A Diatom Gene Regulating Nitric-Oxide Signaling and Susceptibility to Diatom-Derived Aldehydes

Abstract

Diatoms are unicellular phytoplankton accounting for ∼40% of global marine primary productivity, yet the molecular mechanisms underlying their ecological success are largely unexplored. We use a functional-genomics approach in the marine diatom Phaeodactylum tricornutum to characterize a novel protein belonging to the widely conserved YqeH subfamily of GTP-binding proteins thought to play a role in ribosome biogenesis, sporulation, and nitric oxide (NO) generation. Transgenic diatoms overexpressing this gene, designated PtNOA, displayed higher NO production, reduced growth, impaired photosynthetic efficiency, and a reduced ability to adhere to surfaces. A fused YFP-PtNOA protein was plastid localized, distinguishing it from a mitochondria-localized plant ortholog. PtNOA was upregulated in response to the diatom-derived unsaturated aldehyde 2E,4E/Z-decadienal (DD), a molecule previously shown to regulate intercellular signaling, stress surveillance, and defense against grazers. Overexpressing cell lines were hypersensitive to sublethal levels of this aldehyde, manifested by altered expression of superoxide dismutase and metacaspases, key components of stress and death pathways. NOA-like sequences were found in diverse oceanic regions, suggesting that a novel NO-based system operates in diatoms and may be widespread in phytoplankton, providing a biological context for NO in the upper ocean.