Abstract
Planktonic algae <5 μm in size are major fixers of inorganic carbon in the ocean1. They dominate phytoplankton biomass in post-bloom, stratified oceanic temperate waters2. Traditionally, large and small algae are viewed as having a critical growth dependence on inorganic nutrients, which the latter can better acquire at lower ambient concentrations owing to their higher surface area to volume ratios3,4. Nonetheless, recent phosphate tracer experiments in the oligotrophic ocean5 have suggested that small algae obtain inorganic phosphate indirectly, possibly through feeding on bacterioplankton. There have been numerous microscopy-based studies of algae feeding mixotrophically6,7 in the laboratory8,9,10 and field11,12,13,14, as well as mathematical modelling of the ecological importance of mixotrophy15. However, because of methodological limitations16 there has not been a direct comparison of obligate heterotrophic and mixotrophic bacterivory. Here we present direct evidence that small algae carry out 40–95% of the bacterivory in the euphotic layer of the temperate North Atlantic Ocean in summer. A similar range of 37–70% was determined in the surface waters of the tropical North-East Atlantic Ocean, suggesting the global significance of mixotrophy. This finding reveals that even the smallest algae have less dependence on dissolved inorganic nutrients than previously thought, obtaining a quarter of their biomass from bacterivory. This has important implications for how we perceive nutrient acquisition and limitation of carbon-fixing protists as well as control of bacterioplankton in the ocean.
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Acknowledgements
We gratefully acknowledge the captain, officers and crew aboard the RRS Discovery for their help during the cruises, M. Moore for sharing chlorophyll concentration measurements, P. Hill for helping with setting up experiments on the second cruise, and P. Warwick for his help with radiotracer measurements ashore. We thank M. Sleigh, A. Martin and R. Leakey for their critical comments on the earlier drafts of the paper. We thank H. Ducklow for constructive criticism of the earlier version of this paper. This study was supported by the UK Natural Environment Research Council (NERC) through the Oceans 2025 core programmes of the National Oceanography Centre, Southampton and Plymouth Marine Laboratory. The second cruise was supported by the NERC thematic programme Surface Ocean Low Atmosphere Study (SOLAS).
Author Contributions The experimental approach was designed by M.Z., who carried out the tracer work. Flow cytometric analyses were done by G.T. and M.Z., respectively, on the first and second cruise.
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Zubkov, M., Tarran, G. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455, 224–226 (2008). https://doi.org/10.1038/nature07236
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DOI: https://doi.org/10.1038/nature07236
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