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Title: Multi-omics analysis provides insight to the Ignicoccus hospitalis - Nanoarchaeum equitans association

Abstract

Studies of interspecies interactions are inherently difficult due to the complex mechanisms which enable these relationships. A model system for studying interspecies interactions is the marine hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans. Recent independently-conducted ‘omics’ analyses have generated insights into the molecular factors modulating this association. However, significant questions remain about the nature of the interactions between these archaea. We jointly analyzed multiple levels of omics datasets obtained from published, independent transcriptomics, proteomics, and metabolomics analyses. DAVID identified functionally-related groups enriched when I. hospitalis is grown alone or in co-culture with N. equitans. Enriched molecular pathways were subsequently visualized using interaction maps generated using STRING. Key findings of our multi-level omics analysis indicated that I. hospitalis provides precursors to N. equitans for energy metabolism. Analysis indicated an overall reduction in diversity of metabolic precursors in the I. hospitalis–N. equitans co-culture, which has been connected to the differential use of ribosomal subunits and was previously unnoticed. We also identified differences in precursors linked to amino acid metabolism, NADH metabolism, and carbon fixation, providing new insights into the metabolic adaptions of I. hospitalis enabling the growth of N. equitans. In conclusion, this multi-omics analysis builds upon previously identified cellular patterns while offeringmore » new insights into mechanisms that enable the I. hospitalis–N. equitans association. This study applies statistical and visualization techniques to a mixed-source omics dataset to yield a more global insight into a complex system, that was not readily discernable from separate omics studies.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [3];  [4];  [5];  [5]
  1. Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology; Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
  2. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
  5. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry; Montana State Univ., Bozeman, MT (United States). Thermal Biology Inst.
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF)
OSTI Identifier:
1400161
Grant/Contract Number:
AC05-00OR22725; SC0006654; DEB1134877; 2015066:MNL:11/19/2015
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Biochimica et Biophysica Acta - General Subjects
Additional Journal Information:
Journal Volume: 1861; Journal Issue: 9; Journal ID: ISSN 0304-4165
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Rawle, Rachel A., Hamerly, Timothy, Tripet, Brian P., Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, and Bothner, Brian. Multi-omics analysis provides insight to the Ignicoccus hospitalis - Nanoarchaeum equitans association. United States: N. p., 2017. Web. doi:10.1016/j.bbagen.2017.06.001.
Rawle, Rachel A., Hamerly, Timothy, Tripet, Brian P., Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, & Bothner, Brian. Multi-omics analysis provides insight to the Ignicoccus hospitalis - Nanoarchaeum equitans association. United States. doi:10.1016/j.bbagen.2017.06.001.
Rawle, Rachel A., Hamerly, Timothy, Tripet, Brian P., Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, and Bothner, Brian. Sun . "Multi-omics analysis provides insight to the Ignicoccus hospitalis - Nanoarchaeum equitans association". United States. doi:10.1016/j.bbagen.2017.06.001.
@article{osti_1400161,
title = {Multi-omics analysis provides insight to the Ignicoccus hospitalis - Nanoarchaeum equitans association},
author = {Rawle, Rachel A. and Hamerly, Timothy and Tripet, Brian P. and Giannone, Richard J. and Wurch, Louie and Hettich, Robert L. and Podar, Mircea and Copié, Valerie and Bothner, Brian},
abstractNote = {Studies of interspecies interactions are inherently difficult due to the complex mechanisms which enable these relationships. A model system for studying interspecies interactions is the marine hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans. Recent independently-conducted ‘omics’ analyses have generated insights into the molecular factors modulating this association. However, significant questions remain about the nature of the interactions between these archaea. We jointly analyzed multiple levels of omics datasets obtained from published, independent transcriptomics, proteomics, and metabolomics analyses. DAVID identified functionally-related groups enriched when I. hospitalis is grown alone or in co-culture with N. equitans. Enriched molecular pathways were subsequently visualized using interaction maps generated using STRING. Key findings of our multi-level omics analysis indicated that I. hospitalis provides precursors to N. equitans for energy metabolism. Analysis indicated an overall reduction in diversity of metabolic precursors in the I. hospitalis–N. equitans co-culture, which has been connected to the differential use of ribosomal subunits and was previously unnoticed. We also identified differences in precursors linked to amino acid metabolism, NADH metabolism, and carbon fixation, providing new insights into the metabolic adaptions of I. hospitalis enabling the growth of N. equitans. In conclusion, this multi-omics analysis builds upon previously identified cellular patterns while offering new insights into mechanisms that enable the I. hospitalis–N. equitans association. This study applies statistical and visualization techniques to a mixed-source omics dataset to yield a more global insight into a complex system, that was not readily discernable from separate omics studies.},
doi = {10.1016/j.bbagen.2017.06.001},
journal = {Biochimica et Biophysica Acta - General Subjects},
number = 9,
volume = 1861,
place = {United States},
year = {Sun Jun 04 00:00:00 EDT 2017},
month = {Sun Jun 04 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
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  • BACKGROUND: The relationship between the hyperthermophiles Ignicoccus hospitalis and Nanoarchaeum equitans is the only known example of a specific association between two species of Archaea. Little is known about the mechanisms that enable this relationship. RESULTS: We sequenced the complete genome of I. hospitalis and found it to be the smallest among independent, free-living organisms. A comparative genomic reconstruction suggests that the I. hospitalis lineage has lost most of the genes associated with a heterotrophic metabolism that is characteristic of most of the Crenarchaeota. A streamlined genome is also suggested by a low frequency of paralogs and fragmentation of manymore » operons. However, this process appears to be partially balanced by lateral gene transfer from archaeal and bacterial sources. CONCLUSIONS: A combination of genomic and cellular features suggests highly efficient adaptation to the low energy yield of sulfur-hydrogen respiration and efficient inorganic carbon and nitrogen assimilation. Evidence of lateral gene exchange between N. equitans and I. hospitalis indicates that the relationship has impacted both genomes. This association is the simplest symbiotic system known to date and a unique model for studying mechanisms of interspecific relationships at the genomic and metabolic levels.« less
  • Nanoarchaeum equitans, the only cultured representative of the Nanoarchaeota, is dependent on direct physical contact with its host, the hyperthermophile Ignicoccus hospitalis. The molecular mechanisms that enable this relationship are unknown. Using whole-cell proteomics, differences in the relative abundance of >75% of predicted protein-coding genes from both Archaea were measured to identify the specific response of I. hospitalis to the presence of N. equitans on its surface. A purified N. equitans sample was also analyzed for evidence of interspecies protein transfer. The depth of cellular proteome coverage achieved here is amongst the highest reported for any organism. Based on changesmore » in the proteome under the specific conditions of this study, I. hospitalis reacts to N. equitans by curtailing genetic information processing (replication, transcription) in lieu of intensifying its energetic, protein processing and cellular membrane functions. We found no evidence of significant Ignicoccus biosynthetic enzymes being transported to N. equitans. These results suggest that, under laboratory conditions, N. equitans diverts some of its host's metabolism and cell cycle control to compensate for its own metabolic shortcomings, thus appearing to be entirely dependent on small, transferable metabolites and energetic precursors from I. hospitalis.« less
  • Based on serial sectioning, focused ion beam scanning electron microscopy (FIB/SEM), and electron tomography, we depict in detail the highly unusual anatomy of the marine hyperthermophilic crenarchaeon, Ignicoccus hospitalis. Our data support a complex and dynamic endomembrane system consisting of cytoplasmic protrusions, and with secretory function. Moreover, we reveal that the cytoplasm of the putative archaeal ectoparasite Nanoarchaeum equitans can get in direct contact with this endomembrane system, complementing and explaining recent proteomic, transcriptomic and metabolomic data on this inter-archaeal relationship. In addition, we identified a matrix of filamentous structures and/or tethers in the voluminous inter-membrane compartment (IMC) of I.more » hospitalis, which might be responsible for membrane dynamics. Overall, this unusual cellular compartmentalization, ultrastructure and dynamics in an archaeon that belongs to the recently proposed TACK superphylum prompts speculation that the eukaryotic endomembrane system might originate from Archaea.« less