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Single cell activity reveals direct electron transfer in methanotrophic consortia

McGlynn, Shawn E. and Chadwick, Grayson L. and Kempes, Christopher P. and Orphan, Victoria J. (2015) Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature, 526 (7574). pp. 531-535. ISSN 0028-0836. http://resolver.caltech.edu/CaltechAUTHORS:20150729-141906854

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[img] Image (JPEG) (Extended Data Figure 1: Image processing workflow for single cell correlation between FISH and nanoSIMS data sets) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 2: Spatial and geometric relationships for modelled aggregate geometries (well mixed to segregated) as a function of relative diffusivity (the ratio of growth rates to growth yields and diffusivity) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 3: Summary of aggregate characteristics) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 4: Illustration of the value of single-cell resolution activity analysis) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 5: Evaluation of metrics for partner mixing) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 6: Insensitivity of cell activities to distance from nearest syntrophic partner for AD consortia) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 7: Schematic of network analysis for microbial consortia) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 8: Insensitivity of cell activities to distance from surface) - Supplemental Material
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[img] Image (JPEG) (Extended Data Figure 9: Spatial and geometric relationships for all modelled aggregate geometries as a function of relative conductivity within the direct electron transfer model) - Supplemental Material
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Abstract

Multicellular assemblages of microorganisms are ubiquitous in nature, and the proximity afforded by aggregation is thought to permit intercellular metabolic coupling that can accommodate otherwise unfavourable reactions. Consortia of methane-oxidizing archaea and sulphate-reducing bacteria are a well-known environmental example of microbial co-aggregation; however, the coupling mechanisms between these paired organisms is not well understood, despite the attention given them because of the global significance of anaerobic methane oxidation. Here we examined the influence of interspecies spatial positioning as it relates to biosynthetic activity within structurally diverse uncultured methane-oxidizing consortia by measuring stable isotope incorporation for individual archaeal and bacterial cells to constrain their potential metabolic interactions. In contrast to conventional models of syntrophy based on the passage of molecular intermediates, cellular activities were found to be independent of both species intermixing and distance between syntrophic partners within consortia. A generalized model of electric conductivity between co-associated archaea and bacteria best fit the empirical data. Combined with the detection of large multi-haem cytochromes in the genomes of methanotrophic archaea and the demonstration of redox-dependent staining of the matrix between cells in consortia, these results provide evidence for syntrophic coupling through direct electron transfer.


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http://dx.doi.org/10.1038/nature15512DOIArticle
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ORCID:
AuthorORCID
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2015 Macmillan Publishers Limited. Received 06 March 2015 Accepted 10 August 2015 Published online 16 September 2015. We are grateful for the use of the facilities of the Beckman Resource Center for Transmission Electron Microscopy at Caltech (BRCem) and advice provided by A. McDowall, our collaborators T. Deerinck and M. Ellisman from the National Center for Microscopy and Imaging Research (NCMIR), C. Miele (UGA) and M. El-Naggar at USC. Metagenomic binning of ANME-2b was conducted by C. Skennerton and M. Haroon in collaboration with G. Tyson and M. Imelfort (University of Queensland). This work was supported by the US Department of Energy, Office of Science, Office of Biological Environmental Research under award numbers (DE-SC0004949 and DE-SC0010574) and a grant from the Gordon and Betty Moore foundation Marine Microbiology Initiative (grant number 3780). V.J.O. is supported by a DOE-BER early career grant (DE-SC0003940). S.E.M. acknowledges support from an Agouron Geobiology Option post-doctoral fellowship in the Division of Geological and Planetary Sciences at Caltech and C.P.K. was supported by the NASA Astrobiology Institute (award number NNA13AA92A). This is NAI-Life Underground Publication 049. Author Contributions: V.J.O., S.M. and G.L.C. devised the study, S.M. and G.L.C. conducted the experiments and analyses and C.P.K. conducted the diffusion and electrical conductivity modelling, and all authors contributed to data interpretation and writing of the manuscript.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0004949
Department of Energy (DOE)DE-SC0010574
Gordon and Betty Moore Foundation3780
Department of Energy (DOE)DE-SC0003940
Agouron InstituteUNSPECIFIED
NASANNA13AA92A
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NAI-Life Underground049
Record Number:CaltechAUTHORS:20150729-141906854
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20150729-141906854
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:59070
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:17 Sep 2015 16:22
Last Modified:30 Nov 2015 17:00

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