Molybdate:sulfate ratio affects redox metabolism and viability of the dinoflagellate Lingulodinium polyedrum

Abstract

Molybdenum is a transition metal used primarily (90% or more) as an additive to steel and corrosion-resistant alloys in metallurgical industries and its release into the environment is a growing problem. As a catalytic center of some redox enzymes, molybdenum is an essential element for inorganic nitrogen assimilation/fixation, phytohormone synthesis, and free radical metabolism in photosynthesizing species. In oceanic and estuarine waters, microalgae absorb molybdenum as the water-soluble molybdate anion (MoO42−), although MoO42− uptake is thought to compete with uptake of the much more abundant sulfate anion (SO42−, approximately 25mM in seawater). Thus, those aspects of microalgal biology impacted by molybdenum would be better explained by considering both MoO42− and SO42− concentrations in the aquatic milieu. This work examines toxicological, physiological and redox imbalances in the dinoflagellate Lingulodinium polyedrum that have been induced by changes in the molybdate:sulfate ratios. We prepared cultures of Lingulodinium polyedrum grown in artificial seawater containing eight different MoO42− concentrations (from 0 to 200μM) and three different SO42− concentrations (3.5mM, 9.6mM and 25mM). We measured sulfur content in cells, the activities of the three major antioxidant enzymes (superoxide dismutase, catalase, and ascorbate peroxidase), indexes of oxidative modifications in proteins (carbonyl content) and lipids (thiobarbituric acid-reactive substances, TBARS), the activities of the molybdenum-dependent enzymes xanthine oxidase and nitrate reductase, expression of key protein components of dinoflagellate photosynthesis (peridinin–chlorophyll a protein and ribulose-1,5-biphosphate carboxylase/oxidase) and growth curves. We find evidence for Mo toxicity at relatively high [MoO42−]:[SO42−] ratios. We also find evidence for extensive redox adaptations at Mo levels well below lethal levels.