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Subgroup characteristics of marine methane-oxidizing ANME-2 archaea and their syntrophic partners revealed by integrated multimodal analytical microscopy

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. (2018) Subgroup characteristics of marine methane-oxidizing ANME-2 archaea and their syntrophic partners revealed by integrated multimodal analytical microscopy. Applied and Environmental Microbiology, 84 (11). Art. No. e00399-18. ISSN 0099-2240. PMCID PMC5960974. https://resolver.caltech.edu/CaltechAUTHORS:20180411-080037971

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/AEM.00399-18DOIArticle
http://aem.asm.org/content/84/11/e00399-18/suppl/DCSupplementalPublisherSupplementary Material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960974/PubMed CentralArticle
ORCID:
AuthorORCID
McGlynn, Shawn E.0000-0002-8199-7011
Chadwick, Grayson L.0000-0003-0700-9350
Ellisman, Mark H.0000-0001-8893-8455
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2018 American Society for Microbiology. Received 15 February 2018; Accepted 31 March 2018; Accepted manuscript posted online 6 April 2018. We are grateful for the use of the facilities of the Beckman Resource Center for Transmission Electron Microscopy at Caltech (BRCem) and helpful advice from Alasdair McDowall and Mark Ladinsky. This work also benefited from the Applied Physics and Materials Science Department's Transmission Electron Microscopy Facility at Caltech, where EDS measurements were made with Carol M. Garland. This work was funded by the U.S. Department of Energy, Office of Science, Office of Biological Environmental Research, under award numbers DE-SC0004949 and DE-SC0010574 and by a grant from the Gordon and Betty Moore Foundation Marine Microbiology Initiative (grant number 3780), both to V.J.O. S.E.M. was supported in part by an MEXT KAKENHI Grant-in-Aid for challenging exploratory research (grant award number 15K14608) and the Research Foundation for Opto-Science and Technology. New correlated microscopy and 3D EM method development, as well as access to advanced imaging resources housed at UCSD, was supported by a grant from the NIH National Institute of General Medical Sciences (number P41GM103412 to M.H.E.), an award which partially supports the National Center for Microscopy and Imaging Research.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0004949
Department of Energy (DOE)DE-SC0010574
Gordon and Betty Moore Foundation3780
Ministry of Education, Culture, Sports, Science and Technology (MEXT)15K14608
Research Foundation for Opto-Science and TechnologyUNSPECIFIED
NIHP41GM103412
Subject Keywords:ANME; DIET; polyphosphate metabolism; anaerobic methane oxidation; electron microscopy; fluorescence image analysis; sulfate reduction; syntrophy; ultrastructure
Issue or Number:11
PubMed Central ID:PMC5960974
Record Number:CaltechAUTHORS:20180411-080037971
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180411-080037971
Official Citation:McGlynn SE, Chadwick GL, O'Neill A, Mackey M, Thor A, Deerinck TJ, Ellisman MH, Orphan VJ. 2018. Subgroup characteristics of marine methane-oxidizing ANME-2 archaea and their syntrophic partners as revealed by integrated multimodal analytical microscopy. Appl Environ Microbiol 84:e00399-18. https://doi.org/10.1128/AEM.00399-18
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:85740
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:11 Apr 2018 15:50
Last Modified:03 Oct 2019 19:35

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