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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 circular plasmids PL6A (6,129 bp) and PL6B (6,056 bp).Predicted ORFs are labeled with their locus tags, and arrows represent their orientations and lengths. Nucleotide positions are given above each plasmid. Nucleotide similarity is indicated by the bar chart below the alignment (bar height and darkness of colour indicate the level of nucleotide identity, with solid black indicating 100% identity). The vertically oriented arrowhead at around 3.2 kb indicates a sharp break in homology. Percentage identity values of the corresponding protein sequences (in red) are given between ORFs in the alignment. H-T-H, helix-turn-helix protein domain. TM, transmembrane domain. Solid black arrowheads represent short repeat sequences (see text). The lowest panel shows the cumulative CT-skew plots of both sequences.
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pone-0020968-g003: Comparison of circular plasmids PL6A (6,129 bp) and PL6B (6,056 bp).Predicted ORFs are labeled with their locus tags, and arrows represent their orientations and lengths. Nucleotide positions are given above each plasmid. Nucleotide similarity is indicated by the bar chart below the alignment (bar height and darkness of colour indicate the level of nucleotide identity, with solid black indicating 100% identity). The vertically oriented arrowhead at around 3.2 kb indicates a sharp break in homology. Percentage identity values of the corresponding protein sequences (in red) are given between ORFs in the alignment. H-T-H, helix-turn-helix protein domain. TM, transmembrane domain. Solid black arrowheads represent short repeat sequences (see text). The lowest panel shows the cumulative CT-skew plots of both sequences.

Mentions: Genomic sequencing revealed that the PL6 plasmid band observed in C23T consists of two closely related plasmids, designated PL6A and PL6B. These were in approximately equal proportions in the population, as judged by restriction digests and sequenceing reads (data not shown). Their %G+C is significantly higher than that of the chromosome (51–52% versus 47.8%). They show high sequence identity, particularly over the first two ORFs, but this drops sharply at around 3.2 kb, (arrowed in Figure 3), following immediately after a motif consisting of two direct repeats of the sequence ACAGATTA bordered by an inverted repeat. Both plasmids have six predicted ORFs that show a similar organizational pattern. The corresponding ORFs between plasmids are predicted to code for proteins of similar size and amino acid sequence (Figure 3).


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 circular plasmids PL6A (6,129 bp) and PL6B (6,056 bp).Predicted ORFs are labeled with their locus tags, and arrows represent their orientations and lengths. Nucleotide positions are given above each plasmid. Nucleotide similarity is indicated by the bar chart below the alignment (bar height and darkness of colour indicate the level of nucleotide identity, with solid black indicating 100% identity). The vertically oriented arrowhead at around 3.2 kb indicates a sharp break in homology. Percentage identity values of the corresponding protein sequences (in red) are given between ORFs in the alignment. H-T-H, helix-turn-helix protein domain. TM, transmembrane domain. Solid black arrowheads represent short repeat sequences (see text). The lowest panel shows the cumulative CT-skew plots of both sequences.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3119063&req=5

pone-0020968-g003: Comparison of circular plasmids PL6A (6,129 bp) and PL6B (6,056 bp).Predicted ORFs are labeled with their locus tags, and arrows represent their orientations and lengths. Nucleotide positions are given above each plasmid. Nucleotide similarity is indicated by the bar chart below the alignment (bar height and darkness of colour indicate the level of nucleotide identity, with solid black indicating 100% identity). The vertically oriented arrowhead at around 3.2 kb indicates a sharp break in homology. Percentage identity values of the corresponding protein sequences (in red) are given between ORFs in the alignment. H-T-H, helix-turn-helix protein domain. TM, transmembrane domain. Solid black arrowheads represent short repeat sequences (see text). The lowest panel shows the cumulative CT-skew plots of both sequences.
Mentions: Genomic sequencing revealed that the PL6 plasmid band observed in C23T consists of two closely related plasmids, designated PL6A and PL6B. These were in approximately equal proportions in the population, as judged by restriction digests and sequenceing reads (data not shown). Their %G+C is significantly higher than that of the chromosome (51–52% versus 47.8%). They show high sequence identity, particularly over the first two ORFs, but this drops sharply at around 3.2 kb, (arrowed in Figure 3), following immediately after a motif consisting of two direct repeats of the sequence ACAGATTA bordered by an inverted repeat. Both plasmids have six predicted ORFs that show a similar organizational pattern. The corresponding ORFs between plasmids are predicted to code for proteins of similar size and amino acid sequence (Figure 3).

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