Production of extracellular reactive oxygen species by phytoplankton: past and future directions

Abstract

In aquatic environments, phytoplankton represent a major source of reactive oxygen species (ROS) such as superoxide and hydrogen peroxide. Many phytoplankton taxa also produce extracellular ROS under optimal growth conditions in culture. However, the physiological purpose of extracellular ROS production by phytoplankton and its wider significance to ecosystem-scale trophic interactions and biogeochemistry remain unclear. Here, we review the rates, taxonomic diversity, subcellular mechanisms and functions of extracellular superoxide and hydrogen peroxide production by phytoplankton with a view towards future research directions. Model eukaryotic phytoplankton and cyanobacteria produce extracellular superoxide and hydrogen peroxide at cell-normalized rates that span several orders of magnitude, both within and between taxa. The potential ecophysiological roles of extracellular ROS production are versatile and appear to be shared among diverse phytoplankton species, including ichthyotoxicity, allelopathy, growth promotion, and iron acquisition. Whereas extracellular hydrogen peroxide likely arises from a combination of intracellular and cell surface production mechanisms, extracellular superoxide is predominantly generated by specialized systems for transplasma membrane electron transport. Future insights into the molecular-level basis of extracellular ROS production, combined with existing high-sensitivity geochemical techniques for the direct quantification of ROS dynamics, will help unveil the ecophysiological and biogeochemical significance of phytoplankton-derived ROS in natural aquatic systems.

Keywords: biological interactions; cryptic biogeochemistry; harmful algae; monitoring; oxidative stress; phytoplankton bloom; redox homeostasis.

Fig. 1.

Survey of extracellular superoxide (O₂−) and hydrogen peroxide (H₂O₂) production rates by phytoplankton. Species known to form HABs are indicated in bold. Data and original references are provided in Supplementary Table S1.

Fig. 2.

Mechanisms of superoxide (O₂−) and hydrogen peroxide (H₂O₂) production in phytoplankton. Chloroplast: PSI—photosystem I, PSII—photosystem II, SF—stromal factor, OEC—oxygen-evolving complex, cytb₅₅₉—cytochrome b559; Mitochondria: CI—complex I, CIII—complex III, DH—NAD(P)H dehydrogenase; Peroxisomes: GO—glycolate oxidase, XO—xanthine oxidase, MDAR—monodehydroascorbate reductase, cytb—cytochrome b, PMP29—peroxisome membrane polypeptide 29; Cell surface and cell-free environment: OR—oxidoreductase. Intracellular hydrogen peroxide can diffuse within and outside of cells (white arrows), but intracellular superoxide is unlikely to escape the cell.