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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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Haloarchaeal TATA-binding protein phylogeny.Unrooted phylogenetic tree of haloarchaeal TATA-binding protein (TBP) homologs. Dark green - TbpC, light green - TbpD/B/F, magenta - TbpE/A, salmon - TbpW, dark purple - TbpX, blue – TbpY, light purple – TbpZ, black - unassigned. Number of sequences and species represented in each clade is shown in parenthesis. Bootstrap support values over 30% are shown for major clades. See Dataset S7 for tree file.
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pgen-1004784-g010: Haloarchaeal TATA-binding protein phylogeny.Unrooted phylogenetic tree of haloarchaeal TATA-binding protein (TBP) homologs. Dark green - TbpC, light green - TbpD/B/F, magenta - TbpE/A, salmon - TbpW, dark purple - TbpX, blue – TbpY, light purple – TbpZ, black - unassigned. Number of sequences and species represented in each clade is shown in parenthesis. Bootstrap support values over 30% are shown for major clades. See Dataset S7 for tree file.

Mentions: Evolutionary expansion of the TBP family appears to be a more recent phenomenon, with three haloarchaeal lineages showing distinct patterns of duplication and divergence (Figure 10, Dataset S7, Figure S10, Dataset S8). Phylogenetic distribution of TBP paralogs suggests that the ancestral haloarchaeal TBP was most similar to tbpE of Hbt. sp. NRC-1, with only one species (Natrinema pallidum) apparently lacking this homolog. We speculate that this gene may be present at a contig boundary in the assembly for this organism (which consists of 116 contigs), and may later be uncovered by additional sequencing. The ancestral nature of the tbpE homolog is also supported by it being the only TBP in the natural TBP knockout strain Halobacterium salinarum PHH4 [77].


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)

Haloarchaeal TATA-binding protein phylogeny.Unrooted phylogenetic tree of haloarchaeal TATA-binding protein (TBP) homologs. Dark green - TbpC, light green - TbpD/B/F, magenta - TbpE/A, salmon - TbpW, dark purple - TbpX, blue – TbpY, light purple – TbpZ, black - unassigned. Number of sequences and species represented in each clade is shown in parenthesis. Bootstrap support values over 30% are shown for major clades. See Dataset S7 for tree file.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004784-g010: Haloarchaeal TATA-binding protein phylogeny.Unrooted phylogenetic tree of haloarchaeal TATA-binding protein (TBP) homologs. Dark green - TbpC, light green - TbpD/B/F, magenta - TbpE/A, salmon - TbpW, dark purple - TbpX, blue – TbpY, light purple – TbpZ, black - unassigned. Number of sequences and species represented in each clade is shown in parenthesis. Bootstrap support values over 30% are shown for major clades. See Dataset S7 for tree file.
Mentions: Evolutionary expansion of the TBP family appears to be a more recent phenomenon, with three haloarchaeal lineages showing distinct patterns of duplication and divergence (Figure 10, Dataset S7, Figure S10, Dataset S8). Phylogenetic distribution of TBP paralogs suggests that the ancestral haloarchaeal TBP was most similar to tbpE of Hbt. sp. NRC-1, with only one species (Natrinema pallidum) apparently lacking this homolog. We speculate that this gene may be present at a contig boundary in the assembly for this organism (which consists of 116 contigs), and may later be uncovered by additional sequencing. The ancestral nature of the tbpE homolog is also supported by it being the only TBP in the natural TBP knockout strain Halobacterium salinarum PHH4 [77].

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