Pronounced uptake and metabolism of organic substrates by diatoms revealed by pulse-labeling metabolomics

Abstract

Diatoms contribute as a dominant group of microalgae to approximately 20% of the global carbon fixation. In the plankton, these photosynthetic algae are exposed to a plethora of metabolites, especially when competing algae are lysed. It is well established that diatoms can take up specific metabolites, such as vitamins, amino acids as nitrogen source, or dimethylsulfoniopropoionate to compensate for changes in water salinity. It is, however, unclear to which extent diatoms take up other organic resources and if these are incorporated into the cells metabolism. Here, we ask about the general scope of uptake of metabolites from competitors. Using labeled metabolites released during lysis of algae grown under a 13CO2 atmosphere, we show that the cosmopolitan diatom Chaetoceros didymus takes up organic substrates with little bias and remarkable efficiency. The newly developed pulse label/ mass spectrometry metabolomics approach reveals that polarity and molecular weight has no detectable influence on uptake efficiency. We also reveal that the taken-up pool of metabolites is partly maintained unaltered within the cells but is also subject to catabolic and anabolic transformation. One of the most dominant phytoplankton groups is thus substantially competing with other heterotrophs for organic material, suggesting that the observed absorbotrophy may substantially impact organic material fluxes in the oceans. Our findings call for the refinement of our understanding of competition in the plankton. SignificanceThis study demonstrates a remarkably universal uptake of organic substrates by diatoms. The extent to which one of the most dominant phytoplankton groups is competing for organic material in the plankton is documented by novel pulse labeling metabolomics studies. Our results show that uptake of organic material by the photosynthetic microalgae occurs with remarkably little bias. Taken-up metabolites are further transformed by the diatoms or directly incorporated into the algal metabolome. Our study calls for a re-consideration of organic material fluxes in the oceans. Also, our understanding of competition in the plankton will have to be refined. The broader implications for the cycling of resources in plankton communities are discussed within this work.