Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans View Full Text


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Article Info

DATE

2014-07-11

AUTHORS

Richard J Giannone, Louie L Wurch, Thomas Heimerl, Stanton Martin, Zamin Yang, Harald Huber, Reinhard Rachel, Robert L Hettich, Mircea Podar

ABSTRACT

The marine hyperthermophilic crenarchaeon Ignicoccus hospitalis supports the propagation on its surface of Nanoarchaeum equitans, an evolutionarily enigmatic archaeon that resembles highly derived parasitic and symbiotic bacteria. The cellular and molecular mechanisms that enable this interarchaea relationship and the intimate physiologic consequences to I. hospitalis are unknown. Here, we used concerted proteomic and transcriptomic analyses to probe into the functional genomic response of I. hospitalis as N. equitans multiplies on its surface. The expression of over 97% of the genes was detected at mRNA level and over 80% of the predicted proteins were identified and their relative abundance measured by proteomics. These indicate that little, if any, of the host genomic information is silenced during growth in the laboratory. The primary response to N. equitans was at the membrane level, with increases in relative abundance of most protein complexes involved in energy generation as well as that of several transporters and proteins involved in cellular membrane stabilization. Similar upregulation was observed for genes and proteins involved in key metabolic steps controlling nitrogen and carbon metabolism, although the overall biosynthetic pathways were marginally impacted. Proliferation of N. equitans resulted, however, in selective downregulation of genes coding for transcription factors and replication and cell cycle control proteins as I. hospitalis shifted its physiology from its own cellular growth to that of its ectosymbiont/parasite. The combination of these multiomic approaches provided an unprecedented level of detail regarding the dynamics of this interspecies interaction, which is especially pertinent as these organisms are not genetically tractable. More... »

PAGES

101-114

References to SciGraph publications

  • 2013-04-22. Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park in BIOLOGY DIRECT
  • 2012-12-14. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer in BIOLOGY DIRECT
  • 2009-11-30. Bacterial competition: surviving and thriving in the microbial jungle in NATURE REVIEWS MICROBIOLOGY
  • 2006-10-26. Global analysis of mRNA stability in the archaeon Sulfolobus in GENOME BIOLOGY
  • 2004-09-14. Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I in ARCHIVES OF MICROBIOLOGY
  • 2013-12-02. Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass in BIOTECHNOLOGY FOR BIOFUELS
  • 2012-03-13. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses in NATURE REVIEWS GENETICS
  • 2007-03-05. Adaptations to energy stress dictate the ecology and evolution of the Archaea in NATURE REVIEWS MICROBIOLOGY
  • 2008-01-25. The prokaryotic V4R domain is the likely ancestor of a key component of the eukaryotic vesicle transport system in BIOLOGY DIRECT
  • 2008-11-10. A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans in GENOME BIOLOGY
  • 2008-07-12. Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography in ARCHIVES OF MICROBIOLOGY
  • 2002-05. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont in NATURE
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/ismej.2014.112

    DOI

    http://dx.doi.org/10.1038/ismej.2014.112

    DIMENSIONS

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    PUBMED

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    28 schema:description The marine hyperthermophilic crenarchaeon Ignicoccus hospitalis supports the propagation on its surface of Nanoarchaeum equitans, an evolutionarily enigmatic archaeon that resembles highly derived parasitic and symbiotic bacteria. The cellular and molecular mechanisms that enable this interarchaea relationship and the intimate physiologic consequences to I. hospitalis are unknown. Here, we used concerted proteomic and transcriptomic analyses to probe into the functional genomic response of I. hospitalis as N. equitans multiplies on its surface. The expression of over 97% of the genes was detected at mRNA level and over 80% of the predicted proteins were identified and their relative abundance measured by proteomics. These indicate that little, if any, of the host genomic information is silenced during growth in the laboratory. The primary response to N. equitans was at the membrane level, with increases in relative abundance of most protein complexes involved in energy generation as well as that of several transporters and proteins involved in cellular membrane stabilization. Similar upregulation was observed for genes and proteins involved in key metabolic steps controlling nitrogen and carbon metabolism, although the overall biosynthetic pathways were marginally impacted. Proliferation of N. equitans resulted, however, in selective downregulation of genes coding for transcription factors and replication and cell cycle control proteins as I. hospitalis shifted its physiology from its own cellular growth to that of its ectosymbiont/parasite. The combination of these multiomic approaches provided an unprecedented level of detail regarding the dynamics of this interspecies interaction, which is especially pertinent as these organisms are not genetically tractable.
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    81 levels
    82 life
    83 mRNA levels
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