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Title: Systems Level Dissection of Anaerobic Methane Cycling: Quantitative Measurements of Single Cell Ecophysiology, Genetic Mechanisms, and Microbial Interactions

Abstract

The global biological CH4 cycle is largely controlled through coordinated and often intimate microbial interactions between archaea and bacteria, the majority of which are still unknown or have been only cursorily identified. Members of the methanotrophic archaea, aka ‘ANME’, are believed to play a major role in the cycling of methane in anoxic environments coupled to sulfate, nitrate, and possibly iron and manganese oxides, frequently forming diverse physical and metabolic partnerships with a range of bacteria. The thermodynamic challenges overcome by the ANME and their bacterial partners and corresponding slow rates of growth are common characteristics in anaerobic ecosystems, and, in stark contrast to most cultured microorganisms, this type of energy and resource limited microbial lifestyle is likely the norm in the environment. While we have gained an in-depth systems level understanding of fast-growing, energy-replete microorganisms, comparatively little is known about the dynamics of cell respiration, growth, protein turnover, gene expression, and energy storage in the slow-growing microbial majority. These fundamental properties, combined with the observed metabolic and symbiotic versatility of methanotrophic ANME, make these cooperative microbial systems a relevant (albeit challenging) system to study and for which to develop and optimize culture-independent methodologies, which enable a systems-level understanding ofmore » microbial interactions and metabolic networks. We used an integrative systems biology approach to study anaerobic sediment microcosms and methane-oxidizing bioreactors and expanded our understanding of the methanotrophic ANME archaea, their interactions with physically-associated bacteria, ecophysiological characteristics, and underlying genetic basis for cooperative microbial methane-oxidation linked with different terminal electron acceptors. Our approach is inherently multi-disciplinary and multi-scaled, combining transcriptional and proteomic analyses with high resolution microscopy techniques, and stable isotopic and chemical analyses that span community level ‘omics investigations (cm scale) to interspecies consortia (µm scale), to the individual cell and its subcellular components (nm scale). We have organized our methodological approach into three broad categories, RNA-based, Protein-targeted and Geochemical, each encompassing a range of scales, with many techniques and resulting datasets that are highly complementary with one another, and together, offer a unique systems-level perspective of methane-based microbial interactions.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [1];  [1];  [1];  [1];  [4];  [4];  [5];  [1];  [1];  [1]
  1. California Inst. of Technology (CalTech), Pasadena, CA (United States)
  2. Univ. of Queensland, Brisbane (Australia)
  3. Univ. of Georgia, Athens, GA (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  5. Univ. of California, San Diego, CA (United States)
Publication Date:
Research Org.:
California Inst. of Technology (CalTech), Pasadena, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
Joint Genome Institute, EMSL
OSTI Identifier:
1414771
Report Number(s):
DOE-CIT-10574
DOE Contract Number:  
SC0010574
Resource Type:
Technical Report
Resource Relation:
Related Information: DOE S#: S-143,734 Invention Title: Generation of Reduced Electron Carriers from Methane via Anaerobic Oxidation of Methane Reduction of Electron Shuttle Compounds via Anaerobic Oxidation of Methane
Country of Publication:
United States
Language:
English
Subject:
03 NATURAL GAS; 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Microbial syntrophy; anaerobic methane oxidation; interspecies electron transfer

Citation Formats

Orphan, Victoria, Tyson, Gene, Meile, Christof, McGlynn, Shawn, Yu, Hang, Chadwick, Grayson, Marlow, Jeffrey, Trembath-Reichert, Elizabeth, Dekas, Anne, Hettich, Robert, Pan, Chongle, Ellisman, Mark, Hatzenpichler, Roland, Skennerton, Connor, and Scheller, Silvan. Systems Level Dissection of Anaerobic Methane Cycling: Quantitative Measurements of Single Cell Ecophysiology, Genetic Mechanisms, and Microbial Interactions. United States: N. p., 2017. Web. doi:10.2172/1414771.
Orphan, Victoria, Tyson, Gene, Meile, Christof, McGlynn, Shawn, Yu, Hang, Chadwick, Grayson, Marlow, Jeffrey, Trembath-Reichert, Elizabeth, Dekas, Anne, Hettich, Robert, Pan, Chongle, Ellisman, Mark, Hatzenpichler, Roland, Skennerton, Connor, & Scheller, Silvan. Systems Level Dissection of Anaerobic Methane Cycling: Quantitative Measurements of Single Cell Ecophysiology, Genetic Mechanisms, and Microbial Interactions. United States. doi:10.2172/1414771.
Orphan, Victoria, Tyson, Gene, Meile, Christof, McGlynn, Shawn, Yu, Hang, Chadwick, Grayson, Marlow, Jeffrey, Trembath-Reichert, Elizabeth, Dekas, Anne, Hettich, Robert, Pan, Chongle, Ellisman, Mark, Hatzenpichler, Roland, Skennerton, Connor, and Scheller, Silvan. Mon . "Systems Level Dissection of Anaerobic Methane Cycling: Quantitative Measurements of Single Cell Ecophysiology, Genetic Mechanisms, and Microbial Interactions". United States. doi:10.2172/1414771. https://www.osti.gov/servlets/purl/1414771.
@article{osti_1414771,
title = {Systems Level Dissection of Anaerobic Methane Cycling: Quantitative Measurements of Single Cell Ecophysiology, Genetic Mechanisms, and Microbial Interactions},
author = {Orphan, Victoria and Tyson, Gene and Meile, Christof and McGlynn, Shawn and Yu, Hang and Chadwick, Grayson and Marlow, Jeffrey and Trembath-Reichert, Elizabeth and Dekas, Anne and Hettich, Robert and Pan, Chongle and Ellisman, Mark and Hatzenpichler, Roland and Skennerton, Connor and Scheller, Silvan},
abstractNote = {The global biological CH4 cycle is largely controlled through coordinated and often intimate microbial interactions between archaea and bacteria, the majority of which are still unknown or have been only cursorily identified. Members of the methanotrophic archaea, aka ‘ANME’, are believed to play a major role in the cycling of methane in anoxic environments coupled to sulfate, nitrate, and possibly iron and manganese oxides, frequently forming diverse physical and metabolic partnerships with a range of bacteria. The thermodynamic challenges overcome by the ANME and their bacterial partners and corresponding slow rates of growth are common characteristics in anaerobic ecosystems, and, in stark contrast to most cultured microorganisms, this type of energy and resource limited microbial lifestyle is likely the norm in the environment. While we have gained an in-depth systems level understanding of fast-growing, energy-replete microorganisms, comparatively little is known about the dynamics of cell respiration, growth, protein turnover, gene expression, and energy storage in the slow-growing microbial majority. These fundamental properties, combined with the observed metabolic and symbiotic versatility of methanotrophic ANME, make these cooperative microbial systems a relevant (albeit challenging) system to study and for which to develop and optimize culture-independent methodologies, which enable a systems-level understanding of microbial interactions and metabolic networks. We used an integrative systems biology approach to study anaerobic sediment microcosms and methane-oxidizing bioreactors and expanded our understanding of the methanotrophic ANME archaea, their interactions with physically-associated bacteria, ecophysiological characteristics, and underlying genetic basis for cooperative microbial methane-oxidation linked with different terminal electron acceptors. Our approach is inherently multi-disciplinary and multi-scaled, combining transcriptional and proteomic analyses with high resolution microscopy techniques, and stable isotopic and chemical analyses that span community level ‘omics investigations (cm scale) to interspecies consortia (µm scale), to the individual cell and its subcellular components (nm scale). We have organized our methodological approach into three broad categories, RNA-based, Protein-targeted and Geochemical, each encompassing a range of scales, with many techniques and resulting datasets that are highly complementary with one another, and together, offer a unique systems-level perspective of methane-based microbial interactions.},
doi = {10.2172/1414771},
journal = {},
number = ,
volume = ,
place = {United States},
year = {Mon Dec 25 00:00:00 EST 2017},
month = {Mon Dec 25 00:00:00 EST 2017}
}