Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria
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 w...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/23008 |
| _version_ | 1811180383871434752 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Jean-Baptiste Raina |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T09:01:06Z |
| format | Article |
| id | doaj.art-eaf4018f566a4cbe917c491891bc6d16 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:01:06Z |
| publishDate | 2017-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-eaf4018f566a4cbe917c491891bc6d162022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.23008Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteriaJean-Baptiste Raina0https://orcid.org/0000-0002-7508-0004Peta L Clode1Soshan Cheong2Jeremy Bougoure3Matt R Kilburn4Anthony Reeder5Sylvain Forêt6https://orcid.org/0000-0002-4145-9243Michael Stat7Victor Beltran8Peter Thomas-Hall9Dianne Tapiolas10Cherie M Motti11Bill Gong12Mathieu Pernice13Christopher E Marjo14Justin R Seymour15Bette L Willis16David G Bourne17AIMS@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, AustraliaThe Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia; Oceans Institute, The University of Western Australia, Crawley, AustraliaMark Wainwright Analytical Centre, University of New South Wales, Kensington, AustraliaThe Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, Australia; School of Earth and Environment, The University of Western Australia, Crawley, AustraliaThe Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, AustraliaThe Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Crawley, AustraliaARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia; Research School of Biology, Australian National University, Canberra, AustraliaTrace and Environmental DNA Laboratory, Department of Environment and Agriculture, Curtin University, Perth, AustraliaAustralian Institute of Marine Science, Townsville, AustraliaAustralian Institute of Marine Science, Townsville, AustraliaAustralian Institute of Marine Science, Townsville, AustraliaAIMS@JCU, James Cook University, Townsville, Australia; Australian Institute of Marine Science, Townsville, AustraliaMark Wainwright Analytical Centre, University of New South Wales, Kensington, AustraliaClimate Change Cluster, University of Technology Sydney, Sydney, AustraliaMark Wainwright Analytical Centre, University of New South Wales, Kensington, AustraliaClimate Change Cluster, University of Technology Sydney, Sydney, AustraliaAIMS@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, AustraliaAustralian Institute of Marine Science, Townsville, Australia; College of Science and Engineering, James Cook University, Townsville, AustraliaPhytoplankton-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.https://elifesciences.org/articles/23008phytoplankton-bacteriaNanoSIMSToF-SIMSbiogeochemical cyclingsymbiosis |
| spellingShingle | 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 Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria eLife phytoplankton-bacteria NanoSIMS ToF-SIMS biogeochemical cycling symbiosis |
| title | Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| title_full | Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| title_fullStr | Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| title_full_unstemmed | Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| title_short | Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| title_sort | subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria |
| topic | phytoplankton-bacteria NanoSIMS ToF-SIMS biogeochemical cycling symbiosis |
| url | https://elifesciences.org/articles/23008 |
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