Publication
A proton pump enhancing photosynthesis links phagocytosis to marine algae symbiogenesis
Publisher:
Cold Spring Harbor Laboratory
Date:
28-05-2022
DOI:
10.1101/2022.05.26.493626
Abstract: Diatoms, dinoflagellates, and coccolithophorids are the dominant groups of marine eukaryotic phytoplankton collectively responsible for the majority of primary production in the ocean 1 . These phytoplankton contain additional intracellular membranes around their chloroplasts derived from ancestral engulfment of red microalgae by unicellular heterotrophic eukaryotes that led to secondary endosymbiosis 2 . This symbiogenesis hypothesis for the origin of modern secondary endosymbiotic phytoplankton is supported by a wealth of palaeontologic, morphologic, and genomic evidence 3–6 . 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 invertebrates 7–9 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 ex le of a symbiosis-derived evolutionary innovation with global environmental implications.