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Title: From genomes to metabolomes: Understanding mechanisms of symbiosis and cell-cell signaling using the archaeal system Ignicoccus-Nanoarchaeum

Abstract

The main objective of this project was to use symbiotic Nanoarchaeaota, a group of thermophilic Archaea that are obligate symbionts/parasites on other Archaea, to develop an integrated multi-omic approach to study inter-species interactions as well as to understand fundamental mechanism that enable such relationships. As part of this grant we have achieved a number of important milestone on both technical and scientific levels. On the technical side, we developed immunofluorescence labeling and tracking methods to follow Nanoarchaeota in cultures and in environmental samples, we applied such methods in conjunction with flow cytometry to quantify and isolate uncultured representatives from the environment and characterized them by single cell genomics. On the proteomics side, we developed a more efficient and sensitive method to recover and semi-quantitatively measure membrane proteins, while achieving high total cellular proteome coverage (70-80% of the predicted proteome). Metabolomic analyses used complementary NMR and LC/GC mass spectrometry and led to the identification of novel lipids in these organisms as well as quantification of some of the major metabolites. Importantly, using several informatics approaches we were also able to integrate the transcriptomic, proteomic and metabolomic datasets, revealing aspects of the interspecies interaction that were not evident in the single omicmore » analyses (manuscript in review). On the science side we determined that N. equitans and I. hospitalis are metabolically coupled and that N. equitans is strictly dependent on its host both for metabolic precursors and energetic needs. The actual mechanism by which small molecules move across the cell membrane remains unknown. The Ignicoccus host responds to the metabolic and energetic burned by upregulating of key primary metabolism steps and ATP synthesis. The two species have co-evolved, aspect that we determined by comparative genomics with other species of Ignicoccus (manuscript in preparation) and by characterizing other similar Nanoarchaeota systems. Using a single cell genomics approach we characterized the first terrestrial geothermal Nanoarchaeota system, from Yellowstone National Park. That nanoarchaeon uses a different host, a species of Sulfolobales, and comparative genomics with N. equitans-Ignicoccus allowed us to come up with an evolutionary model for the evolution of this group of organisms across marine and terrestrial ecosystems. Based on metabolic inferences we were also able to isolate in culture the first such terrestrial nanoarchaeal system, also from Yellowstone, which involves a species of Acidilobus. The novel nanoarchaeal system was characterized using proteomics and it helped us better understand the metabolic capabilities of these organisms as well as how co-evolution shapes the genomes of interacting species. It was also one of the very few cases in which prior genomic data was used to successfully design an approach to culture an organism, which remains the gold standard in microbiology research. As a better understanding of interspecies interaction requires multiple model systems, we have pursued identification and genomic characterization or isolation of additional nanoarchaeal systems from geographically and geochemically distinct environments. Two additional nanoarchaeal systems are presently being characterized from hot springs in Yellowstone and Iceland and will be the subject to future publications.« less

Authors:
 [1];  [1];  [2];  [2]
  1. Univ. of Tennessee, Knoxville, TN (United States). Biosciences Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)]
  2. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
Publication Date:
Research Org.:
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
Montana State Univ., Bozeman, MT (United States)
OSTI Identifier:
1336183
Report Number(s):
DOE-UTK-SC0006654
DOE Contract Number:  
SC0006654
Resource Type:
Technical Report
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Podar, Mircea, Hettich, Robert, Copie, Valerie, and Bothner, Brian. From genomes to metabolomes: Understanding mechanisms of symbiosis and cell-cell signaling using the archaeal system Ignicoccus-Nanoarchaeum. United States: N. p., 2016. Web. doi:10.2172/1336183.
Podar, Mircea, Hettich, Robert, Copie, Valerie, & Bothner, Brian. From genomes to metabolomes: Understanding mechanisms of symbiosis and cell-cell signaling using the archaeal system Ignicoccus-Nanoarchaeum. United States. doi:10.2172/1336183.
Podar, Mircea, Hettich, Robert, Copie, Valerie, and Bothner, Brian. Fri . "From genomes to metabolomes: Understanding mechanisms of symbiosis and cell-cell signaling using the archaeal system Ignicoccus-Nanoarchaeum". United States. doi:10.2172/1336183. https://www.osti.gov/servlets/purl/1336183.
@article{osti_1336183,
title = {From genomes to metabolomes: Understanding mechanisms of symbiosis and cell-cell signaling using the archaeal system Ignicoccus-Nanoarchaeum},
author = {Podar, Mircea and Hettich, Robert and Copie, Valerie and Bothner, Brian},
abstractNote = {The main objective of this project was to use symbiotic Nanoarchaeaota, a group of thermophilic Archaea that are obligate symbionts/parasites on other Archaea, to develop an integrated multi-omic approach to study inter-species interactions as well as to understand fundamental mechanism that enable such relationships. As part of this grant we have achieved a number of important milestone on both technical and scientific levels. On the technical side, we developed immunofluorescence labeling and tracking methods to follow Nanoarchaeota in cultures and in environmental samples, we applied such methods in conjunction with flow cytometry to quantify and isolate uncultured representatives from the environment and characterized them by single cell genomics. On the proteomics side, we developed a more efficient and sensitive method to recover and semi-quantitatively measure membrane proteins, while achieving high total cellular proteome coverage (70-80% of the predicted proteome). Metabolomic analyses used complementary NMR and LC/GC mass spectrometry and led to the identification of novel lipids in these organisms as well as quantification of some of the major metabolites. Importantly, using several informatics approaches we were also able to integrate the transcriptomic, proteomic and metabolomic datasets, revealing aspects of the interspecies interaction that were not evident in the single omic analyses (manuscript in review). On the science side we determined that N. equitans and I. hospitalis are metabolically coupled and that N. equitans is strictly dependent on its host both for metabolic precursors and energetic needs. The actual mechanism by which small molecules move across the cell membrane remains unknown. The Ignicoccus host responds to the metabolic and energetic burned by upregulating of key primary metabolism steps and ATP synthesis. The two species have co-evolved, aspect that we determined by comparative genomics with other species of Ignicoccus (manuscript in preparation) and by characterizing other similar Nanoarchaeota systems. Using a single cell genomics approach we characterized the first terrestrial geothermal Nanoarchaeota system, from Yellowstone National Park. That nanoarchaeon uses a different host, a species of Sulfolobales, and comparative genomics with N. equitans-Ignicoccus allowed us to come up with an evolutionary model for the evolution of this group of organisms across marine and terrestrial ecosystems. Based on metabolic inferences we were also able to isolate in culture the first such terrestrial nanoarchaeal system, also from Yellowstone, which involves a species of Acidilobus. The novel nanoarchaeal system was characterized using proteomics and it helped us better understand the metabolic capabilities of these organisms as well as how co-evolution shapes the genomes of interacting species. It was also one of the very few cases in which prior genomic data was used to successfully design an approach to culture an organism, which remains the gold standard in microbiology research. As a better understanding of interspecies interaction requires multiple model systems, we have pursued identification and genomic characterization or isolation of additional nanoarchaeal systems from geographically and geochemically distinct environments. Two additional nanoarchaeal systems are presently being characterized from hot springs in Yellowstone and Iceland and will be the subject to future publications.},
doi = {10.2172/1336183},
journal = {},
number = ,
volume = ,
place = {United States},
year = {2016},
month = {12}
}

Works referenced in this record:

Rescuing Those Left Behind: Recovering and Characterizing Underdigested Membrane and Hydrophobic Proteins To Enhance Proteome Measurement Depth
journal, July 2015


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
  • DOI: 10.1038/ismej.2014.112

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
  • DOI: 10.1038/ncomms12115