Current Techniques for Detecting and Monitoring Algal Toxins and Causative Harmful Algal Blooms

The detection and monitoring techniques for algal toxins and the causative harmful algal blooms (HABs) are essential for the protection of aquatic lives, shellfish safety, drinking water quality, and public health. Toward the development of fast, easy, and reliable techniques, much progress has been made during the last decade for the qualitative and quantitative analysis of algal toxins. This review highlights the recent progress and new trends of these analytical and monitoring tools, ranging from in-situ quick screening protocols for the monitoring of algal blooms to mass spectrometric analysis of trace levels of various algal toxins and structural elucidation. Solid-phase adsorption toxin tracking (SPATT) deployed in the field for the passive sampling of algal toxins has been recently validated, and improved ELISA-based methods with lower detection limits for more toxins have become commercially available for both screening and routine monitoring purposes. Liquid chromatography-mass spectrometry with several recent mass spectrometric innovations has expanded our understanding of traditional toxins, their metabolites along with newly discovered toxins of ecological importance. Several established in vivo and in vitro bioassays will continue to be used as benchmark toxicological testing of algal toxins; however, newly emerged molecular probing techniques such as real-time quantitative polymerase chain reaction (qPCR) have extended our ability to trace algal toxins from causative organisms at the molecular level. New chemical and biological sensors, lab-on-chip and remote sensing of blooms being developed will hold promise for early warning and routine monitoring to better manage and protect our freshwater, coastal and marine resources from adverse impact by harmful algal blooms.

[1]  M. He,et al.  On the Recurrent Ulva prolifera Blooms in the Yellow Sea and East China Sea , 2010 .

[2]  Reinhard Niessner,et al.  Highly sensitive immunoassay based on a monoclonal antibody specific for [4-arginine]microcystins , 2001 .

[3]  S. Richardson Environmental mass spectrometry: emerging contaminants and current issues. , 2004, Analytical chemistry.

[4]  Gian Paolo Rossini,et al.  Functional assays in marine biotoxin detection. , 2005, Toxicology.

[5]  L. Botana,et al.  Study of solid phase adsorption of paralytic shellfish poisoning toxins (PSP) onto different resins , 2011 .

[6]  Huijuan Liu,et al.  Cyanobacteria and their toxins in Guanting Reservoir of Beijing, China. , 2008, Journal of hazardous materials.

[7]  G. Gerdts,et al.  Simultaneous analysis of different algal toxins by LC-MS , 2002 .

[8]  N. Gan,et al.  An ELISA-like time-resolved fluorescence immunoassay for microcystin detection. , 2004, Clinica chimica acta; international journal of clinical chemistry.

[9]  F. Yu,et al.  Development of a sensitive ELISA for the determination of microcystins in algae. , 2002, Journal of agricultural and food chemistry.

[10]  M. Satake,et al.  A sensitive LC-MS/MS assay for brevisulcenal and brevisulcatic acid toxins produced by the dinoflagellate Karenia brevisulcata. , 2014, Toxicon : official journal of the International Society on Toxinology.

[11]  C. Dell’Aversano,et al.  Influence of temperature and salinity on Ostreopsis cf. ovata growth and evaluation of toxin content through HR LC-MS and biological assays. , 2012, Water research.

[12]  Lora E. Fleming,et al.  Blue green algal (cyanobacterial) toxins, surface drinking water, and liver cancer in Florida , 2002 .

[13]  D. Dietrich,et al.  Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? , 2005, Toxicology and applied pharmacology.

[14]  G. Gerdts,et al.  Overview of key phytoplankton toxins and their recent occurrence in the North and Baltic Seas , 2005, Environmental toxicology.

[15]  L. Campbell,et al.  A modified assay to determine hemolytic toxin variability among Karenia clones isolated from the Gulf of Mexico , 2006 .

[16]  G. Boyer,et al.  Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. , 2005, Environmental science & technology.

[17]  J. Cooney,et al.  A novel pectenotoxin, PTX-12, in Dinophysis spp. and shellfish from Norway. , 2004, Chemical research in toxicology.

[18]  G. Rollwagen‐Bollens,et al.  Environmental influence on cyanobacteria abundance and microcystin toxin production in a shallow temperate lake. , 2015, Ecotoxicology and environmental safety.

[19]  A. Jex,et al.  Rapid, multiplex-tandem PCR assay for automated detection and differentiation of toxigenic cyanobacterial blooms. , 2013, Molecular and cellular probes.

[20]  J. Yates,et al.  Structural characterization of toxic cyclic peptides from blue-green algae by tandem mass spectrometry. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[21]  T. Msagati,et al.  Supported liquid membrane-liquid chromatography–mass spectrometry analysis of cyanobacterial toxins in fresh water systems , 2012 .

[22]  S. Sauvé,et al.  Total microcystins analysis in water using laser diode thermal desorption-atmospheric pressure chemical ionization-tandem mass spectrometry. , 2014, Analytica chimica acta.

[23]  S. Watson,et al.  New Microcystin Concerns in the Lower Great Lakes , 2003 .

[24]  C. Fanali,et al.  Monitoring algal toxins in lake water by liquid chromatography tandem mass spectrometry. , 2006, Environmental science & technology.

[25]  Martin Reinhard,et al.  Emerging contaminants of public health significance as water quality indicator compounds in the urban water cycle. , 2014, Environment international.

[26]  A. Penna,et al.  First finding of Ostreopsis cf. ovata toxins in marine aerosols. , 2014, Environmental science & technology.

[27]  A. Gago-Martínez,et al.  Further improvements in the application of high-performance liquid chromatography, capillary electrophoresis and capillary electrochromatography to the analysis of algal toxins in the aquatic environment. , 2003, Journal of chromatography. A.

[28]  Eric A. Johnson,et al.  Association of toxin-producing Clostridium botulinum with the macroalga Cladophora in the Great Lakes. , 2013, Environmental science & technology.

[29]  Lenka Šejnohová,et al.  The first occurrence of the cyanobacterial alkaloid toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC/MS methods. , 2009, Toxicon : official journal of the International Society on Toxinology.

[30]  C. Madramootoo,et al.  Development and application of a multiplex qPCR technique to detect multiple microcystin-producing cyanobacterial genera in a Canadian freshwater lake , 2014, Journal of Applied Phycology.

[31]  J. Eriksson,et al.  Rapid analysis of peptide toxins in cyanobacteria. , 1988, Journal of chromatography.

[32]  M. Smyth,et al.  Electrochemical detection of microcystins, cyanobacterial peptide hepatotoxins, following high-performance liquid chromatography. , 1998, Journal of chromatography. A.

[33]  M. Hennion,et al.  Hepatotoxin Production Kinetics of the Cyanobacterium Microcystis aeruginosa PCC 7820, as Determined by HPLC−Mass Spectrometry and Protein Phosphatase Bioassay , 2000 .

[34]  D. Dietrich,et al.  Comparison of two ELISA-based methods for the detection of microcystins in blood serum. , 2014, Chemico-biological interactions.

[35]  D. Kerr,et al.  A neurophysiological method of rapid detection and analysis of marine algal toxins. , 1999, Toxicon : official journal of the International Society on Toxinology.

[36]  Rui Rosa,et al.  Detection of domoic acid, the amnesic shellfish toxin, in the digestive gland of Eledone cirrhosa and E. moschata (Cephalopoda, Octopoda) from the Portuguese coast , 2005 .

[37]  A. N. Moura,et al.  Cyanobacteria, microcystins and cylindrospermopsin in public drinking supply reservoirs of Brazil. , 2014, Anais da Academia Brasileira de Ciencias.

[38]  Sevasti-Kiriaki Zervou,et al.  Determination of microcystins and nodularin (cyanobacterial toxins) in water by LC-MS/MS. Monitoring of Lake Marathonas, a water reservoir of Athens, Greece. , 2013, Journal of hazardous materials.

[39]  Vera L. Trainer,et al.  Detection of the toxin domoic acid from clam extracts using a portable surface plasmon resonance biosensor , 2007 .

[40]  Roman Marin,et al.  Remote, subsurface detection of the algal toxin domoic acid onboard the Environmental Sample Processor: Assay development and field trials , 2009 .

[41]  J. Ramsdell,et al.  Review and assessment of in vitro detection methods for algal toxins. , 2001, Journal of AOAC International.

[42]  S. Costanzo,et al.  Occurrence and seasonal variations of algal toxins in water, phytoplankton and shellfish from North Stradbroke Island, Queensland, Australia. , 2007, Marine environmental research.

[43]  J. González-Pérez,et al.  Detection of cylindrospermopsin toxin markers in cyanobacterial algal blooms using analytical pyrolysis (Py-GC/MS) and thermally-assisted hydrolysis and methylation (TCh-GC/MS). , 2014, Chemosphere.

[44]  W. Guida,et al.  Chemosensors for the marine toxin saxitoxin. , 2002, Journal of the American Chemical Society.

[45]  P. Hess,et al.  Extended evaluation of polymeric and lipophilic sorbents for passive sampling of marine toxins. , 2014, Toxicon : official journal of the International Society on Toxinology.

[46]  T. Aune,et al.  Detection and identification of spirolides in norwegian shellfish and plankton. , 2005, Chemical research in toxicology.

[47]  I. Creed,et al.  Suitability of a cytotoxicity assay for detection of potentially harmful compounds produced by freshwater bloom-forming algae. , 2014, Harmful algae.

[48]  R. Balasubramanian,et al.  Toxicological evaluation of microcystins in aquatic fish species: current knowledge and future directions. , 2013, Aquatic toxicology.

[49]  C. Miles,et al.  New esters of okadaic acid in seawater and blue mussels (Mytilus edulis). , 2008, Journal of agricultural and food chemistry.

[50]  E. Phlips,et al.  Investigation of extraction and analysis techniques for Lyngbya wollei derived Paralytic Shellfish Toxins. , 2012, Toxicon : official journal of the International Society on Toxinology.

[51]  Tong Zhang,et al.  Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples , 2006, Applied Microbiology and Biotechnology.

[52]  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.

[53]  M. Hennion,et al.  Evaluation of an ELISA Kit for the Monitoring of Microcystins (Cyanobacterial Toxins) in Water and Algae Environmental Samples , 1999 .

[54]  Rajasekhar Balasubramanian,et al.  Methods and Approaches Used for Detection of Cyanotoxins in Environmental Samples: A Review , 2013 .

[55]  D. D. Lefebvre,et al.  Algal blooms: proactive strategy. , 2014, Science.

[56]  D. Anderson,et al.  Approaches to monitoring, control and management of harmful algal blooms (HABs). , 2009, Ocean & coastal management.

[57]  H. Zhang,et al.  Identification of microcystins in waters used for daily life by people who live on Tai Lake during a serious cyanobacteria dominated bloom with risk analysis to human health , 2009, Environmental toxicology.

[58]  Jinhui Wang,et al.  Occurrence and potential risks of harmful algal blooms in the East China Sea. , 2009, The Science of the total environment.

[59]  M. Sandvik,et al.  A convenient and cost-effective method for monitoring marine algal toxins with passive samplers. , 2009, Toxicon : official journal of the International Society on Toxinology.

[60]  R. Franklin,et al.  Exposure to the cyanotoxin microcystin arising from interspecific differences in feeding habits among fish and shellfish in the James River Estuary, Virginia. , 2014, Environmental science & technology.

[61]  L. Stobo,et al.  Surveillance of algal toxins in shellfish from Scottish waters. , 2008, Toxicon : official journal of the International Society on Toxinology.

[62]  Tyler A. Johnson,et al.  Rapid Enzyme-linked Immunosorbent Assay for Detection of the Algal Toxin Domoic Acid , 2008 .

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

[64]  B. Reguera,et al.  Extraction of microalgal toxins by large-scale pumping of seawater in Spain and Norway, and isolation of okadaic acid and dinophysistoxin-2. , 2007, Toxicon : official journal of the International Society on Toxinology.

[65]  R. Pistocchi,et al.  High sensitivity bioassay of paralytic (PSP) and amnesic (ASP) algal toxins based on the fluorimetric detection of [Ca(2+)](i) in rat cortical primary cultures. , 2000, Toxicon : official journal of the International Society on Toxinology.

[66]  P. Xie,et al.  Quantitative liquid chromatography-tandem mass spectrometry method for determination of microcystin-RR and its glutathione and cysteine conjugates in fish plasma and bile. , 2014, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[67]  Mouna Fertouna-Bellakhal,et al.  Harmful algal blooms (HABs) associated with phycotoxins in shellfish: What can be learned from five years of monitoring in Bizerte Lagoon (Southern Mediterranean Sea)? , 2014 .

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

[69]  M. Moline,et al.  Improved monitoring of HABs using autonomous underwater vehicles (AUV) , 2006 .

[70]  A. Furey,et al.  Application of passive (SPATT) and active sampling methods in the profiling and monitoring of marine biotoxins. , 2014, Toxicon : official journal of the International Society on Toxinology.

[71]  David R. Walt,et al.  Fiber-Optic Microarray for Simultaneous Detection of Multiple Harmful Algal Bloom Species , 2006, Applied and Environmental Microbiology.

[72]  W. Nelson,et al.  Differentiation of algae clones on the basis of resonance Raman spectra excited by visible light. , 1998, Analytical chemistry.

[73]  D. B. Nedwell,et al.  Environmental costs of freshwater eutrophication in England and Wales. , 2003, Environmental science & technology.

[74]  V. Vasconcelos,et al.  Methods to detect cyanobacteria and their toxins in the environment , 2014, Applied Microbiology and Biotechnology.

[75]  Xiao-ru Wang,et al.  Detection, occurrence and monthly variations of typical lipophilic marine toxins associated with diarrhetic shellfish poisoning in the coastal seawater of Qingdao City, China. , 2014, Chemosphere.

[76]  V. Trainer,et al.  Remote sampling of harmful algal blooms: A case study on the Washington State coast ☆ , 2012 .

[77]  C. Miles,et al.  Enzyme-linked immunosorbent assay for the detection of yessotoxin and its analogues. , 2004, Journal of Agricultural and Food Chemistry.

[78]  D R Dietrich,et al.  Congener-independent immunoassay for microcystins and nodularins. , 2001, Environmental science & technology.

[79]  L. MacKenzie,et al.  In situ passive solid-phase adsorption of micro-algal biotoxins as a monitoring tool. , 2010, Current opinion in biotechnology.

[80]  M. Lam,et al.  Solid-phase extraction-fluorimetric high performance liquid chromatographic determination of domoic acid in natural seawater mediated by an amorphous titania sorbent. , 2007, Analytica chimica acta.

[81]  Raj Mutharasan,et al.  Highly sensitive and rapid detection of microcystin-LR in source and finished water samples using cantilever sensors. , 2011, Environmental science & technology.

[82]  M. Quilliam,et al.  Quantitative 1H NMR with external standards: use in preparation of calibration solutions for algal toxins and other natural products. , 2005, Analytical chemistry.

[83]  H. Chou,et al.  A modified high-performance liquid chromatography method for analysis of PSP toxins in dinoflagellate, Alexandrium minutum, and shellfish from Taiwan , 2002 .

[84]  Callee M. Walsh,et al.  High-throughput quantitative analysis of domoic acid directly from mussel tissue using Laser Ablation Electrospray Ionization - tandem mass spectrometry. , 2014, Toxicon : official journal of the International Society on Toxinology.

[85]  R. Kudela,et al.  Detection of persistent microcystin toxins at the land-sea interface in Monterey Bay, California , 2014 .

[86]  R. Lewis,et al.  Ciguatera: recent advances but the risk remains. , 2000, International journal of food microbiology.

[87]  Wes R. Budakowski,et al.  Liquid chromatography-electrospray ionisation-mass spectrometry based method for the simultaneous determination of algal and cyanobacterial toxins in phytoplankton from marine waters and lakes followed by tentative structural elucidation of microcystins. , 2003, Journal of chromatography. A.

[88]  P. McNabb,et al.  Solid phase adsorption toxin tracking (SPATT): a new monitoring tool that simulates the biotoxin contamination of filter feeding bivalves. , 2004, Toxicon : official journal of the International Society on Toxinology.

[89]  N. Kulagina,et al.  Detection of marine toxins, brevetoxin-3 and saxitoxin, in seawater using neuronal networks. , 2006, Environmental science & technology.

[90]  M. Halme,et al.  Verification and quantification of saxitoxin from algal samples using fast and validated hydrophilic interaction liquid chromatography-tandem mass spectrometry method. , 2012, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.