Periodic Reporting for period 4 - SUMMIT (Novel roles of dimethylated sulphur in marine microbial interactions)
Okres sprawozdawczy: 2024-03-01 do 2025-08-31
Sulfur is an essential element for life that cycles rapidly in the pelagic ocean in the form of biogenic dimethylated compounds. There is functional and quantitative evidence that these organosulfur compounds are integral to the food web machinery, but their exact roles in the functioning of marine ecosystems remain largely unexplored. This is particularly important now that a renewed picture of marine food webs emerges, where classical functional roles (producer/consumer/decomposer) blur and concepts like multifunctional organisms and functional interdependence become the rule rather than the exception. Food webs are the core of marine ecosystem services like biodiversity and genetic resources, food provision, and CO2 sequestration. We can hardly understand (hence model and predict) the evolution marine ecosystem services if we do not understand how food webs work.
The SUMMIT project aimed to bridge microbial physiology, ecology and biogeochemistry to investigate the roles of demethylated sulfur compounds in shaping microbial interactions that are fundamental for the functioning of marine ecosystems. As part of (1) phytoplankton-bacteria interactions, SUMMIT has demonstrated that the main algal sulfur-containing osmolyte (named DMSP) is a strong chemoattractant for chemotactic bacteria, more so in synergy with other algal exudates; SUMMIT has also demonstrated that algal-derived compounds trigger the fixation atmospheric nitrogen by heterotrophic bacteria; SUMMIT has shown how the variability of sulfur cycling among phytoplankton and bacteria can be approached through the transcription of the relevant genes. With respect to (2) phytoplankton-phytoplankton interactions, SUMMIT has confirmed that phytoplankton are not only the main producers of the osmolyte DMSP but also consumers, has identified the protein that allows the uptake of external DMSP, and has shown that uptake of external DMSP helps to overcome energy limitation to growth. Finally, by studying (3) phytoplankton-herbivore interactions, SUMMIT has demonstrated there is chemically-oriented selective grazing by predatory protists using algal-released DMSP as the chemical cue, and this selective grazing enhances the recovery of phytoplankton prey populations from physiological stress. Finally, SUMMIT has developed a numerical model that does a better job than previous models to describe sulfur cycling throughout algal blooms. SUMMIT has also developed improved diagnostic models for the distribution and emission of volatile sulfur across the global ocean, present and future.
The SUMMIT project aimed to bridge microbial physiology, ecology and biogeochemistry to investigate the roles of demethylated sulfur compounds in shaping microbial interactions that are fundamental for the functioning of marine ecosystems. As part of (1) phytoplankton-bacteria interactions, SUMMIT has demonstrated that the main algal sulfur-containing osmolyte (named DMSP) is a strong chemoattractant for chemotactic bacteria, more so in synergy with other algal exudates; SUMMIT has also demonstrated that algal-derived compounds trigger the fixation atmospheric nitrogen by heterotrophic bacteria; SUMMIT has shown how the variability of sulfur cycling among phytoplankton and bacteria can be approached through the transcription of the relevant genes. With respect to (2) phytoplankton-phytoplankton interactions, SUMMIT has confirmed that phytoplankton are not only the main producers of the osmolyte DMSP but also consumers, has identified the protein that allows the uptake of external DMSP, and has shown that uptake of external DMSP helps to overcome energy limitation to growth. Finally, by studying (3) phytoplankton-herbivore interactions, SUMMIT has demonstrated there is chemically-oriented selective grazing by predatory protists using algal-released DMSP as the chemical cue, and this selective grazing enhances the recovery of phytoplankton prey populations from physiological stress. Finally, SUMMIT has developed a numerical model that does a better job than previous models to describe sulfur cycling throughout algal blooms. SUMMIT has also developed improved diagnostic models for the distribution and emission of volatile sulfur across the global ocean, present and future.
Work performed:
(1) Phytoplankton – bacterial interactions:
-We combined measurements of organosulfur concentrations and cycling rates with sequencing of taxonomic and functional genes, to assess if microbial activity rates can be predicted by the occurrence and expression of the relevant genes. This has been conducted with sample collections from previous expeditions to Antarctic and tropics as well as from the SUMMIT Mediterranean cruise (June 2021). [Masdeu-Navarro et al., Front. Mar. Sci. 9: 944141 (2022); Mangot, Simó et al., in preparation]
-During the SUMMIT-Moorea Expedition, additions of dimethylsulfoniopropionate (DMSP), acrylate, and glucose triggered N2 fixation rates by heterotrophic bacteria, and we are currently investigating how they upregulated the expression of N2 fixation genes. [Cerdán et al., in preparation]
-We conducted in situ chemotaxis assays (ISCA) to investigate if diazotrophs (N2 fixers) are enriched among bacteria attracted by DMSP [Mangot et al., work in progress]. ISCAs also served to demonstrate synergistic attraction of bacteria by DMSP and polysaccharides [Clerc et al., Nature Comm. 14: 8080 (2023)]
-We experimentally showed that marine sponges and their endosymbiotic bacteria consume volatile sulfur and bromine-containing compounds. [Simó et al., in review in Environ. Sci. Technol.]
-We described the distribution of sulfur compounds, alkylamines and other volatiles in Antarctic seawaters and sea ice. [Rocchi et al., Biogeosci. 22: 3429–3448 (2025); Crabeck et al., in review in Elementa]
-We showed how the volatile compound isoprene is consumed in the surface ocean. [Simó et al., Comm. Earth Environ. 3: 20 (2022)]
(2) Phytoplankton – phytoplankton interactions:
-We have identified the membrane transporter for the uptake of the algal osmolyte DMSP by eukaryotic phytoplankton. The candidate protein was suggested by radioisotope and transcriptomic assays, and its function was confirmed by functional complementation of a mutant of the bacterium Escherichia coli with the PaDT gene from a eukaryotic picoalga. Further experiments supported that exogenous DMSP incorporation as an energy-saving strategy. Finally, we showed the global and taxonomic spread of PaDT expression in the surface ocean. [Simó et al., submitted (2025)]
(3) Predator – phytoplankton interactions:
-We conducted chemotaxis experiments to investigate if protist grazing on phytoplankton is modulated by chemical signals, and if this oriented grazing facilitates the recovery of the prey population from physiological stress. Video cell tracking of predator swimming, cell counting of prey, and measurement of prey physiological stress level and recovery enabled to confirm that model herbivore protists are attracted by the algal osmolyte DMSP, this induces preferential grazing on sunlight-stressed algal cells, and subsequently accelerates prey population recovery from stress. [Güell-Bujons et al., ISME J. 18: wrae130 (2024); Güell-Bujons et al., in preparation]
-We investigated how organosulfur compounds are involved in phytoplankton bloom biomass control by viruses. [Vincent et al., Nature Comm. 4: 510 (2023); Vaqué et al., Antarctic Sci. 37: 265-277 (2025)]
(4) Modelling:
-We developed a numerical 1D model of organosulphur cycling across microbial food web interactions. [LeGland et al., Limnol Oceanogr. 69: 140-157 (2023)]
- We developed diagnostic and machine learning models for a revised assessment of the climate effects of global oceanic emissions of volatile sulfur in present and future scenarios [Wohl et al., Sci. Adv. 10: eadq2465 (2024); Joge et al., PNAS 122 (23): e2502077122] We also contributed to model isoprene emissions from the Southern Ocean. [Ferracci et al., Nature Comm. 15: 2571 (2024)]
(1) Phytoplankton – bacterial interactions:
-We combined measurements of organosulfur concentrations and cycling rates with sequencing of taxonomic and functional genes, to assess if microbial activity rates can be predicted by the occurrence and expression of the relevant genes. This has been conducted with sample collections from previous expeditions to Antarctic and tropics as well as from the SUMMIT Mediterranean cruise (June 2021). [Masdeu-Navarro et al., Front. Mar. Sci. 9: 944141 (2022); Mangot, Simó et al., in preparation]
-During the SUMMIT-Moorea Expedition, additions of dimethylsulfoniopropionate (DMSP), acrylate, and glucose triggered N2 fixation rates by heterotrophic bacteria, and we are currently investigating how they upregulated the expression of N2 fixation genes. [Cerdán et al., in preparation]
-We conducted in situ chemotaxis assays (ISCA) to investigate if diazotrophs (N2 fixers) are enriched among bacteria attracted by DMSP [Mangot et al., work in progress]. ISCAs also served to demonstrate synergistic attraction of bacteria by DMSP and polysaccharides [Clerc et al., Nature Comm. 14: 8080 (2023)]
-We experimentally showed that marine sponges and their endosymbiotic bacteria consume volatile sulfur and bromine-containing compounds. [Simó et al., in review in Environ. Sci. Technol.]
-We described the distribution of sulfur compounds, alkylamines and other volatiles in Antarctic seawaters and sea ice. [Rocchi et al., Biogeosci. 22: 3429–3448 (2025); Crabeck et al., in review in Elementa]
-We showed how the volatile compound isoprene is consumed in the surface ocean. [Simó et al., Comm. Earth Environ. 3: 20 (2022)]
(2) Phytoplankton – phytoplankton interactions:
-We have identified the membrane transporter for the uptake of the algal osmolyte DMSP by eukaryotic phytoplankton. The candidate protein was suggested by radioisotope and transcriptomic assays, and its function was confirmed by functional complementation of a mutant of the bacterium Escherichia coli with the PaDT gene from a eukaryotic picoalga. Further experiments supported that exogenous DMSP incorporation as an energy-saving strategy. Finally, we showed the global and taxonomic spread of PaDT expression in the surface ocean. [Simó et al., submitted (2025)]
(3) Predator – phytoplankton interactions:
-We conducted chemotaxis experiments to investigate if protist grazing on phytoplankton is modulated by chemical signals, and if this oriented grazing facilitates the recovery of the prey population from physiological stress. Video cell tracking of predator swimming, cell counting of prey, and measurement of prey physiological stress level and recovery enabled to confirm that model herbivore protists are attracted by the algal osmolyte DMSP, this induces preferential grazing on sunlight-stressed algal cells, and subsequently accelerates prey population recovery from stress. [Güell-Bujons et al., ISME J. 18: wrae130 (2024); Güell-Bujons et al., in preparation]
-We investigated how organosulfur compounds are involved in phytoplankton bloom biomass control by viruses. [Vincent et al., Nature Comm. 4: 510 (2023); Vaqué et al., Antarctic Sci. 37: 265-277 (2025)]
(4) Modelling:
-We developed a numerical 1D model of organosulphur cycling across microbial food web interactions. [LeGland et al., Limnol Oceanogr. 69: 140-157 (2023)]
- We developed diagnostic and machine learning models for a revised assessment of the climate effects of global oceanic emissions of volatile sulfur in present and future scenarios [Wohl et al., Sci. Adv. 10: eadq2465 (2024); Joge et al., PNAS 122 (23): e2502077122] We also contributed to model isoprene emissions from the Southern Ocean. [Ferracci et al., Nature Comm. 15: 2571 (2024)]
The SUMMIT project went beyond the state of the art in the knowledge of the involvement of organosulfur compounds in marine microbial interactions, by achieving for the first time:
(i) A link between measured rates of the production and consumption of organosulfur compounds and the expression of the genes encoding for these cycling processes, over diel cycles.
(ii) Discovery the identity of the membrane transporter of the important osmolyte and substrate DMSP in eukaryotic phytoplankton.
(iii) Quantification of how phytoplankton exudates trigger heterotrophic N2 fixation.
(iv) Discovery of the role of chemotactic protistan grazing in keeping phytoplankton prey populations healthier.
(v) Estimation of the global distribution and emission of methanethiol (MeSH) in the surface ocean, and its climate effects.
(vi) Discovery that marine sponges consume volatile sulfur and bromine-containing compounds.
(vii) First quantification of the cycling rates of the volatile compound isoprene in the surface ocean.
(i) A link between measured rates of the production and consumption of organosulfur compounds and the expression of the genes encoding for these cycling processes, over diel cycles.
(ii) Discovery the identity of the membrane transporter of the important osmolyte and substrate DMSP in eukaryotic phytoplankton.
(iii) Quantification of how phytoplankton exudates trigger heterotrophic N2 fixation.
(iv) Discovery of the role of chemotactic protistan grazing in keeping phytoplankton prey populations healthier.
(v) Estimation of the global distribution and emission of methanethiol (MeSH) in the surface ocean, and its climate effects.
(vi) Discovery that marine sponges consume volatile sulfur and bromine-containing compounds.
(vii) First quantification of the cycling rates of the volatile compound isoprene in the surface ocean.