Single cell dynamics and nitrogen transformations in the chain forming diatom Chaetoceros affinis

Colony formation in phytoplankton is often considered a disadvantage during nutrient limitation in aquatic systems. Using stable isotopic tracers combined with secondary ion mass spectrometry (SIMS), we unravel cell-specific activities of a chain-forming diatom and interactions with attached bacteria. The uptake of 13C-bicarbonate and15N-nitrate or 15N-ammonium was studied in Chaetoceros affinis during the stationary growth phase. Low cell-to-cell variance of 13C-bicarbonate and 15N-nitrate assimilation within diatom chains prevailed during the early stationary phase. Up to 5% of freshly assimilated 13C and 15N was detected in attached bacteria within 12 h and supported bacterial C- and N-growth rates up to 0.026 h-1. During the mid-stationary phase, diatom chain-length decreased and 13C and 15N-nitrate assimilation was significantly higher in solitary cells as compared to that in chain cells. During the late stationary phase, nitrate assimilation ceased and ammonium assimilation balanced C fixation. At this stage, we observed highly active cells neighboring inactive cells within the same chain. In N-limited regimes, bacterial remineralization of N and the short diffusion distance between neighbors in chains may support surviving cells. This combination of microbial gardening and nutrient transfer within diatom chains represents a strategy which challenges current paradigms of nutrient fluxes in plankton communities.

Automated summary

This study investigates the cell-specific activities of a chain-forming diatom and its interactions with attached bacteria using stable isotopic tracers and secondary ion mass spectrometry (SIMS). The results show that, under nutrient limitation, there is low variance of assimilation within diatom chains, with attached bacteria able to obtain nutrients from the assimilates. However, as the chain length decreases, assimilation in the solitary cells becomes more significant. In the late stationary phase, cells with different activities coexist within the same chain, and bacterial remineralization and nutrient transfer between neighboring cells may play an important role in cell survival under nitrogen-limited conditions.