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

Author:

Raina Jean-Baptiste12345ORCID,Clode Peta L67,Cheong Soshan8,Bougoure Jeremy69,Kilburn Matt R6,Reeder Anthony6,Forêt Sylvain410ORCID,Stat Michael11,Beltran Victor2,Thomas-Hall Peter2,Tapiolas Dianne2,Motti Cherie M12,Gong Bill8,Pernice Mathieu3,Marjo Christopher E8,Seymour Justin R3,Willis Bette L145,Bourne David G25

Affiliation:

1. AIMS@JCU, James Cook University, Townsville, Australia

2. Australian Institute of Marine Science, Townsville, Australia

3. Climate Change Cluster, University of Technology Sydney, Sydney, Australia

4. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia

5. College of Science and Engineering, James Cook University, Townsville, Australia

6. The Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia

7. Oceans Institute, The University of Western Australia, Crawley, Australia

8. Mark Wainwright Analytical Centre, University of New South Wales, Kensington, Australia

9. School of Earth and Environment, The University of Western Australia, Crawley, Australia

10. Research School of Biology, Australian National University, Canberra, Australia

11. Trace and Environmental DNA Laboratory, Department of Environment and Agriculture, Curtin University, Perth, Australia

Abstract

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.

Funder

Australian Research Council

ANNiMS

AMMRF Centre for Microscopy, Characterisation and Analysis

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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