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Title: 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:
 [1];  [1];  [1];  [1];  [2];  [3]
  1. California Institute of Technology 1200 E. California Blvd. Pasadena CA 91125 USA
  2. University of California Los Angeles 609 Charles E. Young Dr. S. Los Angeles CA USA
  3. 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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1758-2229.12265

Citation Metrics:
Cited by: 60 works
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Works referenced in this record:

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
  • DOI: 10.1139/m63-047

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
  • DOI: 10.1155/2004/204953

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
  • DOI: 10.1038/nature13805

Fast tomographic reconstruction on multicore computers
journal, December 2010


Evolution of Two-Component Signal Transduction
journal, December 2000


Horizontal gene transfer in eukaryotic evolution
journal, August 2008

  • Keeling, Patrick J.; Palmer, Jeffrey D.
  • Nature Reviews Genetics, Vol. 9, Issue 8
  • DOI: 10.1038/nrg2386

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
  • DOI: 10.1073/pnas.0905181106

Chemotaxis in Bacteria
journal, August 1966


Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis
journal, February 2011


Isolation and Ultrastructure of the Flagella of Methanococcus thermolithotrophicus and Methanospirillum hungatei
journal, June 1989


Polarity in Action: Asymmetric Protein Localization in Bacteria
journal, June 2001


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
  • DOI: 10.1186/1471-2180-9-56

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
  • DOI: 10.1038/nrmicro1852

Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling
journal, March 2014

  • Briegel, Ariane; Ladinsky, Mark S.; Oikonomou, Catherine
  • eLife, Vol. 3
  • DOI: 10.7554/eLife.02151

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
  • DOI: 10.1016/j.tibs.2007.09.014

Bacterial and archaeal flagella as prokaryotic motility organelles
journal, November 2004


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
  • DOI: 10.1093/nar/gkp940

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
  • DOI: 10.1016/j.mib.2011.04.015

Structural, mass and elemental analyses of storage granules in methanogenic archaeal cells: Storage granules in methanogenic archaeal cells
journal, August 2011


The archaellum: an old motility structure with a new name
journal, July 2012


The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography
journal, August 2006


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
  • DOI: 10.1006/jsbi.1996.0013

Origins and Diversification of a Complex Signal Transduction System in Prokaryotes
journal, June 2010