Diversity and genetics of Australasian dinoflagellates, including Gambierdiscus spp. the causative agent of Ciguatera Fish Poisoning

Abstract

Marine microbial protists from benthic habitats include species of the genera Gambierdiscus, which can produce polyketide toxins with ecosystem-wide impacts and impacts on human health. Knowledge of the presence, diversity, effects and distribution of benthic dinoflagellates and their toxins is vital both for basic ecological research and for managing potential impacts on human health. However, at present such information is limited. This study designed novel pyrosequencing-based tools that utilised 18S rRNA and mitochondrial cytochrome b barcoding marker genes. Using these tools, the largest set of dinoflagellate cytochrome b gene sequences to date was developed, and dinoflagellate species richness within marine benthic samples from five tropical marine benthic sites were determined. These tools were applied to samples from a temperate marine benthic site from southern NSW and the species Gambierdiscus carpenteri was found to be highly abundant throughout the region. This was unexpected, given that it is primarily considered a tropical species. The significance of finding this species is discussed in the context of long term monitoring data and its potential for toxin production. Species of Gambierdiscus produce two major toxin groups, ciguatoxins (CTXs) and maitotoxins (MTXs), that can accumulate via marine food chains in seafood and ultimately cause ciguatera fish poisoning (CFP) in humans. While the role of CTXs is well established in CFP, little is known about the role of MTXs. This work showed experimentally that MTXs can accumulate in liver and muscle tissues of carnivorous fish (Pagrus auratus). The levels of MTX detected in fish tissues showed for the first time that MTX may accumulate in fish at levels harmful for human consumption. In order to investigate the genetic basis of toxin biosynthesis in species of Gambierdiscus, two comprehensive transcriptomic libraries for the species Gambierdiscus australes and Gambierdiscus belizeanus, which produce MTXs were sequenced and assembled. Data analysis discovered three hundred and seven genes that formed eight clades within a phylogeny of dinoflagellate polyketide synthesis genes, and may be involved in MTX biosynthesis. This is the first step towards identifying prospective genes that may be involved in MTX biosynthesis, and provides a basis for the future development of molecular tools to assess the risk of CFP.