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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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Updated haloarchaeal phylogeny.Multi-marker concatenated phylogeny of the 80 genomes included in this study and other haloarchaeal genomes gathered from IMG. The unrooted tree was built from a concatenated alignment of 40 PhyEco markers using PHYML. Branch support values for top-level branches have been removed for ease of visualization. The full tree file can be accessed through Dataset S19. Grey boxes represent haloarchaeal clades as described in [19], expanded as described in text. Tree roots in the Methanocella (not shown).
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pgen-1004784-g002: Updated haloarchaeal phylogeny.Multi-marker concatenated phylogeny of the 80 genomes included in this study and other haloarchaeal genomes gathered from IMG. The unrooted tree was built from a concatenated alignment of 40 PhyEco markers using PHYML. Branch support values for top-level branches have been removed for ease of visualization. The full tree file can be accessed through Dataset S19. Grey boxes represent haloarchaeal clades as described in [19], expanded as described in text. Tree roots in the Methanocella (not shown).

Mentions: Previous phylogenetic studies have described two major haloarchaeal clades and several smaller groups with poorly defined relationships to these clades [19]. Here we update this previous work based on a phylogeny constructed using a concatenated set of 40 highly conserved genes (Figure 2) [20]. We expand the previously defined clades as follows: we consider a species to belong to a clade if a member of that genus was previously assigned to that clade and the genus is not paraphyletic or polyphyletic, and we also include any species which group with that clade with at least 75% support. Using this process for determining clade relationship, the increased resolution in the multi-marker phylogeny allows us to assign Halovivax to Clade 1. On the basis of the same phylogeny, we also propose designation of a third haloarchaeal clade, including the Halobacterium, Natronomonas, Halorhabdus, Halosimplex, Halomicrobium, and Haloarcula genera.


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)

Updated haloarchaeal phylogeny.Multi-marker concatenated phylogeny of the 80 genomes included in this study and other haloarchaeal genomes gathered from IMG. The unrooted tree was built from a concatenated alignment of 40 PhyEco markers using PHYML. Branch support values for top-level branches have been removed for ease of visualization. The full tree file can be accessed through Dataset S19. Grey boxes represent haloarchaeal clades as described in [19], expanded as described in text. Tree roots in the Methanocella (not shown).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004784-g002: Updated haloarchaeal phylogeny.Multi-marker concatenated phylogeny of the 80 genomes included in this study and other haloarchaeal genomes gathered from IMG. The unrooted tree was built from a concatenated alignment of 40 PhyEco markers using PHYML. Branch support values for top-level branches have been removed for ease of visualization. The full tree file can be accessed through Dataset S19. Grey boxes represent haloarchaeal clades as described in [19], expanded as described in text. Tree roots in the Methanocella (not shown).
Mentions: Previous phylogenetic studies have described two major haloarchaeal clades and several smaller groups with poorly defined relationships to these clades [19]. Here we update this previous work based on a phylogeny constructed using a concatenated set of 40 highly conserved genes (Figure 2) [20]. We expand the previously defined clades as follows: we consider a species to belong to a clade if a member of that genus was previously assigned to that clade and the genus is not paraphyletic or polyphyletic, and we also include any species which group with that clade with at least 75% support. Using this process for determining clade relationship, the increased resolution in the multi-marker phylogeny allows us to assign Halovivax to Clade 1. On the basis of the same phylogeny, we also propose designation of a third haloarchaeal clade, including the Halobacterium, Natronomonas, Halorhabdus, Halosimplex, Halomicrobium, and Haloarcula genera.

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