Summary
Diatoms, dinoflagellates, and coccolithophorids are the dominant groups of marine eukaryotic phytoplankton collectively responsible for the majority of primary production in the ocean1. These phytoplankton contain additional intracellular membranes around their chloroplasts derived from ancestral engulfment of red microalgae by unicellular heterotrophic eukaryotes that led to secondary endosymbiosis2. This symbiogenesis hypothesis for the origin of modern secondary endosymbiotic phytoplankton is supported by a wealth of palaeontologic, morphologic, and genomic evidence3–6. However, the selectable evolutionary advantage of these membranes and the physiological significance for extant phytoplankton are unknown. We report that the proton-pumping enzyme V-type H+-ATPase (VHA), ubiquitously used in eukaryotic intercellular digestion, is localized around the chloroplasts of centric diatoms and that VHA-activity significantly enhances photosynthesis over a wide range of oceanic irradiances. Similar results in pennate diatoms, dinoflagellates, and coccolithophorids, but not green or red microalgae, imply a mechanism resulting from the co-option of phagocytic VHA activity into a carbon concentrating mechanism that is common to secondary endosymbiotic phytoplankton. Furthermore, analogous VHA-dependent mechanisms in extant photosymbiotic marine invertebrates7–9 provide functional evidence for an adaptive advantage throughout the transition from endosymbiosis to symbiogenesis. Our results suggest that VHA-dependent enhancement of photosynthesis contributes at least 7% of primary production in the ocean, providing an example of a symbiosis-derived evolutionary innovation with global environmental implications.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
The manuscript format (i.e. figures, supplemental materials, and associated text) were modified to adjust to the style of a different journal. The results and conclusions have remained unchanged.
