Bacterial capture and lysis on diatom spines reveal a suspension-feeding strategy
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Phytoplankton contribute nearly half of global primary production and play a central role in ocean biogeochemistry. Although traditionally viewed as phototrophs, a growing body of evidence indicates that many phytoplankton are mixotrophic, supplementing photosynthesis with heterotrophic acquisition of nutrients and organic matter. Yet, the mechanisms enabling heterotrophic feeding in diatoms remain poorly understood. Here, we show that the chitinous spines of the diatom Conticribra weissflogii can serve as attachment sites for the bacterium Marinobacter adhaerens . Cryo-electron tomography and viability staining revealed that a substantial fraction of spine-associated M. adhaerens undergoes lysis. Consistent with bacterial lysis on the spines, Raman spectroscopy showed that diatom cells bearing spine-associated bacteria acquired more bacteria-derived nitrogen than uncolonized cells. Although microfluidic assays revealed a low bacterial affinity for the spines, our results suggest that attachment can be promoted by fucoidan deposits identified on the spines — a compound for which bacteria showed significantly higher binding affinity than chitin — as well as by their geometry, which encounter rate calculations show to be particularly efficient at intercepting bacteria. Together, these findings reveal a previously undescribed form of suspension-feeding in phytoplankton, reminiscent of the role of zooplankton pseudopods in prey capture. Diatom spines intercept bacteria from the surrounding water, retain them near the cell surface, and facilitate subsequent nutrient acquisition, probably through bacterial lysis. Our results expand the functional repertoire of diatom spines beyond defense and buoyancy, identifying spine-mediated bacterial capture as a previously overlooked pathway contributing to phytoplankton mixotrophy.
Significance statement
Diatoms produce long chitinous spines whose functions have been linked to buoyancy control and defense against grazers. Here, we reveal a previously unrecognized function of these appendages: the spines of the diatom Conticribra weissflogii serve as attachment sites for the bacterium Marinobacter adhaerens , a substantial fraction of which undergoes lysis on the spine surface. Using 15 N isotopic labelling and Raman spectroscopy, we demonstrate that diatoms harboring spine-associated bacteria acquire significantly more bacterial-derived nitrogen than uncolonized cells, consistent with spine-mediated bacterial capture contributing to diatom nutrient acquisition. We further show that C. weissflogii spines are coated with fucoidan, which likely promotes bacterial attachment. This suspension-feeding strategy — in which spines coated with fucoidan, intercept bacteria from the surrounding water, analogous to the slime-coated pseudopods of radiolarians and foraminiferans — has never previously been documented in phytoplankton. Our findings expand the known functional repertoire of diatom spines and identify a previously overlooked pathway of mixotrophic nutrient acquisition in phytoplankton with potentially broad implications for marine nutrient cycling.
