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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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Proteome-wide isoelectric point distributions.Histograms of computed pI values for (A) Haloferax mediterranei, (B) Halorubrum litoreum, (C) Haloarcula argentinensis, and (D) Natrialba aegyptia. Each of these four species is a representative from the four most populous genera in the set, which collectively contain 66% of the organisms in the study. For all sequenced haloarchaea, the pI histograms exhibited a bimodal distribution with a major mode at about 4.5 and much smaller minor mode around 10. For all isoelectric point plots see Data Dryad package [67].
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pgen-1004784-g005: Proteome-wide isoelectric point distributions.Histograms of computed pI values for (A) Haloferax mediterranei, (B) Halorubrum litoreum, (C) Haloarcula argentinensis, and (D) Natrialba aegyptia. Each of these four species is a representative from the four most populous genera in the set, which collectively contain 66% of the organisms in the study. For all sequenced haloarchaea, the pI histograms exhibited a bimodal distribution with a major mode at about 4.5 and much smaller minor mode around 10. For all isoelectric point plots see Data Dryad package [67].

Mentions: In addition to the ability to rapidly adapt to changing environmental salinities, haloarchaeal adaptations to high salt also include intrinsic physiological features present under all environmental conditions. These adaptations include an acidified proteome and high genomic G+C content [35], [62], [63], discussed here and in the subsequent section, respectively. Proteome acidification may be beneficial for salt-in strategists by prevention of protein aggregation via the ability of acidic amino acid residues to reorganize protein-solvent interactions [61], [64], [65], although alternative explanations have been proposed [66]. As expected, all 59 organisms whose draft genome we report here have both high genomic G+C content (ranging from 59–69%) and a highly acidified proteome. Histograms of predicted isoelectric points of haloarchaeal proteomes revealed an asymmetric bimodal distribution, with a dramatically larger major mode around pH 4.5, a minor mode around pH 10.0, and a consistent overall shape across haloarchaeal species (Figure 5 and Data Dryad package [67]). Corroborating previous work, this major mode was shifted towards lower pI values compared to non-haloarchaea [68].


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)

Proteome-wide isoelectric point distributions.Histograms of computed pI values for (A) Haloferax mediterranei, (B) Halorubrum litoreum, (C) Haloarcula argentinensis, and (D) Natrialba aegyptia. Each of these four species is a representative from the four most populous genera in the set, which collectively contain 66% of the organisms in the study. For all sequenced haloarchaea, the pI histograms exhibited a bimodal distribution with a major mode at about 4.5 and much smaller minor mode around 10. For all isoelectric point plots see Data Dryad package [67].
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004784-g005: Proteome-wide isoelectric point distributions.Histograms of computed pI values for (A) Haloferax mediterranei, (B) Halorubrum litoreum, (C) Haloarcula argentinensis, and (D) Natrialba aegyptia. Each of these four species is a representative from the four most populous genera in the set, which collectively contain 66% of the organisms in the study. For all sequenced haloarchaea, the pI histograms exhibited a bimodal distribution with a major mode at about 4.5 and much smaller minor mode around 10. For all isoelectric point plots see Data Dryad package [67].
Mentions: In addition to the ability to rapidly adapt to changing environmental salinities, haloarchaeal adaptations to high salt also include intrinsic physiological features present under all environmental conditions. These adaptations include an acidified proteome and high genomic G+C content [35], [62], [63], discussed here and in the subsequent section, respectively. Proteome acidification may be beneficial for salt-in strategists by prevention of protein aggregation via the ability of acidic amino acid residues to reorganize protein-solvent interactions [61], [64], [65], although alternative explanations have been proposed [66]. As expected, all 59 organisms whose draft genome we report here have both high genomic G+C content (ranging from 59–69%) and a highly acidified proteome. Histograms of predicted isoelectric points of haloarchaeal proteomes revealed an asymmetric bimodal distribution, with a dramatically larger major mode around pH 4.5, a minor mode around pH 10.0, and a consistent overall shape across haloarchaeal species (Figure 5 and Data Dryad package [67]). Corroborating previous work, this major mode was shifted towards lower pI values compared to non-haloarchaea [68].

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