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Haloquadratum walsbyi: limited diversity in a global pond.

Dyall-Smith ML, Pfeiffer F, Klee K, Palm P, Gross K, Schuster SC, Rampp M, Oesterhelt D - PLoS ONE (2011)

Bottom Line: Strain C23(T) carries two ∼6 kb plasmids that show similarity to halovirus His1 and to sequences nearby halovirus/plasmid gene clusters commonly found in haloarchaea.Change is also driven by mobile genetic elements but these do not by themselves explain the atypically low gene coding density found in this species.The remarkable genome conservation despite the presence of active systems for genome rearrangement implies both an efficient global dispersal system, and a high selective fitness for this species.

View Article: PubMed Central - PubMed

Affiliation: Department of Membrane Biochemistry, Max-Planck-Institute of Biochemistry, Martinsried, Germany. mdyall-smith@csu.edu.au

ABSTRACT

Background: Haloquadratum walsbyi commonly dominates the microbial flora of hypersaline waters. Its cells are extremely fragile squares requiring >14%(w/v) salt for growth, properties that should limit its dispersal and promote geographical isolation and divergence. To assess this, the genome sequences of two isolates recovered from sites at near maximum distance on Earth, were compared.

Principal findings: Both chromosomes are 3.1 MB in size, and 84% of each sequence was highly similar to the other (98.6% identity), comprising the core sequence. ORFs of this shared sequence were completely synteneic (conserved in genomic orientation and order), without inversion or rearrangement. Strain-specific insertions/deletions could be precisely mapped, often allowing the genetic events to be inferred. Many inferred deletions were associated with short direct repeats (4-20 bp). Deletion-coupled insertions are frequent, producing different sequences at identical positions. In cases where the inserted and deleted sequences are homologous, this leads to variant genes in a common synteneic background (as already described by others). Cas/CRISPR systems are present in C23(T) but have been lost in HBSQ001 except for a few spacer remnants. Numerous types of mobile genetic elements occur in both strains, most of which appear to be active, and with some specifically targetting others. Strain C23(T) carries two ∼6 kb plasmids that show similarity to halovirus His1 and to sequences nearby halovirus/plasmid gene clusters commonly found in haloarchaea.

Conclusions: Deletion-coupled insertions show that Hqr. walsbyi evolves by uptake and precise integration of foreign DNA, probably originating from close relatives. Change is also driven by mobile genetic elements but these do not by themselves explain the atypically low gene coding density found in this species. The remarkable genome conservation despite the presence of active systems for genome rearrangement implies both an efficient global dispersal system, and a high selective fitness for this species.

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Comparison of the chromosomes of Hqr. walsbyi strains C23T and HBSQ001.Panel A: Mummer nucleotide alignment, where dots indicate similar sequences in the same orientation (red), or reverse orientation (blue), shared by the two strains. Panels B and D: Tetra-nucleotide variation (TETRA) along the chromosomal sequences of each strain (labeled). Several divergent regions in each plot are labeled in both panels (see text). The %G+C deviation (if a 1 kb window is more than 2.5 SD from the average) is given for HBSQ001 immediately below the panel TETRA plot of panel D. Panel C: comparison of the chromosomal sequences using the Artemis comparison tool (ACT). Red lines indicate regions of high nucleotide similarity; white regions indicate lack of similarity. Above this plot regions of major divergence (DV 1-12) are indicated (and also on the Mummer plot in panel A), while below the previously described genomic islands (GI 1-4 [13]) are indicated. Panel E: Cumulative GC-skew plots for the chromosomes of C23T (red) and HBSQ001 (black). The boxed region extending upwards to panel D outlines the major drop in the cumulative skew plot of HBSQ001.
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pone-0020968-g005: Comparison of the chromosomes of Hqr. walsbyi strains C23T and HBSQ001.Panel A: Mummer nucleotide alignment, where dots indicate similar sequences in the same orientation (red), or reverse orientation (blue), shared by the two strains. Panels B and D: Tetra-nucleotide variation (TETRA) along the chromosomal sequences of each strain (labeled). Several divergent regions in each plot are labeled in both panels (see text). The %G+C deviation (if a 1 kb window is more than 2.5 SD from the average) is given for HBSQ001 immediately below the panel TETRA plot of panel D. Panel C: comparison of the chromosomal sequences using the Artemis comparison tool (ACT). Red lines indicate regions of high nucleotide similarity; white regions indicate lack of similarity. Above this plot regions of major divergence (DV 1-12) are indicated (and also on the Mummer plot in panel A), while below the previously described genomic islands (GI 1-4 [13]) are indicated. Panel E: Cumulative GC-skew plots for the chromosomes of C23T (red) and HBSQ001 (black). The boxed region extending upwards to panel D outlines the major drop in the cumulative skew plot of HBSQ001.

Mentions: The constant horizontal axis in all cases is the genome from left to right (first to last base of deposited sequence), with a scale given in Mbp. From top to bottom are plots of: (a) %G+C if the deviation for a 1 kb window is more than 2.5 SD from the average, (b) protein-coding pseudogenes (vertical triangles), excluding those of transposases, (c) variation in tetramer nucleotide composition (TETRA), where darker colors indicated more prominent deviation, (d) GC-profile, (e) cumulative GC-skew, (f) positions and orientations of the following gene categories: CDC6, orc1/cdc6 homologues; tRNA, transfer RNA genes; rRNA, ribosomal RNA operons; r-Prot, ribosomal protein genes; RNAP, RNA polymerase subunit genes; CRISPR, loci of clustered regularly interspersed short palindromic repeats. Smaller, unfilled arrowheads in the CDC6 line represent the positions of cdc6 pseudogenes. DV6 (divergent region 6, see Figure 5) is indicated below the cumulative GC-skew plot. Vertical grey-shaded stripes mark correlating features.


Haloquadratum walsbyi: limited diversity in a global pond.

Dyall-Smith ML, Pfeiffer F, Klee K, Palm P, Gross K, Schuster SC, Rampp M, Oesterhelt D - PLoS ONE (2011)

Comparison of the chromosomes of Hqr. walsbyi strains C23T and HBSQ001.Panel A: Mummer nucleotide alignment, where dots indicate similar sequences in the same orientation (red), or reverse orientation (blue), shared by the two strains. Panels B and D: Tetra-nucleotide variation (TETRA) along the chromosomal sequences of each strain (labeled). Several divergent regions in each plot are labeled in both panels (see text). The %G+C deviation (if a 1 kb window is more than 2.5 SD from the average) is given for HBSQ001 immediately below the panel TETRA plot of panel D. Panel C: comparison of the chromosomal sequences using the Artemis comparison tool (ACT). Red lines indicate regions of high nucleotide similarity; white regions indicate lack of similarity. Above this plot regions of major divergence (DV 1-12) are indicated (and also on the Mummer plot in panel A), while below the previously described genomic islands (GI 1-4 [13]) are indicated. Panel E: Cumulative GC-skew plots for the chromosomes of C23T (red) and HBSQ001 (black). The boxed region extending upwards to panel D outlines the major drop in the cumulative skew plot of HBSQ001.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3119063&req=5

pone-0020968-g005: Comparison of the chromosomes of Hqr. walsbyi strains C23T and HBSQ001.Panel A: Mummer nucleotide alignment, where dots indicate similar sequences in the same orientation (red), or reverse orientation (blue), shared by the two strains. Panels B and D: Tetra-nucleotide variation (TETRA) along the chromosomal sequences of each strain (labeled). Several divergent regions in each plot are labeled in both panels (see text). The %G+C deviation (if a 1 kb window is more than 2.5 SD from the average) is given for HBSQ001 immediately below the panel TETRA plot of panel D. Panel C: comparison of the chromosomal sequences using the Artemis comparison tool (ACT). Red lines indicate regions of high nucleotide similarity; white regions indicate lack of similarity. Above this plot regions of major divergence (DV 1-12) are indicated (and also on the Mummer plot in panel A), while below the previously described genomic islands (GI 1-4 [13]) are indicated. Panel E: Cumulative GC-skew plots for the chromosomes of C23T (red) and HBSQ001 (black). The boxed region extending upwards to panel D outlines the major drop in the cumulative skew plot of HBSQ001.
Mentions: The constant horizontal axis in all cases is the genome from left to right (first to last base of deposited sequence), with a scale given in Mbp. From top to bottom are plots of: (a) %G+C if the deviation for a 1 kb window is more than 2.5 SD from the average, (b) protein-coding pseudogenes (vertical triangles), excluding those of transposases, (c) variation in tetramer nucleotide composition (TETRA), where darker colors indicated more prominent deviation, (d) GC-profile, (e) cumulative GC-skew, (f) positions and orientations of the following gene categories: CDC6, orc1/cdc6 homologues; tRNA, transfer RNA genes; rRNA, ribosomal RNA operons; r-Prot, ribosomal protein genes; RNAP, RNA polymerase subunit genes; CRISPR, loci of clustered regularly interspersed short palindromic repeats. Smaller, unfilled arrowheads in the CDC6 line represent the positions of cdc6 pseudogenes. DV6 (divergent region 6, see Figure 5) is indicated below the cumulative GC-skew plot. Vertical grey-shaded stripes mark correlating features.

Bottom Line: Strain C23(T) carries two ∼6 kb plasmids that show similarity to halovirus His1 and to sequences nearby halovirus/plasmid gene clusters commonly found in haloarchaea.Change is also driven by mobile genetic elements but these do not by themselves explain the atypically low gene coding density found in this species.The remarkable genome conservation despite the presence of active systems for genome rearrangement implies both an efficient global dispersal system, and a high selective fitness for this species.

View Article: PubMed Central - PubMed

Affiliation: Department of Membrane Biochemistry, Max-Planck-Institute of Biochemistry, Martinsried, Germany. mdyall-smith@csu.edu.au

ABSTRACT

Background: Haloquadratum walsbyi commonly dominates the microbial flora of hypersaline waters. Its cells are extremely fragile squares requiring >14%(w/v) salt for growth, properties that should limit its dispersal and promote geographical isolation and divergence. To assess this, the genome sequences of two isolates recovered from sites at near maximum distance on Earth, were compared.

Principal findings: Both chromosomes are 3.1 MB in size, and 84% of each sequence was highly similar to the other (98.6% identity), comprising the core sequence. ORFs of this shared sequence were completely synteneic (conserved in genomic orientation and order), without inversion or rearrangement. Strain-specific insertions/deletions could be precisely mapped, often allowing the genetic events to be inferred. Many inferred deletions were associated with short direct repeats (4-20 bp). Deletion-coupled insertions are frequent, producing different sequences at identical positions. In cases where the inserted and deleted sequences are homologous, this leads to variant genes in a common synteneic background (as already described by others). Cas/CRISPR systems are present in C23(T) but have been lost in HBSQ001 except for a few spacer remnants. Numerous types of mobile genetic elements occur in both strains, most of which appear to be active, and with some specifically targetting others. Strain C23(T) carries two ∼6 kb plasmids that show similarity to halovirus His1 and to sequences nearby halovirus/plasmid gene clusters commonly found in haloarchaea.

Conclusions: Deletion-coupled insertions show that Hqr. walsbyi evolves by uptake and precise integration of foreign DNA, probably originating from close relatives. Change is also driven by mobile genetic elements but these do not by themselves explain the atypically low gene coding density found in this species. The remarkable genome conservation despite the presence of active systems for genome rearrangement implies both an efficient global dispersal system, and a high selective fitness for this species.

Show MeSH
Related in: MedlinePlus