RNA-Seq Analysis Reveals Genes Related to Photoreception, Nutrient Uptake, and Toxicity in a Noxious Red-Tide Raphidophyte Chattonella antiqua

Abstract

Aquaculture industries are under threat from noxious red tides, but harm can be mitigated by precautions such as early harvesting and restricting fish feeding to just before the outbreak of a red tide. Therefore, accurate techniques for forecasting red-tide outbreaks are strongly needed. Omics analyses have the potential to expand our understanding of the eco-physiology of these organisms at the molecular level, and to facilitate identification of molecular markers for forecasting their population dynamics and occurrence of damages to fisheries. Red tides of marine raphidophytes, especially Chattonella species, often extensively harm aquaculture industries in regions with a temperate climate around the world. A red tide of Chattonella tends to develop just after an input of nutrients along the coast. Chattonella displays diurnal vertical migration regulated by a weak blue light, so it photosynthesizes in the surface layer during the daytime and takes up nutrients in the bottom layer during the nighttime. Superoxide produced by Chattonella cells is a strong candidate for the cause of its toxicity to bacteria and fishes. Here we conducted mRNA-seq of Chattonella antiqua to identify genes with functions closely related to the dynamics of the noxious red tide, such as photosynthesis, photoreception, nutrient uptake, and superoxide production. The genes related to photosynthetic pigment biosynthesis and nutrient uptake had high similarity with those of model organisms of plants and algae and other red-tide microalgae. We identified orthologous genes of photoreceptors such as aureochrome (newly five genes), the cryptochrome/photolyase (CRY/PHR) family (6-4PHR, plant CRY or cyclobutane pyrimidine dimer [CPD] Class III, CPD Class II, and CRY-DASH), and phytochrome (four genes), which regulate various physiological processes such as flagellar motion and cell cycle in model organisms. Six orthologous genes of NADPH oxidase, which produces superoxide on the cell membrane, were found and divided into two types: one with 5–6 transmembrane domains and another with 11 transmembrane domains. The present study should open the way for analyzing the eco-physiological features of marine raphidophytes at the molecular level.

Molecular phylogeny of fucoxanthin-chlorophyll a/c proteins from Chaetoceros gracilis and Lhcq/Lhcf diversity

“…Sets of translated sequences of other red-lineage microalgae were obtained from the following genome assemblies: Phaeophyceae, Ectocarpus siliculosus (Cock et al, 2010); three Haptophyta; Emiliania huxleyi (Read et al, 2013), Phaeocystis antarctica CCMP1374, and Chrysochromulina tobinii (Hovde et al, 2015); Cryptophyceae, Guillardia theta CCMP2712 (Curtis et al, 2012); and two Rhodophyta, red alga Porphyridium purpureum (Bhattacharya et al, 2013) and Cyanidioschyzon merolae (Tanaka et al ., 2004). Sets of translated sequences derived from the RNA-seq data of Raphidophyceae Chattonella antiqua and Dinophyceae Peridiniales Heterocapsa circularisquama were obtained from the database for research in harmful algal blooms (Shikata et al ., 2019). Genome assemblies of green-lineage organisms have also been used, including Chlamydomonas reinhardtii (Merchant et al, 2007) and Physcomitrella patens (Rensing et al, 2008).…”

Recent Progress in the Study of Peroxiredoxin in the Harmful Algal Bloom Species Chattonella marina

“…Comprehensive analysis of growth-phase-dependent gene expression will provide useful information about the molecular mechanisms that maintain growth potential and the molecular indicators that are candidates for monitoring growth potential in C. marina . Recently, RNA-seq analysis has been performed on harmful algae [ 34 , 35 , 36 , 38 ]. In our current study, RNA-seq analysis is being performed using C. marina cells in the exponential phase as well as the early-, mid-, and late-stationary phases of growth (manuscript in preparation).…”

“…Understanding the physiological mechanisms that allow algae to tolerate these environmental conditions is important to biological and fisheries science. Recently, omics analysis has begun to be used to investigate the comprehensive molecular mechanisms that account for HAB phenomena [ 21 , 33 , 34 , 35 , 36 , 37 , 38 ]. Our studies have focused on the molecular mechanisms that control the growth of HAB species.…”

Effect of elevated pCO2 on thermal performance of Chattonella marina and Chattonella ovata (Raphidophyceae)

“…In general, global warming benefits algal growth if the increased temperature is below the optimal al. 1991, Tilney et al 2015, Shikata et al 2019, Qiu et al 2020. Given the potential role of resting cysts in bloom initiation of Chattonella species, the abundance of vegetative cells in the water column is not always relied on that of viable cysts in the sediments (Onitsuka et al 2020).…”

“…In temperate and subtropical-tropical regions of the world, the fish-killing (ichthyotoxic) raphidophytes Chattonella species have frequently caused serious damage to fisheries and mariculture industries in Korea (Kim et al 2007), Japan (Imai andYamaguchi 2012, Yamaguchi et al 2018), China (Wang et al 2006(Wang et al , 2017, North America (Lewitus et al 2008, García-Mendoza et al 2018, and Europe (Stacca et al 2016, Satta et al 2017, Zingone et al 2020. The production of superoxide is associated with the growth of Chattonella, which is a strong candidate for the cause of its toxicity in fishes (Shikata et al 2019). They inhabit the warm (~30°C) tropical waters around the equator (e.g., Chattonella subsalsa), extending to the colder (~5°C) waters of the Dutch Wadden Sea (e.g., Chattonella marina and Chattonella antiqua) (Vrieling et al 1995).…”