Tags

Type your tag names separated by a space and hit enter

Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy.
Appl Environ Microbiol. 2018 06 01; 84(11)AE

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. 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.IMPORTANCE Methane oxidation in anaerobic environments can be accomplished by a number of archaeal groups, some of which live in syntrophic relationships with bacteria in structured consortia. Little is known of the distinguishing characteristics of these groups. Here, we applied imaging approaches to better understand the properties of these cells. We found unexpected morphological, structural, and volume variability of these uncultured groups by correlating fluorescence labeling of cells with electron microscopy observables.

Authors+Show Affiliations

Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA mcglynn@elsi.jp vorphan@gps.caltech.edu. Biofunctional Catalyst Research Team, RIKEN Center for Sustainable Resource Science (CSRS), Wako, Saitama, Japan. Earth-Life Science Institute, Tokyo Institute of Technology, Meguro, Tokyo, Japan.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA.National Center of Microscopy and Imaging Research (NCMIR), Center for Research on Biological Systems, University of California, San Diego (UCSD), School of Medicine, La Jolla, California, USA.National Center of Microscopy and Imaging Research (NCMIR), Center for Research on Biological Systems, University of California, San Diego (UCSD), School of Medicine, La Jolla, California, USA.National Center of Microscopy and Imaging Research (NCMIR), Center for Research on Biological Systems, University of California, San Diego (UCSD), School of Medicine, La Jolla, California, USA.National Center of Microscopy and Imaging Research (NCMIR), Center for Research on Biological Systems, University of California, San Diego (UCSD), School of Medicine, La Jolla, California, USA. Department of Neurosciences, UCSD, La Jolla, California, USA. Salk Institute for Biological Sciences, La Jolla, California, USA. HHMI Janelia Research Campus, Ashburn, Virginia, USA.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA mcglynn@elsi.jp vorphan@gps.caltech.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

29625978

Citation

McGlynn, Shawn E., et al. "Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed By Integrated Multimodal Analytical Microscopy." Applied and Environmental Microbiology, vol. 84, no. 11, 2018.
McGlynn SE, Chadwick GL, O'Neill A, et al. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. Appl Environ Microbiol. 2018;84(11).
McGlynn, S. E., Chadwick, G. L., O'Neill, A., Mackey, M., Thor, A., Deerinck, T. J., Ellisman, M. H., & Orphan, V. J. (2018). Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. Applied and Environmental Microbiology, 84(11). https://doi.org/10.1128/AEM.00399-18
McGlynn SE, et al. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed By Integrated Multimodal Analytical Microscopy. Appl Environ Microbiol. 2018 06 1;84(11) PubMed PMID: 29625978.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. AU - McGlynn,Shawn E, AU - Chadwick,Grayson L, AU - O'Neill,Ariel, AU - Mackey,Mason, AU - Thor,Andrea, AU - Deerinck,Thomas J, AU - Ellisman,Mark H, AU - Orphan,Victoria J, Y1 - 2018/05/17/ PY - 2018/02/15/received PY - 2018/03/31/accepted PY - 2018/4/8/pubmed PY - 2019/9/29/medline PY - 2018/4/8/entrez KW - ANME KW - DIET KW - anaerobic methane oxidation KW - electron microscopy KW - fluorescence image analysis KW - polyphosphate metabolism KW - sulfate reduction KW - syntrophy KW - ultrastructure JF - Applied and environmental microbiology JO - Appl. Environ. Microbiol. VL - 84 IS - 11 N2 - 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. 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.IMPORTANCE Methane oxidation in anaerobic environments can be accomplished by a number of archaeal groups, some of which live in syntrophic relationships with bacteria in structured consortia. Little is known of the distinguishing characteristics of these groups. Here, we applied imaging approaches to better understand the properties of these cells. We found unexpected morphological, structural, and volume variability of these uncultured groups by correlating fluorescence labeling of cells with electron microscopy observables. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/29625978/Subgroup_Characteristics_of_Marine_Methane_Oxidizing_ANME_2_Archaea_and_Their_Syntrophic_Partners_as_Revealed_by_Integrated_Multimodal_Analytical_Microscopy_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=29625978 DB - PRIME DP - Unbound Medicine ER -