Genomic determinants of organohalide-respiration in <it>Geobacter lovleyi</it>, an unusual member of the <it>Geobacteraceae</it>

<p>Abstract</p> <p>Background</p> <p><it>Geobacter lovleyi</it> is a unique member of the <it>Geobacteraceae</it> because strains of this species share the ability to couple tetrachloroethene (PCE) reductive dechlorination to <it>cis</it>-1,2-dichloroethene (<it>cis</it>-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 <it>G. lovleyi</it> relevant for bioremediation at sites impacted with chlorinated ethenes and radionuclides. <it>G. lovleyi</it> is the only fully sequenced representative of this distinct <it>Geobacter</it> 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 <it>Geobacteraceae</it>.</p> <p>Results</p> <p>Sequencing the <it>G. lovleyi</it> 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 <it>Geobacter</it> 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 <it>Geobacteraceae</it> genomes. Among these chromosome-derived features, pSZ77 encodes 15 out of the 24 genes required for <it>de novo</it> cobalamin biosynthesis, a required cofactor for organohalide respiration. A plasmid with 99% sequence identity to pSZ77 was subsequently detected in the PCE-dechlorinating <it>G. lovleyi</it> strain KB-1 present in the PCE-to-ethene-dechlorinating consortium KB-1. Additional PCE-to-<it>cis</it>-DCE-dechlorinating <it>G. lovleyi</it> 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 <it>G. lovleyi</it> strain SZ genome encode two reductive dehalogenase (RDase) homologs and a putative conjugative pilus system. Despite the loss of many <it>c</it>-type cytochrome and oxidative-stress-responsive genes, strain SZ retained the majority of <it>Geobacter</it> core metabolic capabilities, including U(VI) respiration.</p> <p>Conclusions</p> <p>Gene acquisitions have expanded strain SZ’s respiratory capabilities to include PCE and TCE as electron acceptors. Respiratory processes core to the <it>Geobacter</it> genus, such as metal reduction, were retained despite a substantially reduced number of <it>c</it>-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 <it>G. lovleyi</it> strains SZ and KB-1, and at least the latter signifies adaptation to PCE contamination.</p>