012
Functional genomics of corrinoid starvation in the organohalide-respiring bacterium Dehalobacter restrictus strain PER-K23 journal January 2015
Corrigendum: Diversity of reductive dehalogenase genes from environmental samples and enrichment cultures identified with degenerate primer PCR screens journal February 2015
Indirect Evidence Link PCB Dehalogenation with Geobacteraceae in Anaerobic Sediment-Free Microcosms journal June 2016
Functional Genes and Bacterial Communities During Organohalide Respiration of Chloroethenes in Microcosms of Multi-Contaminated Groundwater journal February 2019
A widely distributed metalloenzyme class enables gut microbial metabolism of host- and diet-derived catechols journal February 2020

Similar Records

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biotechnology & Applied Microbiology
Genetics & Heredity