Phylogenetically driven sequencing of extremely halophilic archaea reveals strategies for static and dynamic osmo-response.
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.
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.
Erin A
EA
Becker
Genome Center, University of California, Davis, Davis, California, United States of America; Department of Biomedical Engineering, University of California, Davis, Davis, California, United States of America; Proteome Software, Portland, Oregon, United States of America.
Phillip M
PM
Seitzer
Department of Energy Joint Genomes Institute, Walnut Creek, California, United States of America.
Andrew
A
Tritt
Genome Center, University of California, Davis, Davis, California, United States of America.
David
D
Larsen
Microbiology Graduate Group, University of California, Davis, Davis, California, United States of America; Department of Earth and Planetary Sciences, University of California, Davis, Davis, California, United States of America.
Megan
M
Krusor
Genome Center, University of California, Davis, Davis, California, United States of America; Department of Biomedical Engineering, University of California, Davis, Davis, California, United States of America.
Andrew I
AI
Yao
Department of Energy Joint Genomes Institute, Walnut Creek, California, United States of America.
Dongying
D
Wu
Université Grenoble Alpes, Institut de Biologie Structurale, Grenoble, France; Centre National de la Recherche Scientifique, Institut de Biologie Structurale, Grenoble, France; Commissariat à l'énergie Atomique et aux Énergies Alternatives, Département du Science du Vivant, Institut de Biologie Structurale, Grenoble, France.
Dominique
D
Madern
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.
Jonathan A
JA
Eisen
ithree Institute, University of Technology, Sydney, Australia.
Aaron E
AE
Darling
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; Department of Biomedical Engineering, University of California, Davis, Davis, California, United States of America.
Marc T
MT
Facciotti
D000222:Adaptation, Physiological / Q000235:genetics*; D001105:Archaea / Q000235:genetics*; D001483:Base Sequence; D019143:Evolution, Molecular; D020745:Genome, Archaeal; D006801:Humans; D056186:Metagenomics; D058977:Molecular Sequence Annotation; D009994:Osmolar Concentration; D010802:Phylogeny; D054712:Salinity; D035181:TATA-Box Binding Protein / Q000235:genetics*
D035181:TATA-Box Binding Protein