Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response
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 originsmore »
- Authors:
-
- Univ. of California, Davis, CA (United States)
- Univ. of California, Davis, CA (United States); Proteome Software, Portland, OR (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Université Grenoble Alpes, Grenoble (France); Centre National de la Recherche Scientifique, Grenoble (France); Commissariat à l'énergie Atomique et aux Énergies Alternatives, Grenoble (France)
- Univ. of Technology, Syndey (Australia)
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1579707
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 11; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Becker, Erin A., Seitzer, Phillip M., Tritt, Andrew, Larsen, David, Krusor, Megan, Yao, Andrew I., Wu, Dongying, Madern, Dominique, Eisen, Jonathan A., Darling, Aaron E., Facciotti, Marc T., and Whitaker, Rachel J. Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response. United States: N. p., 2014.
Web. doi:10.1371/journal.pgen.1004784.
Becker, Erin A., Seitzer, Phillip M., Tritt, Andrew, Larsen, David, Krusor, Megan, Yao, Andrew I., Wu, Dongying, Madern, Dominique, Eisen, Jonathan A., Darling, Aaron E., Facciotti, Marc T., & Whitaker, Rachel J. Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response. United States. https://doi.org/10.1371/journal.pgen.1004784
Becker, Erin A., Seitzer, Phillip M., Tritt, Andrew, Larsen, David, Krusor, Megan, Yao, Andrew I., Wu, Dongying, Madern, Dominique, Eisen, Jonathan A., Darling, Aaron E., Facciotti, Marc T., and Whitaker, Rachel J. Thu .
"Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response". United States. https://doi.org/10.1371/journal.pgen.1004784. https://www.osti.gov/servlets/purl/1579707.
@article{osti_1579707,
title = {Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response},
author = {Becker, Erin A. and Seitzer, Phillip M. and Tritt, Andrew and Larsen, David and Krusor, Megan and Yao, Andrew I. and Wu, Dongying and Madern, Dominique and Eisen, Jonathan A. and Darling, Aaron E. and Facciotti, Marc T. and Whitaker, Rachel J.},
abstractNote = {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.},
doi = {10.1371/journal.pgen.1004784},
journal = {PLoS Genetics},
number = 11,
volume = 10,
place = {United States},
year = {Thu Nov 13 00:00:00 EST 2014},
month = {Thu Nov 13 00:00:00 EST 2014}
}
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- Spang, Anja; Caceres, Eva F.; Ettema, Thijs J. G.
- Science, Vol. 357, Issue 6351
The Prodigal Compound: Return of Ribosyl 1,5-Bisphosphate as an Important Player in Metabolism
journal, December 2018
- Hove-Jensen, Bjarne; Brodersen, Ditlev E.; Manav, M. Cemre
- Microbiology and Molecular Biology Reviews, Vol. 83, Issue 1
Genome-wide identification of transcriptional start sites in the haloarchaeon Haloferax volcanii based on differential RNA-Seq (dRNA-Seq)
journal, August 2016
- Babski, Julia; Haas, Karina A.; Näther-Schindler, Daniela
- BMC Genomics, Vol. 17, Issue 1
Hundreds of novel composite genes and chimeric genes with bacterial origins contributed to haloarchaeal evolution
journal, June 2018
- Méheust, Raphaël; Watson, Andrew K.; Lapointe, François-Joseph
- Genome Biology, Vol. 19, Issue 1
HaloDom: a new database of halophiles across all life domains
journal, January 2018
- Loukas, Alexios; Kappas, Ilias; Abatzopoulos, Theodore J.
- Journal of Biological Research-Thessaloniki, Vol. 25, Issue 1
With a pinch of extra salt—Did predatory protists steal genes from their food?
journal, February 2018
- Czech, Laura; Bremer, Erhard
- PLOS Biology, Vol. 16, Issue 2
Structure and function of archaeal histones
journal, September 2018
- Henneman, Bram; van Emmerik, Clara; van Ingen, Hugo
- PLOS Genetics, Vol. 14, Issue 9
A Large and Phylogenetically Diverse Class of Type 1 Opsins Lacking a Canonical Retinal Binding Site
journal, June 2016
- Becker, Erin A.; Yao, Andrew I.; Seitzer, Phillip M.
- PLOS ONE, Vol. 11, Issue 6
Characterization of the transcriptome of Haloferax volcanii, grown under four different conditions, with mixed RNA-Seq
journal, April 2019
- Laass, Sebastian; Monzon, Vivian A.; Kliemt, Jana
- PLOS ONE, Vol. 14, Issue 4
Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019
- Uritskiy, Gherman; DiRuggiero, Jocelyne
- Genes, Vol. 10, Issue 3
Intermediate-Salinity Systems at High Altitudes in the Peruvian Andes Unveil a High Diversity and Abundance of Bacteria and Viruses
journal, November 2019
- Castelán-Sánchez, Hugo Gildardo; Elorrieta, Paola; Romoacca, Pedro
- Genes, Vol. 10, Issue 11
Metagenomic Insights into the Phylogenetic and Metabolic Diversity of the Prokaryotic Community Dwelling in Hypersaline Soils from the Odiel Saltmarshes (SW Spain)
journal, March 2018
- Vera-Gargallo, Blanca; Ventosa, Antonio
- Genes, Vol. 9, Issue 3