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Cited by 27

The DOI matches its Crossref record; 78 of the 78 references it cites were found in a registry or an index.

Sister Dehalobacter Genomes Reveal Specialization in Organohalide Respiration and Recent Strain Differentiation Likely Driven by Chlorinated Substrates

Tang, Shuiquan, Wang, Po Hsiang, Higgins, Steven A., Löffler, Frank E., Edwards, Elizabeth A.·2016·Frontiers in Microbiology
DOI 10.3389/fmicb.2016.00100PMC PMC4751268
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Abstract

The genomes of two closely related Dehalobacter strains (strain CF and strain DCA) were assembled from the metagenome of an anaerobic enrichment culture that reductively dechlorinates chloroform (CF), 1,1,1-trichloroethane (1,1,1-TCA) and 1,1-dichloroethane (1,1-DCA). The 3.1 Mbp genomes of strain CF (that dechlorinates CF and 1,1,1-TCA) and strain DCA (that dechlorinates 1,1-DCA) each contain 17 putative reductive dehalogenase homologous (rdh) genes. These two genomes were systematically compared to three other available organohalide-respiring Dehalobacter genomes (Dehalobacter restrictus strain PER-K23, Dehalobacter sp. strain E1 and Dehalobacter sp. strain UNSWDHB), and to the genomes of Dehalococcoides mccartyi strain 195 and Desulfitobacterium hafniense strain Y51. This analysis compared 42 different metabolic and physiological categories. The genomes of strains CF and DCA share 90% overall average nucleotide identity and >99.8% identity over a 2.9 Mbp alignment that excludes large insertions, indicating that these genomes differentiated from a close common ancestor. This differentiation was likely driven by selection pressures around two orthologous reductive dehalogenase genes, cfrA and dcrA, that code for the enzymes that reduce CF or 1,1,1-TCA and 1,1-DCA. The many reductive dehalogenase genes found in the five Dehalobacter genomes cluster into two small conserved regions and were often associated with Crp/Fnr transcriptional regulators. Specialization is on-going on a strain-specific basis, as some strains but not others have lost essential genes in the Wood-Ljungdahl (strain E1) and corrinoid biosynthesis pathways (strains E1 and PER-K23). The gene encoding phosphoserine phosphatase, which catalyzes the last step of serine biosynthesis, is missing from all five Dehalobacter genomes, yet D. restrictus can grow without serine, suggesting an alternative or unrecognized biosynthesis route exists. In contrast to D. mccartyi, a complete heme biosynthesis pathway is present in the five Dehalobacter genomes. This pathway corresponds to a newly described alternative heme biosynthesis route first identified in Archaea. This analysis of organohalide-respiring Firmicutes and Chloroflexi reveals profound evolutionary differences despite very similar niche-specific metabolism and function.

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Crossref · 10.3389/fmicb.2016.00100

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Figures

Figure 1 Circular Genome map of Dehalobacter sp. strain CF outlining major features and relationship to strains DCA, UNSW, PER-K23, and E1. The gray bars (labeled A, B, C, and D, ring 13) highlight some variable regions and the two blue bars, ring 13, hightlight the two rdhA clusters.
Figure 1 Circular Genome map of Dehalobacter sp. strain CF outlining major features and relationship to strains DCA, UNSW, PER-K23, and E1. The gray bars (labeled A, B, C, and D, ring 13) highlight some variable regions and the two blue bars, ring 13, hightlight the two rdhA clusters.CC BY · PubMed Central
Figure 2 Whole genome alignment of strains CF and DCA. Sequence discrepancies are highlighted in black (compared to light gray) in the aligned sequences; this is a feature common to all sequence alignments presented in this paper. Blue blocks highlight three major regions of sequence variations: A1/A2, B1/B2, and C1/C2, with size and G+C content in parentheses. Red triangles represent strain-specific insertion sequences. Two arrows show the loci of cfrA and dcrA. The two genomes have a nucleotide identity of ~90% in this alignment.
Figure 2 Whole genome alignment of strains CF and DCA. Sequence discrepancies are highlighted in black (compared to light gray) in the aligned sequences; this is a feature common to all sequence alignments presented in this paper. Blue blocks highlight three major regions of sequence variations: A1/A2, B1/B2, and C1/C2, with size and G+C content in parentheses. Red triangles represent strain-specific insertion sequences. Two arrows show the loci of cfrA and dcrA. The two genomes have a nucleotide identity of ~90% in this alignment.CC BY · PubMed Central
Figure 3 Sequence alignments of the cfrA and dcrA gene neighborhoods. The alignment is represented by two horizontal bars where light gray means that the residue at the position is the same in both sequences while black indicates substitutions. All coding sequences (CDSs) are indicated as directional blocks in different colors: rdhA genes (yellow), rdhB genes (green), pceC-like genes (purple), crp/fnr transcriptional regulators (red), ISs (light blue) and others (gray). The pairs of numbers in parentheses below are the counts of synonymous and non-synonymous substitutions (total 30 and 97, respectively).
Figure 3 Sequence alignments of the cfrA and dcrA gene neighborhoods. The alignment is represented by two horizontal bars where light gray means that the residue at the position is the same in both sequences while black indicates substitutions. All coding sequences (CDSs) are indicated as directional blocks in different colors: rdhA genes (yellow), rdhB genes (green), pceC-like genes (purple), crp/fnr transcriptional regulators (red), ISs (light blue) and others (gray). The pairs of numbers in parentheses below are the counts of synonymous and non-synonymous substitutions (total 30 and 97, respectively).CC BY · PubMed Central
Figure 4 Three potential genome rearrangements between Dehalobacter restrictus strain PER-K23 and Dehalobacter sp. strain CF. Note the blocks with identical color represent corresponding areas between the genomes of strain CF and strain PER-K23 with high similarity. Panel (A) shows the Mauve alignment and original GC skew profile of the two genomes. Panels (B–D) represent the 3-step artificial reversion scenario that could explain the genome rearrangements observed between the two strains. Steps 1 and 2 in Panels (B, C) describe two sequence inversions, and step 3 in Panel (D) represents a translocation. The resulting changes in Mauve alignments are depicted with corresponding changes in GC skew profiles shown to the right.
Figure 4 Three potential genome rearrangements between Dehalobacter restrictus strain PER-K23 and Dehalobacter sp. strain CF. Note the blocks with identical color represent corresponding areas between the genomes of strain CF and strain PER-K23 with high similarity. Panel (A) shows the Mauve alignment and original GC skew profile of the two genomes. Panels (B–D) represent the 3-step artificial reversion scenario that could explain the genome rearrangements observed between the two strains. Steps 1 and 2 in Panels (B, C) describe two sequence inversions, and step 3 in Panel (D) represents a translocation. The resulting changes in Mauve alignments are depicted with corresponding changes in GC skew profiles shown to the right.CC BY · PubMed Central
Figure 5 Schematic of the central carbon metabolism and corrinoid/heme biosynthesis of Dehalobacter sp. strain CF inferred from genome annotation. Enzymes involved in the reactions are listed below with full name and gene locus_tags from strain CF: PK, pyruvate kinase, p653; PPDK, pyruvate, phosphate dikinase, p2541; FDH, formate dehydrogenase, p924-927; FHL, formate hydrogenlyase, p760-766; ACS, acetate:CoA ligase (AMP-forming), p435; PFL, pyruvate formate-lyase, p2283 + p2284; PFO, pyruvate-flavodoxin oxidoreductase, p269 or p2740; PCT, pyruvate carboxyl transferase, p2314; NDME, NADP-dependent malic enzyme, p397; CS, citrate synthase (si), p2711 or p2808; AH, aconitate hydratase, p995; ICDH, isocitrate dehydrogenase [NADP], p1096; 2-OGs, 2-oxoglutarate:ferredoxin oxidoreductase, p978-981; SCL, succinate:CoA ligase, p393 + p395; FH, fumarate hydratase, p2651 + p2652; SMHT, serine hydroxymethyltransferase, p2888. A red X on a pathway means the gene for the enzyme is not found. GK, glucokinase; OAD, oxaloacetate decarboxylase; PSPH, phosphoserine phosphatase; SDH, succinate dehydrogenase; MDH, malate dehydrogenase; ICL, isocitrate lyase; MS, malate synthase; TAL, threonine aldolase.
Figure 5 Schematic of the central carbon metabolism and corrinoid/heme biosynthesis of Dehalobacter sp. strain CF inferred from genome annotation. Enzymes involved in the reactions are listed below with full name and gene locus_tags from strain CF: PK, pyruvate kinase, p653; PPDK, pyruvate, phosphate dikinase, p2541; FDH, formate dehydrogenase, p924-927; FHL, formate hydrogenlyase, p760-766; ACS, acetate:CoA ligase (AMP-forming), p435; PFL, pyruvate formate-lyase, p2283 + p2284; PFO, pyruvate-flavodoxin oxidoreductase, p269 or p2740; PCT, pyruvate carboxyl transferase, p2314; NDME, NADP-dependent malic enzyme, p397; CS, citrate synthase (si), p2711 or p2808; AH, aconitate hydratase, p995; ICDH, isocitrate dehydrogenase [NADP], p1096; 2-OGs, 2-oxoglutarate:ferredoxin oxidoreductase, p978-981; SCL, succinate:CoA ligase, p393 + p395; FH, fumarate hydratase, p2651 + p2652; SMHT, serine hydroxymethyltransferase, p2888. A red X on a pathway means the gene for the enzyme is not found. GK, glucokinase; OAD, oxaloacetate decarboxylase; PSPH, phosphoserine phosphatase; SDH, succinate dehydrogenase; MDH, malate dehydrogenase; ICL, isocitrate lyase; MS, malate synthase; TAL, threonine aldolase.CC BY · PubMed Central
Figure 6 Schematic of the metabolic defects in amino acid biosynthesis of Dehalobacter sp. strain CF inferred from genome annotation. THF, tetrahydrofolate; 5,10-MTHF, 5,10- methylene-tetrahydrofolate. A red X on a pathway means the gene encoding the enzyme was not found. The Figure shows that either glycine, cysteine, or serine is needed because all other routes for serine biosynthesis are missing.
Figure 6 Schematic of the metabolic defects in amino acid biosynthesis of Dehalobacter sp. strain CF inferred from genome annotation. THF, tetrahydrofolate; 5,10-MTHF, 5,10- methylene-tetrahydrofolate. A red X on a pathway means the gene encoding the enzyme was not found. The Figure shows that either glycine, cysteine, or serine is needed because all other routes for serine biosynthesis are missing.CC BY · PubMed Central

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Cites

Research works printed but not linked: 3

  1. Drummond, 2011, Geneious v5.4.2
  2. Tang, 2014, Investigation of Dehalobacter-Containing Cultures that Reductively Dechlorinate Chloroform and 1,1,1-Trichloroethane (Doctoral dissertation)
  3. Ward, 2010, In situ Remediation of Chlorinated Solvent Plumes. SERDP and ESTCP Remediation Technology Monograph Series.

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Metadata

Authors
Tang, S., Wang, P. H., Higgins, S. A., Löffler, F. E., & Edwards, E. A.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2016-02-12
Volume
7
ISSN
1664-302X
DOI
10.3389/fmicb.2016.00100
PMC
PMC4751268
Cited by
27
References
78
Funders
Genome Canada (2009-OGI-ABC-1405)

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