Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response

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.

doi:10.1371/journal.pgen.1004784

Title: Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response

Journal Article · Thu Nov 13 00:00:00 EST 2014 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1004784· OSTI ID:1579707

Becker, Erin A. ^[1]; Seitzer, Phillip M. ^[2]; Tritt, Andrew ^[3]; Larsen, David ^[1]; Krusor, Megan ^[1]; Yao, Andrew I. ^[1]; Wu, Dongying ^[3]; Madern, Dominique ^[4]; Eisen, Jonathan A. ^[1]; Darling, Aaron E. ^[5]; Facciotti, Marc T. ^[1]; Whitaker, Rachel J. ^[6]

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)

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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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1579707

Journal Information:: PLoS Genetics, Vol. 10, Issue 11; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 88 works

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Methanonatronarchaeum thermophilum gen. nov., sp. nov. and 'Candidatus Methanohalarchaeum thermophilum', extremely halo(natrono)philic methyl-reducing methanogens from hypersaline lakes comprising a new euryarchaeal class Methanonatronarchaeia classis nov. Sorokin, Dimitry Y.; Merkel, Alexander Y.; Abbas, Ben International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 7 https://doi.org/10.1099/ijsem.0.002810	journal	July 2018
Strangers in the archaeal world: osmostress-responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus: Ectoine and hydroxyectoine biosynthesis in Archaea Widderich, Nils; Czech, Laura; Elling, Felix J. Environmental Microbiology, Vol. 18, Issue 4 https://doi.org/10.1111/1462-2920.13156	journal	January 2016
Functional interactions of archaea, bacteria and viruses in a hypersaline endolithic community: Halite metagenome Crits-Christoph, Alexander; Gelsinger, Diego R.; Ma, Bing Environmental Microbiology, Vol. 18, Issue 6 https://doi.org/10.1111/1462-2920.13259	journal	March 2016
Analysis of multiple haloarchaeal genomes suggests that the quinone-dependent respiratory nitric oxide reductase is an important source of nitrous oxide in hypersaline environments: Analysis of multiple haloarchaeal genomes Torregrosa-Crespo, Javier; González-Torres, Pedro; Bautista, Vanesa Environmental Microbiology Reports, Vol. 9, Issue 6 https://doi.org/10.1111/1758-2229.12596	journal	November 2017
Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life Spang, Anja; Caceres, Eva F.; Ettema, Thijs J. G. Science, Vol. 357, Issue 6351 https://doi.org/10.1126/science.aaf3883	journal	August 2017
The Prodigal Compound: Return of Ribosyl 1,5-Bisphosphate as an Important Player in Metabolism Hove-Jensen, Bjarne; Brodersen, Ditlev E.; Manav, M. Cemre Microbiology and Molecular Biology Reviews, Vol. 83, Issue 1 https://doi.org/10.1128/mmbr.00040-18	journal	December 2018
Genome-wide identification of transcriptional start sites in the haloarchaeon Haloferax volcanii based on differential RNA-Seq (dRNA-Seq) Babski, Julia; Haas, Karina A.; Näther-Schindler, Daniela BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2920-y	journal	August 2016
Hundreds of novel composite genes and chimeric genes with bacterial origins contributed to haloarchaeal evolution Méheust, Raphaël; Watson, Andrew K.; Lapointe, François-Joseph Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1454-9	journal	June 2018
HaloDom: a new database of halophiles across all life domains Loukas, Alexios; Kappas, Ilias; Abatzopoulos, Theodore J. Journal of Biological Research-Thessaloniki, Vol. 25, Issue 1 https://doi.org/10.1186/s40709-017-0072-0	journal	January 2018
With a pinch of extra salt—Did predatory protists steal genes from their food? Czech, Laura; Bremer, Erhard PLOS Biology, Vol. 16, Issue 2 https://doi.org/10.1371/journal.pbio.2005163	journal	February 2018
Structure and function of archaeal histones Henneman, Bram; van Emmerik, Clara; van Ingen, Hugo PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007582	journal	September 2018
A Large and Phylogenetically Diverse Class of Type 1 Opsins Lacking a Canonical Retinal Binding Site Becker, Erin A.; Yao, Andrew I.; Seitzer, Phillip M. PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156543	journal	June 2016
Characterization of the transcriptome of Haloferax volcanii, grown under four different conditions, with mixed RNA-Seq Laass, Sebastian; Monzon, Vivian A.; Kliemt, Jana PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0215986	journal	April 2019
Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome Uritskiy, Gherman; DiRuggiero, Jocelyne Genes, Vol. 10, Issue 3 https://doi.org/10.3390/genes10030220	journal	March 2019
Intermediate-Salinity Systems at High Altitudes in the Peruvian Andes Unveil a High Diversity and Abundance of Bacteria and Viruses Castelán-Sánchez, Hugo Gildardo; Elorrieta, Paola; Romoacca, Pedro Genes, Vol. 10, Issue 11 https://doi.org/10.3390/genes10110891	journal	November 2019
Metagenomic Insights into the Phylogenetic and Metabolic Diversity of the Prokaryotic Community Dwelling in Hypersaline Soils from the Odiel Saltmarshes (SW Spain) Vera-Gargallo, Blanca; Ventosa, Antonio Genes, Vol. 9, Issue 3 https://doi.org/10.3390/genes9030152	journal	March 2018

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