Nitrogen concentration shapes the size structure and the functional diversity of phytoplankton communities in the southern Indian Ocean

Phytoplankton are fundamental to marine ecosystems, biogeochemical cycling and climate regulation. Their community structure and productivity are shaped by biotic and abiotic factors, notably temperature and macronutrient concentrations. Climate change is altering ocean vertical stratification and nutrient dynamics, with complex and often poorly understood impacts on phytoplankton communities and global primary production. To contribute characterizing these relationships, we analyzed planktonic community composition using 18S rRNA amplicon sequencing and imaging flow cytometry in the southern Indian Ocean across a strong environmental gradient from warm, stratified, N-depleted (but relatively P-repleted) waters in the north to cold, mixed, macronutrient-replete waters in the south. Phytoplankton composition and local diversity correlated primarily with temperature and macronutrient concentrations, but smaller cells (<3 μm) were less affected than larger ones (>3 μm). To disentangle the relative influence of temperature and macronutrients, we applied a model of dissolved macronutrient diffusion, suggesting that nutrient limitation, primarily nitrogen, likely constrains the growth of osmotrophic phytoplankton with cell sizes ranging from 4 to 15 μm in the nutrient-depleted region. We show that smaller cells, with higher surface area-to-volume ratios, are likely to evade this limitation, explaining their lower sensitivity to nitrogen concentrations, both in their taxonomic composition and diversity. Imaging flow cytometry confirmed that larger cells persisting in nitrogen-depleted waters predominantly employ alternative nitrogen acquisition strategies such as diazotrophy or mixotrophy, fostering functional local diversity. Notably, three Prymnesiophyceae taxa exhibited partial limitation by nitrogen diffusion, raising questions about their potential for mixotrophy or diazotrophy, akin to Braarudosphaera bigelowii. Other environmental factors, such as trace metal concentrations, showed weaker correlations with community structure metrics. Overall, our results are consistent with N concentration gradients and N:P imbalances driving a great share of planktonic diversity by constraining large-cell nutrient acquisition strategies and fostering functional diversification in oligotrophic regions of the Ocean.