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Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response.

Becker EA, Seitzer PM, Tritt A, Larsen D, Krusor M, Yao AI, Wu D, Madern D, Eisen JA, Darling AE, Facciotti MT - PLoS Genet. (2014)

Bottom Line: We challenge a recent high-profile proposal regarding the evolutionary origins of the haloarchaea by showing that inclusion of additional genomes significantly reduces support for a proposed large-scale horizontal gene transfer into the ancestral haloarchaeon from the bacterial domain.The combination of broad (17 genera) and deep (≥5 species in four genera) sampling of a phenotypically unified clade has enabled us to uncover both highly conserved and specialized features of osmoadaptation.Finally, we demonstrate the broad utility of such datasets, for metagenomics, improvements to automated gene annotation and investigations of evolutionary processes.

View Article: PubMed Central - PubMed

Affiliation: Microbiology Graduate Group, University of California, Davis, Davis, California, United States of America; Genome Center, University of California, Davis, Davis, California, United States of America.

ABSTRACT
Organisms across the tree of life use a variety of mechanisms to respond to stress-inducing fluctuations in osmotic conditions. Cellular response mechanisms and phenotypes associated with osmoadaptation also play important roles in bacterial virulence, human health, agricultural production and many other biological systems. To improve understanding of osmoadaptive strategies, we have generated 59 high-quality draft genomes for the haloarchaea (a euryarchaeal clade whose members thrive in hypersaline environments and routinely experience drastic changes in environmental salinity) and analyzed these new genomes in combination with those from 21 previously sequenced haloarchaeal isolates. We propose a generalized model for haloarchaeal management of cytoplasmic osmolarity in response to osmotic shifts, where potassium accumulation and sodium expulsion during osmotic upshock are accomplished via secondary transport using the proton gradient as an energy source, and potassium loss during downshock is via a combination of secondary transport and non-specific ion loss through mechanosensitive channels. We also propose new mechanisms for magnesium and chloride accumulation. We describe the expansion and differentiation of haloarchaeal general transcription factor families, including two novel expansions of the TATA-binding protein family, and discuss their potential for enabling rapid adaptation to environmental fluxes. We challenge a recent high-profile proposal regarding the evolutionary origins of the haloarchaea by showing that inclusion of additional genomes significantly reduces support for a proposed large-scale horizontal gene transfer into the ancestral haloarchaeon from the bacterial domain. The combination of broad (17 genera) and deep (≥5 species in four genera) sampling of a phenotypically unified clade has enabled us to uncover both highly conserved and specialized features of osmoadaptation. Finally, we demonstrate the broad utility of such datasets, for metagenomics, improvements to automated gene annotation and investigations of evolutionary processes.

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Genera-level comparisons of genomic features.Assembled genome size (Mbp) (A), number of predicted protein coding sequences (B), %G+C (C), and mean protein isoelectric point (D) were extracted from each genome, organized by genus, and boxplots calculated using MATLAB's Statistics toolbox. Boxplots were generated using 25th and 75th percentile as box edges, with median demarcated with horizontal line within box. Genera are ordered by descending number of species sequenced, with the number of species shown in parentheses. Genera with only a single sequenced member are shown as horizontal lines.
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pgen-1004784-g008: Genera-level comparisons of genomic features.Assembled genome size (Mbp) (A), number of predicted protein coding sequences (B), %G+C (C), and mean protein isoelectric point (D) were extracted from each genome, organized by genus, and boxplots calculated using MATLAB's Statistics toolbox. Boxplots were generated using 25th and 75th percentile as box edges, with median demarcated with horizontal line within box. Genera are ordered by descending number of species sequenced, with the number of species shown in parentheses. Genera with only a single sequenced member are shown as horizontal lines.

Mentions: In addition to local variation in G+C content, we also investigated variation at the genus level. We found that, although some genera display little variability in genomic G+C content (eg. Halorubrum, Haloarcula), others exhibit a wide range (eg. Haloferax, Halococcus) (Figure 8C). This wide deviation in G+C content cannot be attributed to tolerance of a wide range of salinities, as the known NaCl tolerance range of Haloarcula and Halococcus species are very similar (3.2 M and 3.5 M respectively), as are those for Haloferax and Halorubrum species (4.1 M and 4.2 M respectively) [72]. Thus, the link between high G+C content and salinity tolerance in the haloarchaea appears to be more complex than previously appreciated.


Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response.

Becker EA, Seitzer PM, Tritt A, Larsen D, Krusor M, Yao AI, Wu D, Madern D, Eisen JA, Darling AE, Facciotti MT - PLoS Genet. (2014)

Genera-level comparisons of genomic features.Assembled genome size (Mbp) (A), number of predicted protein coding sequences (B), %G+C (C), and mean protein isoelectric point (D) were extracted from each genome, organized by genus, and boxplots calculated using MATLAB's Statistics toolbox. Boxplots were generated using 25th and 75th percentile as box edges, with median demarcated with horizontal line within box. Genera are ordered by descending number of species sequenced, with the number of species shown in parentheses. Genera with only a single sequenced member are shown as horizontal lines.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230888&req=5

pgen-1004784-g008: Genera-level comparisons of genomic features.Assembled genome size (Mbp) (A), number of predicted protein coding sequences (B), %G+C (C), and mean protein isoelectric point (D) were extracted from each genome, organized by genus, and boxplots calculated using MATLAB's Statistics toolbox. Boxplots were generated using 25th and 75th percentile as box edges, with median demarcated with horizontal line within box. Genera are ordered by descending number of species sequenced, with the number of species shown in parentheses. Genera with only a single sequenced member are shown as horizontal lines.
Mentions: In addition to local variation in G+C content, we also investigated variation at the genus level. We found that, although some genera display little variability in genomic G+C content (eg. Halorubrum, Haloarcula), others exhibit a wide range (eg. Haloferax, Halococcus) (Figure 8C). This wide deviation in G+C content cannot be attributed to tolerance of a wide range of salinities, as the known NaCl tolerance range of Haloarcula and Halococcus species are very similar (3.2 M and 3.5 M respectively), as are those for Haloferax and Halorubrum species (4.1 M and 4.2 M respectively) [72]. Thus, the link between high G+C content and salinity tolerance in the haloarchaea appears to be more complex than previously appreciated.

Bottom Line: We challenge a recent high-profile proposal regarding the evolutionary origins of the haloarchaea by showing that inclusion of additional genomes significantly reduces support for a proposed large-scale horizontal gene transfer into the ancestral haloarchaeon from the bacterial domain.The combination of broad (17 genera) and deep (≥5 species in four genera) sampling of a phenotypically unified clade has enabled us to uncover both highly conserved and specialized features of osmoadaptation.Finally, we demonstrate the broad utility of such datasets, for metagenomics, improvements to automated gene annotation and investigations of evolutionary processes.

View Article: PubMed Central - PubMed

Affiliation: Microbiology Graduate Group, University of California, Davis, Davis, California, United States of America; Genome Center, University of California, Davis, Davis, California, United States of America.

ABSTRACT
Organisms across the tree of life use a variety of mechanisms to respond to stress-inducing fluctuations in osmotic conditions. Cellular response mechanisms and phenotypes associated with osmoadaptation also play important roles in bacterial virulence, human health, agricultural production and many other biological systems. To improve understanding of osmoadaptive strategies, we have generated 59 high-quality draft genomes for the haloarchaea (a euryarchaeal clade whose members thrive in hypersaline environments and routinely experience drastic changes in environmental salinity) and analyzed these new genomes in combination with those from 21 previously sequenced haloarchaeal isolates. We propose a generalized model for haloarchaeal management of cytoplasmic osmolarity in response to osmotic shifts, where potassium accumulation and sodium expulsion during osmotic upshock are accomplished via secondary transport using the proton gradient as an energy source, and potassium loss during downshock is via a combination of secondary transport and non-specific ion loss through mechanosensitive channels. We also propose new mechanisms for magnesium and chloride accumulation. We describe the expansion and differentiation of haloarchaeal general transcription factor families, including two novel expansions of the TATA-binding protein family, and discuss their potential for enabling rapid adaptation to environmental fluxes. We challenge a recent high-profile proposal regarding the evolutionary origins of the haloarchaea by showing that inclusion of additional genomes significantly reduces support for a proposed large-scale horizontal gene transfer into the ancestral haloarchaeon from the bacterial domain. The combination of broad (17 genera) and deep (≥5 species in four genera) sampling of a phenotypically unified clade has enabled us to uncover both highly conserved and specialized features of osmoadaptation. Finally, we demonstrate the broad utility of such datasets, for metagenomics, improvements to automated gene annotation and investigations of evolutionary processes.

Show MeSH
Related in: MedlinePlus