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Title: Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy

Abstract

Phylogenetically diverse environmental ANME archaea and sulfate-reducing bacteria cooperatively catalyze the anaerobic oxidation of methane oxidation (AOM) in multicelled consortia within methane seep environments. To better understand these cells and their symbiotic associations, we applied a suite of electron microscopy approaches, including correlative fluorescence in situ hybridization-electron microscopy (FISH-EM), transmission electron microscopy (TEM), and serial block face scanning electron microscopy (SBEM) three-dimensional (3D) reconstructions. FISH-EM of methane seep-derived consortia revealed phylogenetic variability in terms of cell morphology, ultrastructure, and storage granules. Representatives of the ANME-2b clade, but not other ANME-2 groups, contained polyphosphate-like granules, while some bacteria associated with ANME-2a/2c contained two distinct phases of iron mineral chains resembling magnetosomes. 3D segmentation of two ANME-2 consortium types revealed cellular volumes of ANME and their symbiotic partners that were larger than previous estimates based on light microscopy. Polyphosphate-like granule-containing ANME (tentatively termed ANME-2b) were larger than both ANME with no granules and partner bacteria. This cell type was observed with up to 4 granules per cell, and the volume of the cell was larger in proportion to the number of granules inside it, but the percentage of the cell occupied by these granules did not vary with granule number. Here, thesemore » results illuminate distinctions between ANME-2 archaeal lineages and partnering bacterial populations that are apparently unified in their ability to perform anaerobic methane oxidation.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [3];  [3];  [4];  [2];  [5]
  1. California Inst. of Technology (CalTech), Pasadena, CA (United States); EN Center for Sustainable Resource Science (CSRS), Saitama (Japan); Tokyo Institute of Technology, Tokyo (Japan)
  2. California Inst. of Technology (CalTech), Pasadena, CA (United States)
  3. Univ. of California, San Diego (UCSD), La Jolla, CA (United States)
  4. Univ. of California, San Diego (UCSD), La Jolla, CA (United States); Salk Institute for Biological Sciences, La Jolla, CA (United States); HHMI Janelia Research Campus, Ashburn, VA (United States)
  5. Kyoto Univ., Kyoto (Japan)
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)
OSTI Identifier:
1529227
Grant/Contract Number:  
SC0004949
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 11; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ANME; DIET; polyphosphate metabolism; anaerobic methane oxidation; electron microscopy; fluorescence image analysis; sulfate reduction; syntrophy; ultrastructure

Citation Formats

McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., and Atomi, Haruyuki. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. United States: N. p., 2018. Web. doi:10.1128/aem.00399-18.
McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., & Atomi, Haruyuki. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. United States. doi:10.1128/aem.00399-18.
McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., and Atomi, Haruyuki. Fri . "Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy". United States. doi:10.1128/aem.00399-18. https://www.osti.gov/servlets/purl/1529227.
@article{osti_1529227,
title = {Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy},
author = {McGlynn, Shawn E. and Chadwick, Grayson L. and O'Neill, Ariel and Mackey, Mason and Thor, Andrea and Deerinck, Thomas J. and Ellisman, Mark H. and Orphan, Victoria J. and Atomi, Haruyuki},
abstractNote = {Phylogenetically diverse environmental ANME archaea and sulfate-reducing bacteria cooperatively catalyze the anaerobic oxidation of methane oxidation (AOM) in multicelled consortia within methane seep environments. To better understand these cells and their symbiotic associations, we applied a suite of electron microscopy approaches, including correlative fluorescence in situ hybridization-electron microscopy (FISH-EM), transmission electron microscopy (TEM), and serial block face scanning electron microscopy (SBEM) three-dimensional (3D) reconstructions. FISH-EM of methane seep-derived consortia revealed phylogenetic variability in terms of cell morphology, ultrastructure, and storage granules. Representatives of the ANME-2b clade, but not other ANME-2 groups, contained polyphosphate-like granules, while some bacteria associated with ANME-2a/2c contained two distinct phases of iron mineral chains resembling magnetosomes. 3D segmentation of two ANME-2 consortium types revealed cellular volumes of ANME and their symbiotic partners that were larger than previous estimates based on light microscopy. Polyphosphate-like granule-containing ANME (tentatively termed ANME-2b) were larger than both ANME with no granules and partner bacteria. This cell type was observed with up to 4 granules per cell, and the volume of the cell was larger in proportion to the number of granules inside it, but the percentage of the cell occupied by these granules did not vary with granule number. Here, these results illuminate distinctions between ANME-2 archaeal lineages and partnering bacterial populations that are apparently unified in their ability to perform anaerobic methane oxidation.},
doi = {10.1128/aem.00399-18},
journal = {Applied and Environmental Microbiology},
number = 11,
volume = 84,
place = {United States},
year = {2018},
month = {4}
}

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Works referenced in this record:

Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments
journal, May 2002

  • Orphan, V. J.; House, C. H.; Hinrichs, K.-U.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668
  • DOI: 10.1073/pnas.072210299