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Morphological, Molecular, and Toxin Analysis of Field Populations of Alexandrium Genus from the Argentine Sea1

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Morphological, Molecular, and Toxin Analysis of Field Populations of Alexandrium Genus from the Argentine Sea1 J. Phycol. 53, 1206–1222 (2017) © 2017 Phycological Society of America DOI: 10.1111/jpy.12574 MORPHOLOGICAL, MOLECULAR, AND TOXIN ANALYSIS OF FIELD POPULATIONS OF ALEXANDRIUM GENUS FROM THE ARGENTINE SEA1 Elena Fabro,2 Gaston O. Almandoz, Martha Ferrario Division Ficologıa, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n (B1900FWA), La Plata, Argentina Consejo Nacional de Investigaciones Cientıficas y Tecnicas (CONICET), Buenos Aires, Argentina Uwe John, Urban Tillmann , Kerstin Toebe, Bernd Krock and Allan Cembella Alfred Wegener Institut-Helmholtz Zentrum fur€ Polar- und Meeresforschung, Am Handelshafen 12, 27570 Bremerhaven, Germany In the Argentine Sea, blooms of toxigenic Abbreviations: APC, apical pore complex; GTX, dinoflagellates of the Alexandrium tamarense species gonyautoxin(s); LC-FD, liquid chromatography with complex have led to fish and bird mortalities and fluorescence detection; LC-MS/MS, liquid chro- human deaths as a consequence of paralytic shellfish matography coupled to tandem mass spectrometry; poisoning (PSP). Yet little is known about the NeoSTX, neosaxitoxin; Po, apical pore plate; PSP, occurrence of other toxigenic species of the genus paralytic shellfish poisoning; PST, paralytic shellfish Alexandrium, or of their toxin composition beyond toxin(s); Sa, anterior sulcal plate; Sp, posterior coastal waters. The distribution of Alexandrium sulcal plate; SPX, spirolide(s); STX, saxitoxin; vp, species and related toxins in the Argentine Sea was ventral pore determined by sampling surface waters on an oceanographic expedition during austral spring from ~39°Sto48°S. Light microscope and SEM analysis for species identification and enumeration Among toxic marine dinoflagellates, the genus was supplemented by confirmatory PCR analysis Alexandrium is one of the best studied because of its from field samples. The most frequent Alexandrium tendency to form harmful algal blooms and its taxon identified by microscopy corresponded to the broad biogeographical distribution from polar, tem- classical description of A. tamarense. Only weak perate, and subtropical waters worldwide (Anderson signals of Group I from the A. tamarense species et al. 2012). From a morphological perspective, the complex were detected by PCR of bulk field genus Alexandrium is rather homogeneous, therefore samples, but phylogenetic reconstruction of rDNA detailed analysis of several characters such as cell sequences from single cells from one station size and shape, chain formation, sulcal list develop- Alexandrium ment, sulcal excavation, and size and shape of the assigned them to ribotype Group I ( 0 catenella). PCR probes for Alexandrium minutum and thecal plates (mainly Po, 1 ,6ʺ, Sp and Sa) are Alexandrium ostenfeldii yielded a positive signal, needed for species identification (Balech 1995). although A. minutum morphology did not completely Nevertheless, attempts to define consistent mor- match the classical description. Analysis of PSP phospecies within the genus have not always been toxin composition of plankton samples revealed successful and remain controversial (John et al. toxin profiles dominated by gonyautoxins (GTX1/ 2014). 4). The main toxic cyclic imine detected was 13- With the advent of molecular techniques, the clas- desMe-spirolide C and this supported the association sification of Alexandrium species has been revised by with A. ostenfeldii in the field. This study represents several authors. Phylogenetic analyses identified the first integrated molecular, morphological and well-supported clades within the genus, although toxinological analysis of field populations of the these were not always consistent with classical spe- genus Alexandrium in the Argentine Sea. cies descriptors (Penna et al. 2008, Anderson et al. 2012). Phylogenetic analyses inferred by maximum Key index words: Alexandrium minutum; Alexandrium ostenfeldii likelihood analysis of partial sequences of the LSU ; LC-FD; LC-MS/MS; PCR; PSP; south- rDNA gene showed the existence of three well-sup- western Atlantic; spirolides ported complexes of species: the Alexandrium osten- feldii group, the Alexandrium minutum group, and 1Received 19 January 2017. Accepted 22 July 2017. First Published the Alexandrium tamarense species complex (John Online 9 August 2017. Published Online 14 September 2017, Wiley Online Library (wileyonlinelibrary.com). et al. 2003, Lilly et al. 2007, Anderson et al. 2012). 2Author for correspondence: e-mail [email protected]. Within the Alexandrium tamarense species complex, Editorial Responsibility: S. Lin (Associate Editor) phylogenetic analysis has revealed distinct clusters 1206 ALEXANDRIUM SPECIES FROM THE ARGENTINE SEA 1207 of ribotypes. A comprehensive phylogeny con- peruvianum by Van Wagoner et al. 2011 and Bork- structed from a broad data set of ribosomal operon man et al. 2012), from the Netherlands (Van de sequences yielded ribosomal phylogenetic trees that Waal et al. 2015) and from the Baltic Sea (Salgado always recovered five distinct groups, showing et al. 2015, Harju et al. 2016). genetic distances separating the Groups as large as Particularly in western South Atlantic waters, PSP those observed between other Alexandrium species events and the presence of several toxic species of (Wang et al. 2014). A detailed examination of the Alexandrium have been known for many decades morphological criteria previously proposed for taxo- (Balech 1995). Toxic outbreaks are documented nomic identification demonstrated that most fea- from Argentina, Uruguay, and southern Brazil (e.g., tures are shared or variable among the five reported by Davison and Yentsch 1985, Carreto respective ribosomal groups, rendering them unsuit- et al. 1986, Brazeiro et al. 1997, Odebrecht et al. able for species definition and discrimination (John 2002). In the Argentine Sea, blooms of the A. ta- et al. 2003, 2014, Lilly et al. 2007, Anderson et al. marense species complex have been frequently 2012). In particular, Group I showed intragenomic detected during spring since 1980 (Carreto et al. rDNA variants dispersed across strains in the phylo- 1981, Esteves et al. 1992, Gayoso and Fulco 2006), genetic tree uniting the many different genotypes to leading in some cases to fish and bird mortalities the same or closely related populations (Miranda and also to human deaths (Elbusto et al. 1981, Vec- et al. 2012). Recently, named species have been pro- chio et al. 1986, Montoya et al. 1996, 1998, Montoya posed to describe the five ribotypes (John et al. and Carreto 2007). In southern Brazil coastal waters, 2014). The nomenclature of Group I has generated the first Alexandrium bloom was recorded in 1996 debate with different opinions on how to rename (Odebrecht et al. 2002). Specimens of the A. ta- the Group I members (John et al. 2014, Fraga et al. marense species complex were reported as belonging 2015); the Nomenclature Committee for Algae to Group I, now recognized as A. catenella (Prud’- (Prud’homme van Reine 2017) has finally estab- homme van Reine 2017), in Argentina (Penna et al. lished Alexandrium catenella as the valid name for 2008) and Brazil (Persich et al. 2006). The PST pro- this group based upon nomenclatural priority. ducer Gymnodinium catenatum was also recorded in Around half of the ~30 morphologically described northern Argentinean waters (Balech 1995) and it species of the genus Alexandrium are known to pro- was recently associated with PSP events (Sunesen duce toxins (Anderson et al. 2012). Most dangerous et al. 2014). The causative species of a toxic bloom for health are the paralytic shellfish toxins (PST), reported from southeastern Brazil near Rio de which are produced by certain members of the Janeiro (Menezes et al. 2007) was identified at the A. tamarense species complex and A. minutum, and time as A. minutum, although the authors observed are responsible for human illness and even deaths the presence of a strong reticulation on the of human seafood consumers and economic losses hypotheca that is not found in A. minutum. Further in aquaculture and fisheries (Boesch et al. 1997, analysis has suggested that this may represent a new Lagos 2003, Garcıa et al. 2004). This PST family of species with the proposed name Alexandrium fragae tetrahydropurine neurotoxins consists of saxitoxin (Branco et al. 2016). Along the Uruguayan coast, (STX) and more than three dozen naturally occur- members of the A. tamarense species complex have ring analogs. Among paralytic shellfish poisoning also been frequently found since 1980 (Davison and (PSP) toxins, the nonsulfated carbamoyl toxins STX Yentsch 1985, Brazeiro et al. 1997, Mendez et al. and neosaxitoxin (neoSTX) are the most potent 2000). The more distantly related, Alexandrium frater- blockers of voltage-gated Na+-ion channels, followed culus is typically nontoxic but has been associated by the sulfated carbamoyl toxins, such as the with PSP events from Uruguayan waters (Mendez gonyautoxins (GTX), then the decarbamoyl (dc-) 1993). toxins, and finally the N-sulfocarbamoyl (B and C Toxic strains of Alexandrium ostenfeldii have been toxins) as the least toxic group (Wiese et al. 2010). obtained from the Beagle Channel, southern Argen- In addition to the frequent presence of PST tina (Almandoz et al. 2014), but A. ostenfeldii has among populations of Alexandrium ostenfeldii, other not been previously reported from open shelf and toxins linked to this species include cyclic imine slope waters of the Argentine Sea. Nevertheless, an neurotoxins (Cembella et al. 2001, Franco et al. associated
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