Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Multiplex biotoxin surface plasmon resonance method for marine biotoxins in algal and seawater samples

  • 2698 Accesses

  • 46 Citations

Abstract

A multiplex surface plasmon resonance (SPR) biosensor method for the detection of paralytic shellfish poisoning (PSP) toxins, okadaic acid (and analogues) and domoic acid was developed. This method was compared to enzyme-linked immunosorbent assay (ELISA) methods. Seawater samples (n = 256) from around Europe were collected by the consortia of an EU project MIcroarrays for the Detection of Toxic Algae (MIDTAL) and evaluated using each method. A simple sample preparation procedure was developed which involved lysing and releasing the toxins from the algal cells with glass beads followed by centrifugation and filtering the extract before testing for marine biotoxins by both multi-SPR and ELISA. Method detection limits based on IC20 values for PSP, okadaic acid and domoic acid toxins were 0.82, 0.36 and 1.66 ng/ml, respectively, for the prototype multiplex SPR biosensor. Evaluation by SPR for seawater samples has shown that 47, 59 and 61 % of total seawater samples tested positive (result greater than the IC20) for PSP, okadaic acid (and analogues) and domoic acid toxins, respectively. Toxic samples were received mainly from Spain and Ireland. This work has demonstrated the potential of multiplex analysis for marine biotoxins in algal and seawater samples with results available for 24 samples within a 7 h period for three groups of key marine biotoxins. Multiplex immunological methods could therefore be used as early warning monitoring tools for a variety of marine biotoxins in seawater samples.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adams AL, Doucette TA, James R, Ryan CL (2009) Persistent changes in learning and memory in rats following neonatal treatment with domoic acid. Physiol Behav 96:505–512

  2. Alvarez G, Uribe E, Quijano-Scheggia S, Lopez-Rivera A, Marino C, Blanco J (2009) Domoic acid production by Pseudo-nitzschia australis and Pseudo-nitzschia calliantha isolated from North Chile RID C-3959-2011. Harmful Algae 8:938–945

  3. Anderson D (1994) Red tides. Sci Am 271:62–68

  4. Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52:342–347

  5. Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu Rev Mar Sci 4:143–176

  6. Besiktepe S, Ryabushko L, Ediger D, Yimaz D, Zenginer A, Ryabushko V, Lee R (2008) Domoic acid production by Pseudo-nitzschia calliantha Lundholm, Moestrup et Hasle (bacillariophyta) isolated from the Black Sea. Harmful Algae 7:438–442

  7. Blanco J, Livramento F, Rangel IM (2010) Amnesic shellfish poisoning (ASP) toxins in plankton and molluscs from Luanda Bay, Angola. Toxicon 55:541–546

  8. Bravo I, Fernandez M, Ramilo I, Martinez A (2001) Toxin composition of the toxic dinoflagellate Prorocentrum lima isolated from different locations along the Galician coast (NW Spain). Toxicon 39:1537–1545

  9. Brown L, Bresnan E, Graham J, Lacaze J, Turrell E, Collins C (2010) Distribution, diversity and toxin composition of the genus Alexandrium (Dinophyceae) in Scottish waters. Eur J Phycol 45:375–393

  10. Campbell K, Stewart LD, Doucette GJ, Fodey TL, Haughey SA, Vilarino N, Kawatsu K, Elliott CT (2007) Assessment of specific binding proteins suitable for the detection of paralytic shellfish poisons using optical biosensor technology. Anal Chem 79:5906–5914

  11. Campbell K, Huet A, Charlier C, Higgins C, Delahaut P, Elliott CT (2009) Comparison of ELISA and SPR biosensor technology for the detection of paralytic shellfish poisoning toxins. J Chromatogr B-Analy Technol Biomed Life Sci 877:4079–4089

  12. Campbell K, Haughey SA, van den Top H, van Egmond H, Vilarino N, Botana LM, Elliott CT (2010) Single laboratory validation of a surface plasmon resonance biosensor screening method for paralytic shellfish poisoning toxins. Anal Chem 82:2977–2988

  13. Campbell K, Rawn DFK, Niedzwiadek B, Elliott CT (2011a) Paralytic shellfish poisoning (PSP) toxin binders for optical biosensor technology: problems and possibilities for the future: a review. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 28:711–725

  14. Campbell K, McGrath T, Sjolander S, Hanson T, Tidare M, Jansson O, Moberg A, Mooney M, Elliott C, Buijs J (2011b) Use of a novel micro-fluidic device to create arrays for multiplex analysis of large and small molecular weight compounds by surface plasmon resonance. Biosens Bioelectron 26:3029–3036

  15. Chadsey M, Trainer VL, Leschine TM (2012) Cooperation of science and management for harmful algal blooms: domoic acid and the Washington Coast Razor clam fishery. Coast Manag 40:33–54

  16. Cusack C, Bates S, Quilliam M, Patching J, Raine R (2002) Confirmation of domoic acid production by Pseudo-nitzschia australis (Bacillariophyceae) isolated from Irish waters. J Phycol 38:1106–1112

  17. de la Iglesia P, Gimenez G, Diogene J (2008) Determination of dissolved domoic acid in seawater with reversed-phase extraction disks and rapid resolution liquid chromatography tandem mass spectrometry with head-column trapping. J Chromatogr 1215:116–124

  18. Del Rio R, Bargu S, Baltz D, Fire S, Peterson G, Wang Z (2010) Gulf menhaden (Brevoortia patronus): a potential vector of domoic acid in coastal Louisiana food webs. Harmful Algae 10:19–29

  19. Devlin RA, Campbell K, Kawatsu K, Elliott CT (2011) Physical and immunoaffinity extraction of paralytic shellfish poisoning toxins from cultures of the dinoflagellate Alexandrium tamarense. Harmful Algae 10:542–548

  20. Dubois M, Demoulin L, Charlier C, Singh G, Godefroy SB, Campbell K, Elliott CT, Delahaut P (2010) Development of ELISAs for detecting domoic acid, okadaic acid, and saxitoxin and their applicability for the detection of marine toxins in samples collected in Belgium. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 27:859–868

  21. Fehling J, Davidson K, Bolch C, Bates S (2004) Growth and domoic acid production by Pseudo-nitzschia seriata (Bacillariophyceae) under phosphate and silicate limitation. J Phycol 40:674–683

  22. Fleming LE, Broad K, Clement A, Dewailly E, Elmir S, Knap A, Pomponi SA, Smith S, Gabriele HS, Walsh P (2006) Oceans and human health: emerging public health risks in the marine environment. Mar Pollut Bull 53:545–560

  23. Fonfria ES, Vilarino N, Campbell K, Elliott C, Haughey SA, Ben-Gigirey B, Vieites JM, Kawatsu K, Botana LM (2007) Paralytic shellfish poisoning detection by surface plasmon resonance-based biosensors in shellfish matrixes. Anal Chem 79:6303–6311

  24. Fux E, Bire R, Hess P (2009) Comparative accumulation and composition of lipophilic marine biotoxins in passive samplers and in mussels (M. edulis) on the West Coast of Ireland. Harmful Algae 8:523–537

  25. Fux E, Smith JL, Tong M, Guzman L, Anderson DM (2011) Toxin profiles of five geographical isolates of Dinophysis spp. from North and South America. Toxicon 57:275–287

  26. Gerssen A, Mulder PPJ, de Boer J (2011) Screening of lipophilic marine toxins in shellfish and algae: development of a library using liquid chromatography coupled to orbitrap mass spectrometry. Anal Chim Acta 685:176–185

  27. Glibert PM, Anderson DM, Gentein P, Graneli E, Sellner KG (2005) The global, complex phenomena of harmful algal blooms. Oceanography 18:136–147

  28. Hackett JD, Tong M, Kulis DM, Fux E, Hess P, Bire R, Anderson DM (2009) DSP toxin production de novo in cultures of Dinophysis acuminata (Dinophyceae) from North America RID G-1761-2010. Harmful Algae 8:873–879

  29. Hallegraeff G (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

  30. Hallegraeff G, Bolch C (1992) Transport of diatom and dinoflagellate resting spores in ships ballast water—implications for plankton biogeography and aquaculture. J Plankton Res 14:1067–1084

  31. Halme M, Rapinoja M, Karjalainen M, Vanninen P (2012) Verification and quantification of saxitoxin from algal samples using fast and validated hydrophilic interaction liquid chromatography-tandem mass spectrometry method. J Chromatogr B-Anal Technol Biomed Life Sci 880:50–57

  32. Haughey SA, Campbell K, Yakes BJ, Prezioso SM, DeGrasse SL, Kawatsu K, Elliott CT (2011) Comparison of biosensor platforms for surface plasmon resonance based detection of paralytic shellfish toxins. Talanta 85:519–526

  33. He H, Li H, Jiang Y, Chen F (2005) Determination of paralytic shellfish poisoning toxins in cultured microalgae by high-performance liquid chromatography with fluorescence detection. Anal Bioanal Chem 383:1014–1017

  34. Honkanen R, Codispoti B, Tse K, Boynton A (1994) Characterization of natural toxins with inhibitory activity against serine/threonine protein phosphatases. Toxicon 32:519–519

  35. Kao CY (1996) Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena. Pharmacol 18:997–1049

  36. Lefebvre KA, Bill BD, Erickson A, Baugh KA, O'Rourke L, Costa PR, Nance S, Trainer VL (2008) Characterization of intracellular and extracellular saxitoxin levels in both field and cultured Alexandrium spp. samples from Sequim Bay, Washington RID F-2192-2011. Mar Drugs 6:103–116

  37. Llamas NM, Stewart L, Fodey T, Higgins HC, Velasco MLR, Botana LM, Elliott CT (2007) Development of a novel immunobiosensor method for the rapid detection of okadaic acid contamination in shellfish extracts. Anal Bioanal Chem 389:581–587

  38. Mafra LL Jr, Leger C, Bates SS, Quilliam MA (2009) Analysis of trace levels of domoic acid in seawater and plankton by liquid chromatrography without derivatization, using UV or mass spectrometry detection. J Chromatogr 1216:6003–6011

  39. Marchesini GR, Hooijerink H, Haasnoot W, Buijs J, Campbell K, Elliott CT, Nielen MWF (2009) Towards surface plasmon resonance biosensing combined with bioaffinity-assisted nano HILIC liquid chromatography time-of-flight mass spectrometry identification of paralytic shellfish poisons. Trac-Trends Anal Chem 28:792–803

  40. Montoya NG, Fulco VK, Carignan MO, Carreto JI (2010) Toxin variability in cultured and natural populations of Alexandrium tamarense from southern South America—evidences of diversity and environmental regulation. Toxicon 56:1408–1418

  41. Oshima Y (1995) Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J AOAC Int 78:528–532

  42. Pocklington JE, Milley JE, Bates SS, Bird CJ, De Freitas ASW, Quilliam MA (1990) Trace determination of domoic acid in seawater and phytoplankton by high performance liquid chromatography of the fluorenylmethoxycarbonyl (FMOC) derivative. Int J Environ Anal Chem 28:351–368

  43. Quijano-Scheggia S, Garces E, Andree KB, de la Iglesia P, Diogene J, Fortuno J, Camp J (2010) Pseudo-nitzschia species on the Catalan coast: characterization and contribution to the current knowledge of the distribution of this genus in the Mediterranean Sea RID C-5701-2011. Sci Mar 74:395–410

  44. Ravn H, Anthoni U, Christophersen C, Nielsen P, Oshima Y (1995) Standardized extraction method for paralytic shellfish toxins in phytoplankton. J Appl Phycol 7:589–594

  45. Rawn DFK, Niedzwiadek B, Campbell K, Higgins HC, Elliott CT (2009) Evaluation of surface plasmon resonance relative to high pressure liquid chromatography for the determination of paralytic shellfish toxins. J Agric Food Chem 57:10022–10031

  46. Smith FMJ, Wood SA, van Ginkel R, Broady PA, Gaw S (2011) First report of saxitoxin production by a species of the freshwater benthic cyanobacterium, Scytonema Agardh. Toxicon 57:566–573

  47. Stewart LD, Elliott CT, Walker AD, Curran RM, Connolly L (2009a) Development of a monoclonal antibody binding okadaic acid and dinophysistoxins-1,-2 in proportion to their toxicity equivalence factors. Toxicon 54:491–498

  48. Stewart LD, Hess P, Connolly L, Elliott CT (2009b) Development and single-laboratory validation of a pseudofunctional biosensor immunoassay for the detection of the Okadaic acid group of toxins. Anal Chem 81:10208–10214

  49. Touzet N, Franco JM, Raine R (2007) Influence of inorganic nutrition on growth and PSP toxin production of Alexandrium minutum (Dinophyceae) from Cork Harbour, Ireland. Toxicon 50:106–119

  50. Traynor I, Plumpton L, Fodey T, Higgins C, Elliott C (2006) Immunobiosensor detection of domoic acid as a screening test in bivalve molluscs: comparison with liquid chromatography-based analysis. J AOAC Int 89:868–872

  51. Turrell E, Bresnan E, Collins C, Brown L, Graham J, Grieve A (2008) Detection of Pseudo-nitzschia (Bacillariophyceae) species and amnesic shellfish toxins in Scottish coastal waters using oligonucleotide probes and the Jellet Rapid Test (TM). Harmful Algae 7:443–458

  52. Vale P, Veloso V, Amorim A (2009) Toxin composition of a Prorocentrum lima strain isolated from the Portuguese coast. Toxicon 54:145–152

  53. Van den Top HJ, Elliott CT, Haughey SA, Viarino N, van Egmond HP, Botana LM, Campbell K (2011) Surface plasmon resonance biosensor screening method for paralytic shellfish poisoning toxins: a pilot interlaboratory study. Anal Chem 83:4206–4213

  54. Wang D, Zhang S, Gu H, Chan LL, Hong H (2006) Paralytic shellfish toxin profiles, and toxin variability of the genus Alexandrium (Dinophyceae) isolated from the Southeast China Sea RID G-3412-2010 RID F-6943-2011 RID G-3347-2010. Toxicon 48:138–151

  55. Wang Z, King KL, Ramsdell JS, Doucette GJ (2007) Determination of domoic acid in seawater and phytoplankton by liquid chromatography-tandem mass spectrometry. J Chromatogr 1163:169–176

  56. Wiese M, D'Agostino PM, Mihali TK, Moffitt MC, Neilan BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Mar Drugs 8:2185–2211

  57. Yakes BJ, Prezioso S, Haughey SA, Campbell K, Elliott CT, DeGrasse SL (2011) An improved immunoassay for detection of saxitoxin by surface plasmon resonance biosensors. Sensors Actuators B-Chem 156:805–811

  58. Yu Q, Chen S, Taylor A, Homola J, Hock B, Jiang S (2005) Detection of low-molecular-weight domoic acid using surface plasmon resonance sensor. Sensors Actuators B-Chem 107:193–201

Download references

Acknowledgments

This research was funded by the European Commission as part of the FP7 European MIDTAL project, grant number 201724. We gratefully acknowledge all partners in the MIDTAL project and their contribution to this study. Linda Medlin and Jessica Kegel, (Marine Biological Association, Plymouth, UK), Marina Montresor and Lucia Barra, (Stazione Zoologica ‘A. Dohrn’ di Napoli, Naples, Italy), Edna Graneli, Johannes Hagstrom and Eva Perez, (Linnaeus University, Kalmar, Sweden), Beatriz Reguera and Francisco Rodriguez, (Instituto Espanol de Oceanografia, Vigo, Spain), Robin Raine and Gary McCoy, (Martin Ryan Institute, National University of Ireland, Galway, Ireland), Bente Edvardsen and Simon Dittami, (University of Oslo, Oslo, Norway), Jane Lewis and Joe Taylor, (University of Westminster, London, UK) and Yolanda Pazos (Technological Institute for the marine environment control of Galicia, Pontevedra, Spain) for collecting and providing seawater samples from around Europe .We also acknowledge those partners for providing algal cultures for cell lysis experiments, Francisco Rodriguez (Prorocentrum and Pseudo-nitizschia), Johannes Hagstrom and Eva Perez (Prorocentrum), Lucia Barra (Pseudo-nitizschia) and Amber Bratcher (University of Maine, USA) for providing Alexandrium cultures. We also acknowledge Jos Buijis (GE Healthcare Bio-Sciences, Uppsala, Sweden) for instrumentation support for the multiplex SPR biosensor.

Author information

Correspondence to Sara E. McNamee.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Cite this article

McNamee, S.E., Elliott, C.T., Delahaut, P. et al. Multiplex biotoxin surface plasmon resonance method for marine biotoxins in algal and seawater samples. Environ Sci Pollut Res 20, 6794–6807 (2013). https://doi.org/10.1007/s11356-012-1329-7

Download citation

Keywords

  • Biosensor
  • Surface plasmon resonance (SPR)
  • Biotoxins
  • Multiplexing
  • Paralytic shellfish poisoning (PSP) toxins
  • Okadaic acid
  • Domoic acid
  • Harmful algal bloom (HAB)