Asparagine-based production of hydrogen peroxide triggers cell death in the diatom Phaeodactylum tricornutum

As a major component of coastal phytoplankton blooms, diatoms are an important source of dissolved organic matter (DOM) in the ocean. While this DOM pool fuels the growth of diverse bacterial populations, diatom population dynamics itself is considered unaffected by it. Here, we identified strong negative effects of the amino acid asparagine on the growth of the marine model diatom Phaeodactylum tricornutum. Using microscopic analyses and physiological assays, we showed that while asparagine fuelled photosynthetic growth, its supplementation to NO3− medium significantly decreased the culture’s cell density and photosynthetic capacity (Fv/Fm) during the stationary phase of the growth cycle. We further showed that these effects resulted from asparagine-based production of hydrogen peroxide (H2O2) that triggered a massive cell death event. Effective lethal asparagine concentrations were as low as 12.5 µM, while 1 μM affected Fv/Fm, but did not trigger culture collapse. Based on sequence similarity with the characterized H2O2-producing L-amino acid oxidase (LAAO) of Chlamydomonas reinhardtii, LAO1, we identified putative LAO1 orthologs in the genomes of P. tricornutum and the toxigenic pennate species Pseudo-nitzschia multiseries. The molecular phylogeny of this gene indicates a shared ancestry with other algal LAAOs and suggests a conserved oxidative deaminase function that could mediate DOM release from diatom populations through the triggering of autocatalytic cell death events.