North American <i>Dinophysis</i>, late‐comers to the harmful algae world

Species of Dinophysis produce diarrhetic toxins and pectenotoxins and frequently cause harvesting bans in intensive shellfish cultivation sites in Western Europe, Chile, Perú, and Japan (Reguera et al., 2014). These dinoflagellates have attracted attention during the last 30 years due to their socio-economic impacts and the long trail of difficulties faced before identification of their nutritional sources and establishment of laboratory cultures (Park et al., 2006; Reguera et al., 2012). For decades, it was a common belief that Dinophysis posed no threat to public health or shellfish exploitation in the USA (Horner et al., 1997; Wolny et al., 2020). The first official report of a diarrhetic shellfish poisoning (DSP) event in 2008 was triggered by serendipitous detection of a bloom of Dinophysis ovum in Texas Bay (Gulf of Mexico) where an in situ imaging flowcytobot had been deployed for early warning of Karenia brevis (Campbell et al., 2010). Unsafe levels of okadaic acid (OA) led to the first harvesting bans on Galveston Bay oysters (Deeds et al., 2010). On the Northwest (Pacific) coast, three persons were intoxicated by the end of July 2011 after consuming mussels from Sequim Bay State Park (recreational picking), and this event prompted the first DSP closures in the Olympic Peninsula and Strait of Juan de Fuca (Trainer et al., 2013). Eighty nautical miles further north, more than 60 people became sick after eating mussels in restaurants on Salt Spring Island, Canada, that had been collected the same last week of July (Taylor et al., 2013). Guided by the magnitude of the (luckily non-fatal) human bioassays, we suggest that the Sequim Bay State Park event was probably at the southern limit of a mesoscale event of the same Dinophysis populations contaminating shellfish in the whole Salish Sea area. In the Northeast USA, the mild toxicity of the first Dinophysis acuminata strain established in culture (Hackett et al., 2009) and field observations questioning the toxic nature of Canadian D. norvegica (Lawrence et al., 2000) both contributed to the perception of Dinophysis blooms as irrelevant events. In 2015, a dense and persistent population of D. acuminata led to the first DSP-related harvesting bans in coastal embayments of the southern Gulf of Maine (ICES, 2016). Dinophysis are patchily distributed low biomass harmful algal blooms (HABs) that are, most of the year, below detection levels. It is possible that no Dinophysis-related issues occurred in the USA before the Texas event in 2008. But caution is necessary since systematic monitoring of DSP in most United States waters is lacking, and toxin analyses are prompted in most places only when high numbers of Dinophysis are observed. The sequence of “exceptional” DSP events may be anomalous. Since there are no long-term records, these isolated events are simply oddities and cannot be linked to environmental change (GlobalHAB, 2021). About 12 species of Dinophysis have been established in culture and shown to produce lipophilic toxins, (Nagai et al., 2020). But their physiological and behavioral traits, and their strain-specific toxin composition and impacts, are extremely variable. A synoptic view of the current distribution of Dinophysis species and reported DSP events (Figure 1) confirms that occurrence of toxic outbreaks is determined by the composition (profile and content) of local strains and the shellfish species affected (Blanco, 2018). Mussels are heavy filter-feeders and toxin accumulators, which explains why in North America, as previously observed elsewhere, human illnesses were first detected in consumers of mussels (US West coast) and very rarely reported after oyster consumption (Texas Gulf region). Much effort was invested in recent years to isolate, culture, and characterize 20 strains corresponding to the five most common species of Dinophysis in the United States. Extreme intraspecific differences were found between D. acuminata strains from the Northwest coast, with a profile dominated by DTX1 (the same toxic potential as OA), and the same species from the Northeast coast, with an overwhelming dominance of pectenotoxins, which are not harmful via oral intake. Ayache et al. (2023) showed that: i) USA Pacific D. acuminata and Gulf of Mexico D. ovum strains have toxin contents comparable to those from southwest European regions subject to permanent risk of DSP outbreaks, and ii) the intensity of outbreaks is not necessarily related to cell density, and site specific strategies are required for trigger levels and monitoring. Pectenotoxins, regulated in Europe until 2021 (European Commission, 2021), were never regulated in the United States, a fact that adds to the large difference in historic DSP reporting between Europe and North America (Anderson et al., 2021; Bresnan et al. 2021). Similar differences in toxicity are observed between D. acuminata strains from the northern and southernmost regions in Chile (Díaz et al., 2022). Dinophysis cells and related toxins in shellfish were possibly masked in the northeast United States as well as in southern Chile by far more dangerous paralytic shellfish poisoning (PSP) outbreaks that are subject to rigorous monitoring and associated with lengthy quarantines. An interesting new finding in Ayache's review concerns the new DTX1 derivative dihydroxi-DTX1, first detected with enzymatic assays in infested mussels and further identified with chemical analyses in cultured strains of Dinophysis norvegica from the Northwest coast (Deeds et al., 2020). This toxin is not identified with current standard liquid-chromatography mass-spectrometry (LC–MS) procedures, which raises questions such as: (i) How many times have shellfish infested with this toxin been unreported? (ii) Were earlier cases of DSP toxicity in mussels from Nova Scotia, Canada, attributed to epiphytic Prorocentrum lima, caused by D. norvegica? This issue points to the constraints of targeted analytical methods when emerging toxins occur in areas where lipophilic toxins are relatively unexplored. Priority should be given to estimation of the toxic potential of this new toxin so that it is regulated on a sound scientific basis. Dinophysis species are obligate mixotrophs that require ciliate prey (e.g., Mesodinium species), light, and nutrients for sustained growth (Hansen et al., 2013; Kim, Kim, et al., 2012). A three-species food chain—D. acuminata fed the ciliate M. rubrum, the latter fed cryptophytes—was established in laboratory cultures (Park et al., 2006) and later used with other toxic Dinophysis species (Nagai et al., 2020). After years of controversy about the nature of Dinophysis plastids, evidence of the gathering, morphological transformation, and complete replacement of kleptoplastids was obtained (Kim, Nam, et al., 2012). This last finding and their paucity of plastid-related genes (Wisecaver & Hackett, 2010), led Mitra et al. (2016) to classify Dinophysis as a “plastidic specialist Non-Constitutive Mixotroph (psNCM)” (p. 110). Multiple new questions have arisen that need to be addressed with next-generation tools, in particular concerning intraspecific differences in toxin production and Dinophysis prey specificity, including potential alternative prey other than Mesodinium. These two issues are dealt with and all available results related to Dinophysis and their toxins in the United States are reviewed in: “A survey of Dinophysis spp. and their potential to cause diarrhetic shellfish poisoning in coastal waters of the United States” (Ayache et al., 2023). We only begin to understand a mixotrophic species if we know its nutritional sources and are able to establish it in culture. Is Mesodinium rubrum, the only possible prey for Dinophysis? Most plastid sequences obtained from single-cell isolates from field populations of Dinophysis matched those from cryptophytes of the genera Teleaulax/Plagioselmis/Geminigera (TPG clade; Herfort et al., 2017, Kim, Kim, et al., 2012, Nishitani et al., 2010, Rial et al., 2015, Stern et al., 2014). This pointed to Mesodinium species, known to harbor red plastids from the TPG clade, as vectors of Dinophysis kleptoplastids. Rial et al. (2015) found a coincidence of plastidic sequences in local Dinophysis species in the Galician Rias with those from M. rubrum and M. major and a single base-pair difference between T. amphioxeia and P. prolonga, later recognized by Altenburger et al. (2020) as the diploid and haploid phases, respectively, of the same species. In cultures of M. rubrum, growth rate and yield varied with different prey, and optimal results were obtained only if strains of ciliate and its cryptophyte prey had been isolated from the same location (Hernández-Urcera et al., 2018). At the same time, Dinophysis growth is not the same within different strains/species of Mesodinium. Thus, M. major, more abundant than M. rubrum in samples from Argentina and Chile (Johnson et al., 2017) and recently established in culture, grows better with T. amphioxeia and seems to be the optimal prey for D. acuta (Drumm et al., 2021). Furthermore, predominance of identical cryptophyte plastid sequences belonging to Rhodomonas/Rhinomonas/Storeatula (clade V) were found in several species of Dinophysis, in ciliates of the genus Strombidium, and in co-occurring heliozoans in oceanic waters off Los Lagos, Chile (Díaz et al., 2020). These observations support the possibility of prey other than Mesodinium in Southern Chile (Figure 2). Difficulties in establishing Dinophysis cultures have also been faced by American experts, who observed differences in Dinophysis growth and toxin production in response to the physiological status (size, photosynthesis rate, etc.) of the same prey species (Mesodinium rubrum) (Fiorendino et al., 2020). American isolates of Mesodinium and Teleaulax are not available yet, and their best results have been obtained using Japanese strains of M. rubrum and T. amphioxea. Micrographs of cultured specimens of the five species of Dinophysis (Figure 2 in Ayane et al., 2023) reflect the differing responses of each one to a common prey, not necessarily equivalent to their natural resources. The abundant dark material accumulated in the lower half of Lugol's stained specimens from cultures has been interpreted as an overproduction of starch, stored as reserve material, in prey-starved cells of obligate mixotrophs (Kim, Nam et al., 2012). The most stressed-looking specimens, judged by the large cell proportion occupied by dark intracellular cytoplasmic material are the more recently isolated strains of D. norvegica (figure 1 l-o in Ayane et al., this volume). Coincidentally, these correspond to the cultures with the lowest growth rates. Future work of plastidic sequences from North American Dinophysis, Mesodinium, and cryptophytes belonging to the Teleaulax-Geminigera clade will help to unveil the optimal prey for each Dinophysis strain and will guide the exploration of new trophic relations. In the meantime, increased monitoring of Dinophysis, including collaborative partnerships among coastal tribes, researchers, state fisheries, and health managers, as described in Trainer and King (2023), will contribute to the larger picture of Dinophysis distribution in North America. Patricio A. Díaz and Beatriz Reguera contributed equally.

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