Reactive oxygen species production and scavenging; genomic patterns across marine phytoplankton

Abstract

Marine phytoplankton produce and scavenge Reactive Oxygen Species (ROS), to maintain intracellular ROS homeostasis to support cellular processes, but limit damaging reactions. Some prokaryotic picophytoplankton have lost genes encoding the capacity to scavenge Hydrogen Peroxide (HO2). The “Black Queen Hypothesis” postulates that prokaryotic picophytoplankton might thereby lower costs through H2O2 diffusing across the membrane of the small source cells. We investigated genomes and transcriptomes from diverse taxonomic lineages of eukaryotic phytoplankton, ranging from 0.4 to 44 µm cell radius, to analyze the fraction of total genes dedicated to producing enzymes metabolizing three distinct ROS. H2O2 has low reactivity, long intracellular and extracellular lifetimes, and readily crosses cell membranes, and can therefore potentially leave a cell before provoking damaging intracellular reactions. Across eukaryotic phytoplankton, the fraction of total genes dedicated to H2O2 production indeed decreases with increasing cell radius, consistent with the maintenance of ROS homeostasis in the face of slower diffusional losses of H2O2. The fraction of total genes dedicated to H2O2 scavenging does not change with increasing cell radius, although taxonomic lineage influences the fraction of total genes dedicated to H2O2 metabolism. Superoxide (O2•−) has high reactivity, short intracellular and extracellular lifetimes and limited membrane permeability. As expected, genes encoding O2•− scavenging were ubiquitous, and did not change with radius, consistent with separate intracellular and extracellular O2•− pools separated by the cell membrane. Nitric Oxide (•NO) has low reactivity, long intracellular and extracellular lifetimes, and readily crosses cell membranes. Neither •NO production nor scavenging genomic capacities changed with increasing cell radius, but were influenced by taxonomic lineage, consistent with the low cytotoxicity and diverse regulatory roles of •NO.