Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria

Jean-Baptiste Raina; Peta L Clode; Soshan Cheong; Jeremy Bougoure; Matt R Kilburn; Anthony Reeder; Sylvain Forêt; Michael Stat; Victor Beltran; Peter Thomas-Hall; Dianne Tapiolas; Cherie M Motti; Bill Gong; Mathieu Pernice; Christopher E Marjo; Justin R Seymour; Bette L Willis; David G Bourne

doi:10.7554/eLife.23008

eLife (Apr 2017)

Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria

Jean-Baptiste Raina,
Peta L Clode,
Soshan Cheong,
Jeremy Bougoure,
Matt R Kilburn,
Anthony Reeder,
Sylvain Forêt,
Michael Stat,
Victor Beltran,
Peter Thomas-Hall,
Dianne Tapiolas,
Cherie M Motti,
Bill Gong,
Mathieu Pernice,
Christopher E Marjo,
Justin R Seymour,
Bette L Willis,
David G Bourne

Affiliations

Jean-Baptiste Raina: ORCiD; AIMS@JCU, James Cook University, Townsville, Australia; Australian Institute of Marine Science, Townsville, Australia; Climate Change Cluster, University of Technology Sydney, Sydney, Australia; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia; College of Science and Engineering, James Cook University, Townsville, Australia
Peta L Clode: The Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia; Oceans Institute, The University of Western Australia, Crawley, Australia
Soshan Cheong: Mark Wainwright Analytical Centre, University of New South Wales, Kensington, Australia
Jeremy Bougoure: The Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia; School of Earth and Environment, The University of Western Australia, Crawley, Australia
Matt R Kilburn: The Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia
Anthony Reeder: The Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia
Sylvain Forêt: ORCiD; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia; Research School of Biology, Australian National University, Canberra, Australia
Michael Stat: Trace and Environmental DNA Laboratory, Department of Environment and Agriculture, Curtin University, Perth, Australia
Victor Beltran: Australian Institute of Marine Science, Townsville, Australia
Peter Thomas-Hall: Australian Institute of Marine Science, Townsville, Australia
Dianne Tapiolas: Australian Institute of Marine Science, Townsville, Australia
Cherie M Motti: AIMS@JCU, James Cook University, Townsville, Australia; Australian Institute of Marine Science, Townsville, Australia
Bill Gong: Mark Wainwright Analytical Centre, University of New South Wales, Kensington, Australia
Mathieu Pernice: Climate Change Cluster, University of Technology Sydney, Sydney, Australia
Christopher E Marjo: Mark Wainwright Analytical Centre, University of New South Wales, Kensington, Australia
Justin R Seymour: Climate Change Cluster, University of Technology Sydney, Sydney, Australia
Bette L Willis: AIMS@JCU, James Cook University, Townsville, Australia; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia; College of Science and Engineering, James Cook University, Townsville, Australia
David G Bourne: Australian Institute of Marine Science, Townsville, Australia; College of Science and Engineering, James Cook University, Townsville, Australia

DOI: https://doi.org/10.7554/eLife.23008
Journal volume & issue: Vol. 6

Abstract

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Phytoplankton-bacteria interactions drive the surface ocean sulfur cycle and local climatic processes through the production and exchange of a key compound: dimethylsulfoniopropionate (DMSP). Despite their large-scale implications, these interactions remain unquantified at the cellular-scale. Here we use secondary-ion mass spectrometry to provide the first visualization of DMSP at sub-cellular levels, tracking the fate of a stable sulfur isotope (34S) from its incorporation by microalgae as inorganic sulfate to its biosynthesis and exudation as DMSP, and finally its uptake and degradation by bacteria. Our results identify for the first time the storage locations of DMSP in microalgae, with high enrichments present in vacuoles, cytoplasm and chloroplasts. In addition, we quantify DMSP incorporation at the single-cell level, with DMSP-degrading bacteria containing seven times more 34S than the control strain. This study provides an unprecedented methodology to label, retain, and image small diffusible molecules, which can be transposable to other symbiotic systems.

Published in eLife

ISSN: 2050-084X (Online)
Publisher: eLife Sciences Publications Ltd
Country of publisher: United Kingdom
LCC subjects: Medicine; Science: Biology (General)
Website: https://elifesciences.org

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