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

ABSTRACT

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 (F_v/F_m) 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 F_v/F_m, 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.

KEYWORDS:

• Phytoplankton
• dissolved organic matter
• dom
• don
• hydrogen peroxide
• diatom
• nitrogen
• cell death

Acknowledgments

This research was supported by the Research Council of the University (RCU) of California State University Bakersfield. The authors acknowledge the laboratory work by Martha Peraza, Jacob Spriester, Alejandro Carlos, and Alex Hernandez. We also thank Isolde Francis, Sigrid Neys, and Matthew Johnson for their helpful revisions of the manuscript.

Author contributions

J.T.F.G. conceived the experiments, J.T.F.G. and J.A.C conducted the experiments and analyzed the results, J.T.F.G. wrote the manuscript. Both authors reviewed the manuscript.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary Material

Supplemental data for this article can be accessed here.

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.