The brown alga Saccharina japonica features distinct vanadium-dependent bromoperoxidases and iodoperoxidases

Abstract

Marine algae have an extraordinary ability to absorb halogens which provide algae with an inorganic antioxidant impacting atmospheric chemistry. Although brown algal Laminariales species are the most efficient iodine accumulators among all living systems, and Saccharina japonica is the primary material used for iodine extraction, the functions and regulatory mechanisms of these species have not been fully documented. In this study, a functional genomics analysis of the algal vanadium-dependent haloperoxidase (vHPO) gene family was conducted; there genes can introduce halogen atoms into organic compounds. The comprehensive analyses regarding the bioinformatics and phylogenetics of novel genomic and transcriptomic sequencing data of 21 Rhodophyta and 19 Ochrophyta marine algal species revealed that brown algal vHPOs have two gene types, vanadium-dependent bromoperoxidase (vBPO) and vanadium-dependent iodoperoxidase (vIPO), with secondary endosymbiotic host origin. The enzyme activity of S. japonica vBPO and vIPO were verified for the first time and were quite stable in a wide range of temperature and pH values. However, the specific activity and optimal conditions were considerably different between vBPO and vIPO. The transcript expression analysis in different S. japonica tissues (including rhizoids), generations (sporophytes and gametophytes), sexes (male and female), and stress conditions (hyposaline and hyperthermia) also showed great differences between vBPOs and vIPOs. Most of the vBPOs were constitutively expressed with higher expression dose, which may be responsible for basal halogen metabolism. On the contrary, vIPOs mainly showed specific expression, which may be involved in tissue differentiation, generation differentiation, sex differentiation, and stress regulation. Comprehensive analysis of gene family evolution, enzyme biochemical characteristics, and complex transcriptional mechanisms were conducive to the environmental adaptation and sophisticated system evolution of Laminariales. The successful bromination of small-molecule compound substrate by SjavBPO provided high activity and efficient enzymatic tools for artificial synthesis of halogenated compounds.