Structural conservation of chemotaxis machinery across A rchaea and B acteria
Abstract
Summary Chemotaxis allows cells to sense and respond to their environment. In B acteria, stimuli are detected by arrays of chemoreceptors that relay the signal to a two‐component regulatory system. These arrays take the form of highly stereotyped super‐lattices comprising hexagonally packed trimers‐of‐receptor‐dimers networked by rings of histidine kinase and coupling proteins. This structure is conserved across chemotactic B acteria, and between membrane‐bound and cytoplasmic arrays, and gives rise to the highly cooperative, dynamic nature of the signalling system. The chemotaxis system, absent in eukaryotes, is also found in A rchaea, where its structural details remain uncharacterized. Here we provide evidence that the chemotaxis machinery was not present in the last archaeal common ancestor, but rather was introduced in one of the waves of lateral gene transfer that occurred after the branching of Eukaryota but before the diversification of E uryarchaeota. Unlike in B acteria, the chemotaxis system then evolved largely vertically in A rchaea, with very few subsequent successful lateral gene transfer events. By electron cryotomography, we find that the structure of both membrane‐bound and cytoplasmic chemoreceptor arrays is conserved between B acteria and A rchaea, suggesting the fundamental importance of this signalling architecture across diverse prokaryotic lifestyles.
- Authors:
-
- California Institute of Technology 1200 E. California Blvd. Pasadena CA 91125 USA
- University of California Los Angeles 609 Charles E. Young Dr. S. Los Angeles CA USA
- California Institute of Technology 1200 E. California Blvd. Pasadena CA 91125 USA, Howard Hughes Medical Institute 1200 E. California Blvd. Pasadena CA 91125 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1401606
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Environmental Microbiology Reports
- Additional Journal Information:
- Journal Name: Environmental Microbiology Reports Journal Volume: 7 Journal Issue: 3; Journal ID: ISSN 1758-2229
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Briegel, Ariane, Ortega, Davi R., Huang, Audrey N., Oikonomou, Catherine M., Gunsalus, Robert P., and Jensen, Grant J. Structural conservation of chemotaxis machinery across A rchaea and B acteria. United States: N. p., 2015.
Web. doi:10.1111/1758-2229.12265.
Briegel, Ariane, Ortega, Davi R., Huang, Audrey N., Oikonomou, Catherine M., Gunsalus, Robert P., & Jensen, Grant J. Structural conservation of chemotaxis machinery across A rchaea and B acteria. United States. https://doi.org/10.1111/1758-2229.12265
Briegel, Ariane, Ortega, Davi R., Huang, Audrey N., Oikonomou, Catherine M., Gunsalus, Robert P., and Jensen, Grant J. Wed .
"Structural conservation of chemotaxis machinery across A rchaea and B acteria". United States. https://doi.org/10.1111/1758-2229.12265.
@article{osti_1401606,
title = {Structural conservation of chemotaxis machinery across A rchaea and B acteria},
author = {Briegel, Ariane and Ortega, Davi R. and Huang, Audrey N. and Oikonomou, Catherine M. and Gunsalus, Robert P. and Jensen, Grant J.},
abstractNote = {Summary Chemotaxis allows cells to sense and respond to their environment. In B acteria, stimuli are detected by arrays of chemoreceptors that relay the signal to a two‐component regulatory system. These arrays take the form of highly stereotyped super‐lattices comprising hexagonally packed trimers‐of‐receptor‐dimers networked by rings of histidine kinase and coupling proteins. This structure is conserved across chemotactic B acteria, and between membrane‐bound and cytoplasmic arrays, and gives rise to the highly cooperative, dynamic nature of the signalling system. The chemotaxis system, absent in eukaryotes, is also found in A rchaea, where its structural details remain uncharacterized. Here we provide evidence that the chemotaxis machinery was not present in the last archaeal common ancestor, but rather was introduced in one of the waves of lateral gene transfer that occurred after the branching of Eukaryota but before the diversification of E uryarchaeota. Unlike in B acteria, the chemotaxis system then evolved largely vertically in A rchaea, with very few subsequent successful lateral gene transfer events. By electron cryotomography, we find that the structure of both membrane‐bound and cytoplasmic chemoreceptor arrays is conserved between B acteria and A rchaea, suggesting the fundamental importance of this signalling architecture across diverse prokaryotic lifestyles.},
doi = {10.1111/1758-2229.12265},
journal = {Environmental Microbiology Reports},
number = 3,
volume = 7,
place = {United States},
year = {Wed Apr 08 00:00:00 EDT 2015},
month = {Wed Apr 08 00:00:00 EDT 2015}
}
https://doi.org/10.1111/1758-2229.12265
Web of Science
Works referenced in this record:
The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations : The genome of
journal, October 2012
- Spang, Anja; Poehlein, Anja; Offre, Pierre
- Environmental Microbiology, Vol. 14, Issue 12
Specialized Structure in the Region of the Flagella tuft in Spirillum Serpens
journal, June 1963
- Murray, R. G. E.; Birch-Andersen, A.
- Canadian Journal of Microbiology, Vol. 9, Issue 3
Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1
journal, January 2004
- Atomi, Haruyuki; Fukui, Toshiaki; Kanai, Tamotsu
- Archaea, Vol. 1, Issue 4
Origins of major archaeal clades correspond to gene acquisitions from bacteria
journal, October 2014
- Nelson-Sathi, Shijulal; Sousa, Filipa L.; Roettger, Mayo
- Nature, Vol. 517, Issue 7532
Fast tomographic reconstruction on multicore computers
journal, December 2010
- Agulleiro, J. I.; Fernandez, J. J.
- Bioinformatics, Vol. 27, Issue 4
Evolution of Two-Component Signal Transduction
journal, December 2000
- Koretke, Kristin K.; Lupas, Andrei N.; Warren, Patrick V.
- Molecular Biology and Evolution, Vol. 17, Issue 12
Horizontal gene transfer in eukaryotic evolution
journal, August 2008
- Keeling, Patrick J.; Palmer, Jeffrey D.
- Nature Reviews Genetics, Vol. 9, Issue 8
Universal architecture of bacterial chemoreceptor arrays
journal, September 2009
- Briegel, A.; Ortega, D. R.; Tocheva, E. I.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 40
Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis
journal, February 2011
- Blainey, Paul C.; Mosier, Annika C.; Potanina, Anastasia
- PLoS ONE, Vol. 6, Issue 2
Isolation and Ultrastructure of the Flagella of Methanococcus thermolithotrophicus and Methanospirillum hungatei
journal, June 1989
- Cruden, Diana; Sparling, Richard; Markovetz, A. J.
- Applied and Environmental Microbiology, Vol. 55, Issue 6
Polarity in Action: Asymmetric Protein Localization in Bacteria
journal, June 2001
- Lybarger, S. R.; Maddock, J. R.
- Journal of Bacteriology, Vol. 183, Issue 11
Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus
journal, January 2009
- Schlesner, Matthias; Miller, Arthur; Streif, Stefan
- BMC Microbiology, Vol. 9, Issue 1
Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota
journal, March 2008
- Brochier-Armanet, Céline; Boussau, Bastien; Gribaldo, Simonetta
- Nature Reviews Microbiology, Vol. 6, Issue 3
Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling
journal, March 2014
- Briegel, Ariane; Ladinsky, Mark S.; Oikonomou, Catherine
- eLife, Vol. 3
Bacterial chemoreceptors: high-performance signaling in networked arrays
journal, January 2008
- Hazelbauer, Gerald L.; Falke, Joseph J.; Parkinson, John S.
- Trends in Biochemical Sciences, Vol. 33, Issue 1
Bacterial and archaeal flagella as prokaryotic motility organelles
journal, November 2004
- Metlina, A. L.
- Biochemistry (Moscow), Vol. 69, Issue 11
The MiST2 database: a comprehensive genomics resource on microbial signal transduction
journal, November 2009
- Ulrich, Luke E.; Zhulin, Igor B.
- Nucleic Acids Research, Vol. 38, Issue suppl_1
Phylogeny and evolution of the Archaea: one hundred genomes later
journal, June 2011
- Brochier-Armanet, Celine; Forterre, Patrick; Gribaldo, Simonetta
- Current Opinion in Microbiology, Vol. 14, Issue 3
Structural, mass and elemental analyses of storage granules in methanogenic archaeal cells: Storage granules in methanogenic archaeal cells
journal, August 2011
- Toso, Daniel B.; Henstra, Anne M.; Gunsalus, Robert P.
- Environmental Microbiology, Vol. 13, Issue 9
The Cell Surface Glycoprotein Layer of the Extreme Halophile Halobacterium salinarum and Its Relation to Haloferax volcanii: Cryo-electron Tomography of Freeze-Substituted Cells and Projection Studies of Negatively Stained Envelopes
journal, May 2000
- Trachtenberg, Shlomo; Pinnick, Baruch; Kessel, Martin
- Journal of Structural Biology, Vol. 130, Issue 1
The archaellum: an old motility structure with a new name
journal, July 2012
- Jarrell, Ken F.; Albers, Sonja-Verena
- Trends in Microbiology, Vol. 20, Issue 7
The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography
journal, August 2006
- Nicastro, D.
- Science, Vol. 313, Issue 5789
Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996
- Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
- Journal of Structural Biology, Vol. 116, Issue 1
Origins and Diversification of a Complex Signal Transduction System in Prokaryotes
journal, June 2010
- Wuichet, K.; Zhulin, I. B.
- Science Signaling, Vol. 3, Issue 128