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

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.DOI: http://dx.doi.org/10.7554/eLife.23008.001

Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks

“…Imaging techniques, such as transmission electron microscopy, have been applied to investigate viral‐mediated coral bleaching and disease (Wilson et al ., ; Davy et al ., ) and have the potential to be applied to observe Symbiodiniaceae‐bacteria associations. Molecular exchange can be measured and visualized at the cellular level using stable isotopic labelling combined with nanoscale secondary‐ion mass spectrometry (NanoSIMS) (Raina et al ., ). Identification and quantification of key metabolites and metabolic pathway activity could be achieved with the integration of metabolomic and transcriptomics analyses, as was recently applied to elucidate mechanisms underlying symbiont compatibility in the Aiptasia‐Symbiodiniaceae symbiosis (Matthews et al ., ).…”

“…Only a few studies have specifically considered Symbiodiniaceae‐bacterial interactions in the coral holobiont, with their results pointing to the potentially critical role that these partnerships might play in regulating holobiont nutrient cycling and competitive fitness (Ritchie, ; Bourne et al ., ; Ainsworth et al ., ; Peixoto et al ., ; Silveira et al ., ; Bernasconi et al ., ); Table ). For example, some coral‐associated bacteria can rapidly take up organosulfur compounds released by Symbiodiniaceae cells, such as dimethylsulfoniopropionate (DMSP), to sustain their growth and produce an antimicrobial compound active against common coral pathogens (Raina et al ., ; Raina et al ., ). The stability of coral‐associated bacterial communities during thermal stress is correlated to the Symbiodiniaceae spp.…”

Ecology and Biotechnological Potential of Bacteria Belonging to the Genus Pseudovibrio

“…This compound is found also in corals and coral mucus, where it can reach a concentration orders of magnitude higher than in the surrounding water, indicating the pivotal role of coral reefs in the oceanic DMSP cycle (56). DMSP has been shown to be used by multiple Pseudovibrio strains as a source of energy and carbon (Table 1) (48,57), and recently, the ability to both assimilate it with other sulfur-containing metabolites produced by the zooxantella Symbiodinium, and use it as sulfur source were shown as well (58,59).…”

Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution

“…We combined ultrastructural analyses, which were executed with a transmission electron microscope (TEM), correlated with nanometre scale secondary ion mass spectrometry (NanoSIMS) imaging (Hoppe et al ., ; Nuñez et al ., ) to localize isotopically labelled 15 N, 13 C and 34 S compounds at a sub‐cellular level and to correlate the elemental isotopic composition with ultrastructural features of N. labradorica . This TEM‐NanoSIMS analysis has revealed the fate of isotopically labelled compounds in diverse marine microorganisms (Finzi‐Hart et al ., ; Pernice et al ., ; Kopp et al ., ; ; Raina et al ., ), including foraminifera (Nomaki et al ., ; LeKieffre et al ., ; ). Additionally, microelectrodes were used to determine the oxygen dynamics around N. labradorica as a function of artificial light exposure (Rink et al ., ; Geslin et al ., ), in order to link C and N assimilation with potential photosynthetic activity.…”