Life on the edge: Functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans

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

Research output: Contribution to journalArticlepeer-review

35 Scopus citations

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.

Original languageEnglish
Pages (from-to)101-114
Number of pages14
JournalISME Journal
Volume9
Issue number1
DOIs
StatePublished - Jan 11 2015

Funding

This research was supported by a grant from the US Department of Energy, Office of Biological and Environmental Research (DE-SC0006654) and by the Laboratory Directed Research and Development Program of Oak Ridge National Laboratory (ORNL). ORNL is managed by UT-Battelle, LLC, for the US Department of Energy. TH, HH and RR were funded by Deutsche Forschungsge-meinschaft. We would like to acknowledge the University of Tennessee Advanced Microscopy and Imaging Center for instrument use, scientific and technical assistance.

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