Toxigenicity and biogeography of the diatom Pseudo-nitzschia across distinct environmental regimes in the South Atlantic Ocean

The community composition and toxigenicity of the diatom Pseudo-nitzschia in the northern Benguela Upwelling Zone and the open South Atlantic Ocean were characterized as part of a transoceanic survey conducted during the austral spring of 2007. Multiple morphological types of Pseudo-nitzschia were detected by light microscopy in coastal waters. Automated ribosomal intergenic spacer analysis (ARISA), a DNA-fingerprinting technique used to assess Pseudo-nitzschia community composition, detected 37 ARISA types distributed among 17 stations in both coastal and open-ocean regions. Through statistical analysis of abiotic factors, we identified 6 distinct environmental regimes across which Pseudo-nitzschia community composition varied. Pseudo-nitzschia were detected in open-ocean waters, where community composition differed between surface and deep chlorophyll maxima. The toxin produced by Pseudo-nitzschia, domoic acid (DA), was present in coastal waters both inside and outside the northern Benguela Upwelling Zone at potentially ecologically harmful levels, up to 184 ng DA l−1 and 4.6 pg DA cell−1. Partial internal transcribed spacer 1 (ITS1) clone libraries putatively identified at least 10 species in the South Atlantic, including P. inflatula, P. subpacifica, P. heimii, and P. galaxiae. Previously, these species were reported to produce DA at levels several orders of magnitude lower than our field measurements. Simple correlations were not able to identify obvious environmental triggers of DA production. Our findings suggest that species commonly believed to be weakly toxigenic could pose harm to humans and marine organisms, including those inhabiting southwestern African coastal regions.

[1]  Katherine Hubbard,et al.  Molecular characterization of Pseudo-nitzschia community structure and species ecology in a hydrographically complex estuarine system (Puget Sound, Washington, USA). , 2014, Marine ecology progress series.

[2]  A. Cembella,et al.  Toxigenic phytoplankton and concomitant toxicity in the mussel Choromytilus meridionalis off the west coast of South Africa , 2012 .

[3]  Thomas Mock,et al.  Frustule‐related gene transcription and the influence of diatom community composition on silica precipitation in an iron‐limited environment , 2012 .

[4]  M. Twiner,et al.  Comparative Analysis of Three Brevetoxin-Associated Bottlenose Dolphin (Tursiops truncatus) Mortality Events in the Florida Panhandle Region (USA) , 2012, PloS one.

[5]  M. Saito,et al.  Basin‐scale inputs of cobalt, iron, and manganese from the Benguela‐Angola front to the South Atlantic Ocean , 2012 .

[6]  C. Carlson,et al.  Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic. , 2012, Environmental microbiology.

[7]  S. Bates,et al.  CRYPTIC AND PSEUDO‐CRYPTIC DIVERSITY IN DIATOMS—WITH DESCRIPTIONS OF PSEUDO‐NITZSCHIA HASLEANA SP. NOV. AND P. FRYXELLIANA SP. NOV. 1 , 2012, Journal of phycology.

[8]  S. Bates,et al.  Pseudo-nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: revisiting previous paradigms , 2012 .

[9]  S. Bates,et al.  Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health , 2012 .

[10]  Fengzhu Sun,et al.  Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates , 2011, BMC Systems Biology.

[11]  R. Wells,et al.  Concurrent Exposure of Bottlenose Dolphins (Tursiops truncatus) to Multiple Algal Toxins in Sarasota Bay, Florida, USA , 2011, PloS one.

[12]  Kenneth W. Bruland,et al.  Toxic diatoms and domoic acid in natural and iron enriched waters of the oceanic Pacific , 2010, Proceedings of the National Academy of Sciences.

[13]  P. Tortell,et al.  Unveiling a phytoplankton hotspot at a narrow boundary between coastal and offshore waters , 2010, Proceedings of the National Academy of Sciences.

[14]  S. Quijano-Scheggia,et al.  Pseudo-nitzschia species on the Catalan coast: characterization and contribution to the current knowledge of the distribution of this genus in the Mediterranean Sea , 2010 .

[15]  B. Hickey,et al.  The physical oceanography of upwelling systems and the development of harmful algal blooms. , 2010, Progress in oceanography.

[16]  Vera L. Trainer,et al.  The distribution and impacts of harmful algal bloom species in eastern boundary upwelling systems , 2010 .

[17]  V. Trainer,et al.  Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas , 2010, Proceedings of the National Academy of Sciences.

[18]  David R Goodlett,et al.  Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction , 2010, The ISME Journal.

[19]  P. Claquin,et al.  Dynamics of Pseudo-nitzschia spp. and domoic acid production in a macrotidal ecosystem of the Eastern English Channel (Normandy, France) , 2010 .

[20]  J. Blanco,et al.  Amnesic shellfish poisoning (ASP) toxins in plankton and molluscs from Luanda Bay, Angola. , 2010, Toxicon : official journal of the International Society on Toxinology.

[21]  M. Ostrowski,et al.  The Benguela Current: An ecosystem of four components , 2009 .

[22]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[23]  V. Trainer,et al.  An ecological study of a massive bloom of toxigenic Pseudo‐nitzschia cuspidata off the Washington State coast , 2009 .

[24]  T. Probyn,et al.  Nitrogen nutrition in assemblages dominated by Pseudo-nitzschia spp., Alexandrium catenella and Dinophysis acuminata off the west coast of South Africa , 2009 .

[25]  Stephanie K. Moore,et al.  Variability of Pseudo‐nitzschia and domoic acid in the Juan de Fuca eddy region and its adjacent shelves , 2009 .

[26]  Deborah K. Steinberg,et al.  VERTIGO (VERtical Transport In the Global Ocean) : A study of particle sources and flux attenuation in the North Pacific , 2008 .

[27]  Katherine Hubbard,et al.  INTER‐ AND INTRASPECIFIC COMMUNITY STRUCTURE WITHIN THE DIATOM GENUS PSEUDO‐NITZSCHIA (BACILLARIOPHYCEAE) 1 , 2008, Journal of phycology.

[28]  Katherine Hubbard,et al.  IDENTIFICATION AND ASSESSMENT OF DOMOIC ACID PRODUCTION IN OCEANIC PSEUDO‐NITZSCHIA (BACILLARIOPHYCEAE) FROM IRON‐LIMITED WATERS IN THE NORTHEAST SUBARCTIC PACIFIC 1 , 2008, Journal of phycology.

[29]  M. Saito,et al.  Cobalt, manganese, and iron near the Hawaiian Islands: A potential concentrating mechanism for cobalt within a cyclonic eddy and implications for the hybrid-type trace metals , 2008 .

[30]  G. Ferreyra,et al.  Distribution and ecology of Pseudo-nitzschia species (Bacillariophyceae) in surface waters of the Weddell Sea (Antarctica) , 2008, Polar Biology.

[31]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[32]  J. Ehrman,et al.  Pseudo-nitzschia species population dynamics in the Quoddy Region, Bay of Fundy , 2007 .

[33]  S. M. McDonald,et al.  Identifying Pseudo-nitzschia species in natural samples using genus-specific PCR primers and clone libraries , 2007 .

[34]  R. Kudela,et al.  Contrasting wind patterns and toxigenic phytoplankton in the southern Benguela upwelling system , 2007 .

[35]  J. Ramsdell,et al.  Determination of domoic acid in seawater and phytoplankton by liquid chromatography-tandem mass spectrometry. , 2007, Journal of chromatography. A.

[36]  H. Kleivdal,et al.  Single-laboratory validation of the biosense direct competitive enzyme-linked immunosorbent assay (ELISA) for determination of domoic acid toxins in shellfish. , 2007, Journal of AOAC International.

[37]  Stephen B. Weisberg,et al.  Blooms of Pseudo-nitzschia and domoic acid in the San Pedro Channel and Los Angeles harbor areas of the Southern California Bight, 2003-2004 , 2007 .

[38]  R. Kudela,et al.  Nitrogenous preference of toxigenic Pseudo-nitzschia australis (Bacillariophyceae) from field and laboratory experiments , 2007 .

[39]  Gregory G. Leptoukh,et al.  Online analysis enhances use of NASA Earth science data , 2007 .

[40]  Libe Washburn,et al.  Circulation and environmental conditions during a toxigenic Pseudo-nitzschia australis bloom in the Santa Barbara Channel, California , 2006 .

[41]  P. Tett,et al.  Seasonality of Pseudo-nitzschia spp. (Bacillariophyceae) in western Scottish waters , 2006 .

[42]  S. Bernard,et al.  Real-time monitoring of harmful algal blooms in the southern Benguela , 2006 .

[43]  V. Trainer,et al.  The first closure of shellfish harvesting due to domoic acid in Puget Sound, Washington, USA , 2006 .

[44]  B. Hickey,et al.  The nearshore advection of a toxigenic Pseudo-nitzschia bloom and subsequent domoic acid contamination of intertidal bivalves , 2006 .

[45]  G. Rocap,et al.  Culture Isolation and Culture-Independent Clone Libraries Reveal New Marine Synechococcus Ecotypes with Distinctive Light and N Physiologies , 2006, Applied and Environmental Microbiology.

[46]  M. Saito,et al.  Examination of precipitation chemistry and improvements in precision using the Mg(OH)2 preconcentration inductively coupled plasma mass spectrometry (ICP-MS) method for high-throughput analysis of open-ocean Fe and Mn in seawater , 2006 .

[47]  I. Hewson,et al.  Improved Strategy for Comparing Microbial Assemblage Fingerprints , 2006, Microbial Ecology.

[48]  B. Hickey,et al.  Transport of surface waters from the Juan de Fuca eddy region to the Washington coast , 2005 .

[49]  Ulf Riebesell,et al.  Synthesis of iron fertilization experiments: From the iron age in the age of enlightenment , 2005 .

[50]  M. Saito,et al.  Cobalt and nickel in the Peru upwelling region: A major flux of labile cobalt utilized as a micronutrient , 2004 .

[51]  P. Harrison,et al.  Environmental conditions and phytoplankton dynamics associated with Pseudo-nitzschia abundance and domoic acid in the Juan de Fuca eddy , 2004 .

[52]  G. Hasle,et al.  A STUDY OF THE PSEUDO‐NITZSCHIA PSEUDODELICATISSIMA/CUSPIDATA COMPLEX (BACILLARIOPHYCEAE): WHAT IS P. PSEUDODELICATISSIMA? 1 , 2003 .

[53]  Ø. Moestrup,et al.  The marine diatom Pseudo-nitzschia galaxiae sp. nov. (Bacillariophyceae): morphology and phylogenetic relationships , 2002 .

[54]  M. Silver,et al.  From sanddabs to blue whales: the pervasiveness of domoic acid. , 2002, Toxicon : official journal of the International Society on Toxinology.

[55]  G. Hasle Are most of the domoic acid-producing species of the diatom genus Pseudo-nitzschia cosmopolites? , 2002 .

[56]  Ø. Moestrup,et al.  TAXONOMIC NOTES ON THE MARINE DIATOM GENUS PSEUDO-NITZSCHIA IN THE ANDAMAN SEA NEAR THE ISLAND OF PHUKET, THAILAND, WITH A DESCRIPTION OF PSEUDO-NITZSCHIA MICROPORA SP. NOV. , 2002 .

[57]  M. Polz,et al.  Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. , 2002, Nucleic acids research.

[58]  M. T. Maldonado,et al.  The effect of Fe and Cu on growth and domoic acid production by Pseudo-nitzschia multiseries and Pseudo‐nitzschia australis , 2002 .

[59]  M. Saito,et al.  Complexation of cobalt by natural organic ligands in the Sargasso Sea as determined by a new high-sensitivity electrochemical cobalt speciation method suitable for open ocean work , 2001 .

[60]  M. Busman,et al.  Domoic acid production near California coastal upwelling zones, June 1998 , 2000 .

[61]  Grant C. Pitcher,et al.  Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997 , 2000 .

[62]  Roman Marin,et al.  Mortality of sea lions along the central California coast linked to a toxic diatom bloom , 2000, Nature.

[63]  Lisa R. Moore,et al.  Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes , 1998, Nature.

[64]  Aaron M.Ellison PC‐ORD: Multivariate Analysis of Ecological Data , 1998, The Bulletin of the Ecological Society of America.

[65]  L. Shapiro,et al.  The occurrence of the toxic diatom genus Pseudo-nitzschia (Bacillariophyceae) on the West Coast of the USA, 1920–1996: a review , 1997 .

[66]  Youlian Pan,et al.  CHANGES IN DOMOIC ACID PRODUCTION AND CELLULAR CHEMICAL COMPOSITION OF THE TOXIGENIC DIATOM PSEUDO‐NITZSCHIA MULTISERIES UNDER PHOSPHATE LIMITATION 1 , 1996 .

[67]  Youlian Pan,et al.  Effects of silicate limitation on production of domoic acid, a neurotoxin, by the diatom Pseudo-nitzschia multiseries. I. Batch culture studies , 1996 .

[68]  D. J. Douglas,et al.  Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. , 1995, Natural toxins.

[69]  S. Bates,et al.  Controls on Domoic Acid Production by the Diatom Nitzschia pungens f. multiseries in Culture: Nutrients and Irradïance , 1991 .

[70]  R. Zatorre,et al.  Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. , 1990, The New England journal of medicine.

[71]  S. Bates,et al.  Pennate Diatom Nitzschia pungens as the Primary Source of Domoic Acid, a Toxin in Shellfish from Eastern Prince Edward Island, Canada , 1989 .

[72]  Mark A. Ragan,et al.  Identification of domoic acid, a neuroexcitatory amino acid, in toxic mussels from eastern Prince Edward Island , 1989 .

[73]  R. S. Alberte,et al.  Photosynthetic and cellular photoadaptive characteristics of three ecotypes of the marine diatom, Skeletonema costatum (Grev.) Cleve , 1985 .

[74]  Dongmei Ai,et al.  Efficient statistical significance approximation for local similarity analysis of high-throughput time series data , 2013, Bioinform..

[75]  M. C. Horner-Devine,et al.  Bacterial community composition differs with species and toxigenicity of the diatom Pseudo-nitzschia , 2012 .

[76]  R. Schlitzer Ocean Data View , 2007 .

[77]  G. Ferreyra,et al.  The genus Pseudo-nitzschia (Bacillariophyceae) in continental shelf waters of Argentina (Southwestern Atlantic Ocean, 38–55°S) , 2007 .

[78]  D. Sarno,et al.  The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae , 2005 .

[79]  M. Silver,et al.  Field evidence of krill grazing on the toxic diatom genus pseudo-Nitzschia in Monterey Bay, California , 2003 .

[80]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[81]  K. R. Clarke,et al.  Change in marine communities : an approach to statistical analysis and interpretation , 2001 .

[82]  S. Bates,et al.  Bloom Dynamics and Physiology of Domoic-Acid-Producing Pseudo-nitzschia Species , 2001 .

[83]  N. Adams,et al.  Environmental conditions associated with domoic acid in razor clams on the Washington coast , 2000 .

[84]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[85]  G. Hasle,et al.  Chapter 2 – Marine Diatoms , 1996 .

[86]  M. Quilliam,et al.  EPIDEMIOLOGY OF DOMOIC ACID POISONING IN BROWN PELICANS (PELECANUS OCCIDENTALIS) AND BRANDT'S CORMORANTS (PHALA CROCORAX PENICILLA TUS) IN CALIFORNIA , 1993 .

[87]  G. Walker-Arnott What are Marine Diatoms , 1859 .