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 »
- Authors:
-
- Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology; Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
- Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
- 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 Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1400161
- Alternate Identifier(s):
- OSTI ID: 1550118
- Grant/Contract Number:
- AC05-00OR22725; SC0006654; DEB1134877; 2015066:MNL:11/19/2015
- Resource Type:
- 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. https://doi.org/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. https://doi.org/10.1016/j.bbagen.2017.06.001. https://www.osti.gov/servlets/purl/1400161.
@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}
}
Web of Science
Works referenced in this record:
Uncovering Hidden Layers of Cell Cycle Regulation through Integrative Multi-omic Analysis
journal, October 2015
- Aviner, Ranen; Shenoy, Anjana; Elroy-Stein, Orna
- PLOS Genetics, Vol. 11, Issue 10
Model‐driven multi‐omic data analysis elucidates metabolic immunomodulators of macrophage activation
journal, January 2012
- Bordbar, Aarash; Mo, Monica L.; Nakayasu, Ernesto S.
- Molecular Systems Biology, Vol. 8, Issue 1
A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides
journal, January 2012
- Zhu, Zhiwei; Zhang, Sufang; Liu, Hongwei
- Nature Communications, Vol. 3, Issue 1
A multi-omic analysis of human naïve CD4+ T cells
journal, November 2015
- Mitchell, Christopher J.; Getnet, Derese; Kim, Min-Sik
- BMC Systems Biology, Vol. 9, Issue 1
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015
- Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
- Nature, Vol. 521, Issue 7551
Community-integrated omics links dominance of a microbial generalist to fine-tuned resource usage
journal, November 2014
- Muller, Emilie E. L.; Pinel, Nicolás; Laczny, Cédric C.
- Nature Communications, Vol. 5, Issue 1
Dietary Modulation of Gut Microbiota Contributes to Alleviation of Both Genetic and Simple Obesity in Children
journal, August 2015
- Zhang, Chenhong; Yin, Aihua; Li, Hongde
- EBioMedicine, Vol. 2, Issue 8
Gut microbiota disturbance during antibiotic therapy: a multi-omic approach
journal, December 2012
- Pérez-Cobas, Ana Elena; Gosalbes, María José; Friedrichs, Anette
- Gut, Vol. 62, Issue 11
Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans'
journal, April 2007
- Paper, W.; Jahn, U.; Hohn, M. J.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 4
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002
- Huber, Harald; Hohn, Michael J.; Rachel, Reinhard
- Nature, Vol. 417, Issue 6884
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
journal, October 2003
- Waters, E.; Hohn, M. J.; Ahel, I.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea
journal, December 2007
- Jahn, U.; Gallenberger, M.; Paper, W.
- Journal of Bacteriology, Vol. 190, Issue 5
Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship
journal, August 2011
- Giannone, Richard J.; Huber, Harald; Karpinets, Tatiana
- PLoS ONE, Vol. 6, Issue 8
Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis
journal, November 2014
- Hamerly, Timothy; Tripet, Brian P.; Tigges, Michelle
- Metabolomics, Vol. 11, Issue 4
The unusual cell biology of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis
journal, June 2012
- Huber, Harald; Küper, Ulf; Daxer, Stefanie
- Antonie van Leeuwenhoek, Vol. 102, Issue 2
Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment
journal, July 2016
- Wurch, Louie; Giannone, Richard J.; Belisle, Bernard S.
- Nature Communications, Vol. 7, Issue 1
Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans
journal, July 2014
- Giannone, Richard J.; Wurch, Louie L.; Heimerl, Thomas
- The ISME Journal, Vol. 9, Issue 1
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
journal, November 2008
- Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
- Nucleic Acids Research, Vol. 37, Issue 1
The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored
journal, November 2010
- Szklarczyk, D.; Franceschini, A.; Kuhn, M.
- Nucleic Acids Research, Vol. 39, Issue Database
ESRP2 controls an adult splicing programme in hepatocytes to support postnatal liver maturation
journal, November 2015
- Bhate, Amruta; Parker, Darren J.; Bebee, Thomas W.
- Nature Communications, Vol. 6, Issue 1
Transcriptomic Changes in Coral Holobionts Provide Insights into Physiological Challenges of Future Climate and Ocean Change
journal, October 2015
- Kaniewska, Paulina; Chan, Chon-Kit Kenneth; Kline, David
- PLOS ONE, Vol. 10, Issue 10
Comprehensive transcriptional landscape of aging mouse liver
journal, November 2015
- White, Ryan R.; Milholland, Brandon; MacRae, Sheila L.
- BMC Genomics, Vol. 16, Issue 1
STRING v9.1: protein-protein interaction networks, with increased coverage and integration
journal, November 2012
- Franceschini, Andrea; Szklarczyk, Damian; Frankild, Sune
- Nucleic Acids Research, Vol. 41, Issue D1
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007
- Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
- Journal of Proteome Research, Vol. 6, Issue 2
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008
- Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
- Nature Protocols, Vol. 4, Issue 1
How fast-growing bacteria robustly tune their ribosome concentration to approximate growth-rate maximization
journal, March 2015
- Bosdriesz, Evert; Molenaar, Douwe; Teusink, Bas
- FEBS Journal, Vol. 282, Issue 10
Mass Spectrometry Defines the Stoichiometry of Ribosomal Stalk Complexes across the Phylogenetic Tree
journal, August 2010
- Gordiyenko, Yuliya; Videler, Hortense; Zhou, Min
- Molecular & Cellular Proteomics, Vol. 9, Issue 8
Zinc regulates a switch between primary and alternative S18 ribosomal proteins in M ycobacterium tuberculosis: Zinc-mediated switch of M. tuberculosis S18 proteins
journal, May 2015
- Prisic, Sladjana; Hwang, Hyonson; Dow, Allexa
- Molecular Microbiology, Vol. 97, Issue 2
A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis
journal, May 2008
- Huber, H.; Gallenberger, M.; Jahn, U.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 22, p. 7851-7856
Physiological and Proteomic Analysis of Escherichia coli Iron-Limited Chemostat Growth
journal, May 2014
- Folsom, J. P.; Parker, A. E.; Carlson, R. P.
- Journal of Bacteriology, Vol. 196, Issue 15
Moonlighting is mainstream: Paradigm adjustment required
journal, June 2012
- Copley, Shelley D.
- BioEssays, Vol. 34, Issue 7
Structural and Functional Analysis of the E. coli NusB-S10 Transcription Antitermination Complex
journal, December 2008
- Luo, Xiao; Hsiao, He-Hsuan; Bubunenko, Mikhail
- Molecular Cell, Vol. 32, Issue 6
Analysis of Nanoarchaeum equitans genome and proteome composition: indications for hyperthermophilic and parasitic adaptation
journal, July 2006
- Das, Sabyasachi; Paul, Sandip; Bag, Sumit K.
- BMC Genomics, Vol. 7, Issue 1
Works referencing / citing this record:
Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis
journal, September 2018
- Jarett, Jessica K.; Nayfach, Stephen; Podar, Mircea
- Microbiome, Vol. 6, Issue 1
Deep‐sea hydrothermal vent metagenome‐assembled genomes provide insight into the phylum Nanoarchaeota
journal, March 2019
- St. John, Emily; Flores, Gilberto E.; Meneghin, Jennifer
- Environmental Microbiology Reports, Vol. 11, Issue 2
Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
journal, July 2019
- Che, Shun; Men, Yujie
- Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10