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Chattonella species, C. marina and C. ovata, are harmful raphidophycean flagellates known to have hemolytic effects on many marine organisms and resulting in massive ecological damage worldwide. However, knowledge of the toxigenic mechanism of these ichthyotoxic flagellates is still limited. Light was reported to be responsible for the hemolytic activity (HA) of Chattonella species. Therefore, the response of photoprotective, photosynthetic accessory pigments, the photosystem II (PSII) electron transport chain, as well as HA were investigated in non-axenic C. marina and C. ovata cultures under variable environmental conditions (light, iron and addition of photosynthetic inhibitors). HA and hydrogen peroxide (H2O2) were quantified using erythrocytes and pHPA assay. Results confirmed that% HA of Chattonella was initiated by light, but was not always elicited during cell division. Exponential growth of C. marina and C. ovata under the light over 100 µmol m−2 s−1 or iron-sufficient conditions elicited high hemolytic activity. Inhibitors of PSII reduced the HA of C. marina, but had no effect on C. ovata. The toxicological response indicated that HA in Chattonella was not associated with the photoprotective system, i.e., xanthophyll cycle and regulation of reactive oxygen species, nor the PSII electron transport chain, but most likely occurred during energy transport through the light-harvesting antenna pigments. A positive, highly significant relationship between HA and chlorophyll (chl) biosynthesis pigments, especially chl c2 and chl a, in both species, indicated that hemolytic toxin may be generated during electron/energy transfer through the chl c2 biosynthesis pathway.

The raphidophyte Chattonella spp. and diatom Skeletonema spp. are the dominant harmful algal species of summer blooms in Ariake Sea, Japan. A new bio-optical algorithm based on backscattering features has been developed to differentiate harmful raphidophyte blooms from diatom blooms using MODIS imagery. Bloom waters were first discriminated from other water types based on the distinct spectral shape of the remote sensing reflectance R r s (λ) data derived from MODIS. Specifically, bloom waters were discriminated by the positive value of Spectral Shape, SS (645), which arises from the R r s (λ) shoulder at 645 nm in bloom waters. Next, the higher cellular-specific backscattering coefficient, estimated from MODIS data and quasi-analytical algorithm (QAA) of raphidophyte, Chattonella spp., was utilized to discriminate it from blooms of the diatom, Skeletonema spp. A new index b b p − i n d e x ( 555 ) was calculated based on a semi-analytical bio-optical model to discriminate the two algal groups. This index, combined with a supplemental Red Band Ratio (RBR) index, effectively differentiated the two bloom types. Validation of the method was undertaken using MODIS satellite data coincident with confirmed bloom observations from local field surveys, which showed that the newly developed method, based on backscattering features, could successfully discriminate the raphidophyte Chattonella spp. from the diatom Skeletonema spp. and thus provide reliable information on the spatial distribution of harmful blooms in Ariake Sea.

In coastal areas around the world, red tides cause economic losses to aquaculture industries. Precautions, such as evacuating cages, can mitigate the damage caused by red tides, and the effectiveness of such measures is enhanced by accurate forecasting of the noxious microalgae’s growth dynamics. Here we examined the relationships between cell morphology and growth under different nutrient conditions using Japanese culture strains of a noxious raphidophyte, Chattonella marina complex. When a culture strain of Chattonella was incubated in nitrogen- or phosphorus-depleted conditions, the growth rate correlated positively with cell area, and negatively with cell roundness and dominance of abnormal cells, such as those with a clearly visible nucleus or with a needle-like tail with fewer pigments (tailed cell). Within 1–3 days after nutrient additions, cell size recovered and abnormal cells disappeared. Moreover, we also observed similar changes of cellular morphology under a nitrogen- and phosphorus-depleted condition for the other three strains, including three varieties. These results suggest a possibility that cytomorphological parameters, such as a predominance of abnormal cells, mark the nutrient limitation in Chattonella marina complex.

Quantifying the abundance of Chattonella species is necessary to effectively manage the threats from ichthyotoxic raphidophytes, which can cause large-scale mortality of aquacultured fish in temperate waters. The identification and cell counting of Chattonella species have been conducted primarily on living cells without fixation by light microscopy because routine fixatives do not retain their morphological features. Species belonging to the Chattonella marina complex, including C. marina and C. marina var. ovata, had high genetic similarities and the lack of clear morphological delimitations between the species. To estimate the abundance of C. marina complex in marine plankton samples, we developed a protocol based on the droplet digital polymerase chain reaction (ddPCR) assay, with C. marina complex-specific primers targeting the internal transcribed spacer (ITS) region of the rDNA. Cell abundance of the C. marina complex can be determined using the ITS copy number per cell, ranging from 25 ± 1 for C. marina to 112 ± 7 for C. marina var. ovata. There were no significant differences in ITS copies estimated by the ddPCR assay between environmental DNA samples from various localities spiked with the same number of cells of culture strains. This approach can be employed to improve the monitoring efficiency of various marine protists and to support the implementation of management for harmful algal blooms, which are difficult to analyze using microscopy alone.

Long-term changes of the fish-killing raphidophyte Chattonella spp. ( Chattonella antiqua , Chattonella marina and Chattonella ovata ) were examined in relation to environmental factors at 19 sampling stations in Harima-Nada, eastern Seto Inland Sea, Japan, for 36 years from 1973 to 2008. Long-term trends in the dynamics of Chattonella populations were considered to relate to environmental factors such as nutrient concentrations and water temperature. High nutrient levels during the period from the 1970s to the early 1980s have contributed to the high cell density and large-scale red tides of Chattonella spp. in Harima-Nada. However, nutrient levels exhibited a decreasing trend thereafter, and it is thought that Chattonella spp. cannot form large-scale blooms under the present conditions. After the mid-1990s, the occurrence period of vegetative cells of Chattonella spp. has been several weeks or 1 month earlier than that of the 1970s and early 1980s, and the appearance frequency of Chattonella spp. has increased in the northern coastal area, although the cell density and the spatial scale of the distribution have become lower and smaller than those in the previous decades. It is suggested that the timing of germination of Chattonella cysts has become earlier as a result of the increase in water temperature, and the chances of vegetative growth have also increased, especially at the northern coast where most of large rivers discharge into the Harima-Nada. In addition, the present results revealed that fewer diatoms were also one of the significant factors for the high abundance of Chattonella spp. in Harima-Nada.

Demura M., Noël M.-H., Kasai F., Watanabe M.M. and Kawachi M. 2009. Taxonomic revision of Chattonella antiqua, C. marina and C. ovata (Raphidophyceae) based on their morphological characteristics and genetic diversity. Phycologia 48: 518-535. DOI: 10.2216/08-98.1. Three raphidophyte species, Chattonella antiqua, C. marina and C. ovata, are red tide-forming harmful phytoplankton species, causing mass mortality at fish farms. These species were originally distinguished from each other solely based on their morphological characters. Recent genetic diversity analyses showed that the three species were extremely similar. It was therefore necessary to re-examine these three species to determine if they were independent single species. We compared 104 strains of the three species using morphological characters, nuclear ITS rDNA regions, the chloroplast rbcL gene, the mitochondrion COI gene and selected microsatellite regions. The morphological characters for the three species formed a continuum of variation instead of clearly defined limits. Compared with other selected heterokontophytes, their genetic divergence in the analyzed three regions was found to be at the intraspecies level. Microsatellite markers distinguished each of the 104 strains, but the strains apparently formed a single geographical population. Based on the morphological characters and the phylogenetic analyses, three groups, corresponding to each of the three Chattonella species, were roughly recognized. Nevertheless, this three-group distribution was insufficient to justify their distinction at the species rank. We therefore proposed a taxonomic revision with C. antiqua and C. ovata reduced to varieties of C. marina, this latter having name priority. We proposed a new status: C. marina var. antiqua (Hada) Demura & Kawachi and C. marina var. ovata (Y. Hara & Chihara) Demura & Kawachi.

Ocean acidification and warming, identified as environmental concerns likely to be affected by climate change, arecrucial determinants of algal growth. The ichthyotoxic raphidophytes Chattonella species are responsible for huge economiclosses and environmental impact worldwide. In this study, we investigated the impact of CO2 on the thermalperformance curves (TPCs) of Chattonella marina and Chattonella ovata grown under temperatures ranging from 13 to34°C under ambient pCO2 (350 μatm) and elevated pCO2 (950 μatm). TPCs were comparable between the species or evenbetween pCO2 levels. With the exception of the critical thermal minimum (CTmin) for C. ovata, CTmin for C. marina and thethermal optimum (Topt) and critical thermal maximum (CTmax) for both species did not change with elevation of pCO2levels. While CO2 enrichment increased the maximum photosynthetic rates (Pmax) up to 125% at the Topt of 30°C, specificgrowth rates were not significantly different under elevated pCO2 for the two species. Overall, C. ovata is likely to benefitfrom climate change, potentially widening its range of thermal tolerance limit in highly acidic waters and contributingto prolonged phenology of future phytoplankton assemblages in coastal waters. KCI Citation Count: 0

Diurnal rhythms in physiological functions contribute to homeostasis in many organisms. Although relationships between molecular biology and diurnal rhythms have been well studied in model organisms like higher plants, those in harmful algal bloom species are poorly understood. Here we measured several physiological parameters and the expression patterns of photosynthesis-related and antioxidant-enzyme genes in the Chattonella marina complex to understand the biological meaning of diurnal rhythm. Under a light–dark cycle, Fv/Fm and expression of psbA, psbD, and 2-Cys prx showed significant increases in the light and decreases during the dark. These rhythms remained even under continuous dark conditions. DCMU suppressed the induction of psbA, psbD, and 2-Cys prx expression under both light regimes. Oxidative stress levels and H2O2 scavenging activities were relatively stable, and there was no significant correlation between H2O2 scavenging activities and antioxidant-enzyme gene expression. These results indicate that the Chattonella marina complex has developed mechanisms for efficient photosynthetic energy production in the light. Our results showed that this species has a diurnal rhythm and a biological clock. These phenomena are thought to contribute to the efficiency of physiological activities centered on photosynthesis and cell growth related to the diurnal vertical movement of this species.

Red tides sometimes impact the aquaculture industry worldwide, resulting in mass fish mortalities. It is known empirically that their effects can be mitigated by cessation of feeding. However, specific methods to maximize this technique’s effectiveness and provide physiological support remain limited. In the present study, we investigated the effects of the feeding‐cessation period on a fish’s resistance to a harmful red‐tide microalga, the Chattonella marina complex (“ Chattonella ”), using yellowtail ( Seriola quinqueradiata ) of two ages and body weights: juveniles (74 days after hatching and ~15 g) and young (201 days after hatching and ~860 g). The fish mortality by Chattonella is thought to be associated with gill damage. Thereby, we measured oxygen consumption to consider plankton contact with the gills. Our results showed that feeding cessation for 4 or more days significantly increased survival, regardless of size. Body weight decreased with longer feeding cessation, but survival rates were not affected by body weight. To test red‐tide resistance, juvenile yellowtail were treated by feeding cessation for 1, 2, and 4 days, and young yellowtail for 1, 4, and 8 days. In the juveniles, a longer feeding pause also reduced oxygen consumption. Moreover, histological examination of the juveniles showed that a longer feeding pause reduced damage to the secondary lamellae of the gills. We propose that gill damage was mitigated by reducing the interaction between Chattonella cells and the gill lamellae, likely as a result of decreased oxygen consumption. These results indicate that feeding cessation for a specific period of time physiologically improves red‐tide resistance in yellowtail.

The marine raphidophyte Chattonella marina complex forms red tides, causing heavy mortalities of aquacultured fishes in temperate coastal waters worldwide. The mechanism for Chattonella fish mortality remains unresolved. Although several toxic chemicals have been proposed as responsible for fish mortality, the cause is still unclear. In this study, we performed toxicity bioassays with red sea bream and yellowtail. We also measured biological parameters potentially related to ichthyotoxicity, such as cell size, superoxide (O2•−) production, and compositions of fatty acids and sugars, in up to eight Chattonella strains to investigate possible correlations with toxicity. There were significant differences in moribundity rates of fish and in all biological parameters among strains. One strain displayed no ichthyotoxicity even at high cell densities. Strains were categorized into three groups based on cell length, but this classification did not significantly correlate with ichthyotoxicity. O2•− production differed by a factor of more than 13 between strains at the late exponential growth phase. O2•− production was significantly correlated with ichthyotoxicity. Differences in fatty acid and sugar contents were not related to ichthyotoxicity. Our study supports the hypothesis that superoxide can directly or indirectly play an important role in the Chattonella-related mortality of aquacultured fishes.