Aptamer-Based Biosensors to Detect Aquatic Phycotoxins and Cyanotoxins

Aptasensors have a great potential for environmental monitoring, particularly for real-time on-site detection of aquatic toxins produced by marine and freshwater microorganisms (cyanobacteria, dinoflagellates, and diatoms), with several advantages over other biosensors that are worth considering. Freshwater monitoring is of vital importance for public health, in numerous human activities, and animal welfare, since these toxins may cause fatal intoxications. Similarly, in marine waters, very effective monitoring programs have been put in place in many countries to detect when toxins exceed established regulatory levels and accordingly enforce shellfish harvesting closures. Recent advances in the fields of aptamer selection, nanomaterials and communication technologies, offer a vast array of possibilities to develop new imaginative strategies to create improved, ultrasensitive, reliable and real-time devices, featuring unique characteristics to produce and amplify the signal. So far, not many strategies have been used to detect aquatic toxins, mostly limited to the optic and electrochemical sensors, the majority applied to detect microcystin-LR using a target-induced switching mode. The limits of detection of these aptasensors have been decreasing from the nM to the fM order of magnitude in the past 20 years. Aspects related to sensor components, performance, aptamers sequences, matrices analyzed and future perspectives, are considered and discussed.

[1]  L. Botana,et al.  Determination of Gonyautoxin-4 in Echinoderms and Gastropod Matrices by Conversion to Neosaxitoxin Using 2-Mercaptoethanol and Post-Column Oxidation Liquid Chromatography with Fluorescence Detection , 2015, Toxins.

[2]  F. Auzel Upconversion and anti-Stokes processes with f and d ions in solids. , 2004, Chemical reviews.

[3]  Priscilla G. L. Baker,et al.  Electrochemical Aptatoxisensor Responses on Nanocomposites Containing Electro-Deposited Silver Nanoparticles on Poly(Propyleneimine) Dendrimer for the Detection of Microcystin-LR in Freshwater , 2016, Sensors.

[4]  V. Adam,et al.  G-Quadruplexes as Sensing Probes , 2013, Molecules.

[5]  Liling Hao,et al.  Graphene oxide-assisted non-immobilized SELEX of okdaic acid aptamer and the analytical application of aptasensor , 2016, Scientific Reports.

[6]  L. Gold,et al.  Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. , 1990, Science.

[7]  Mohammed Zourob,et al.  Selection, characterization, and biosensing application of high affinity congener-specific microcystin-targeting aptamers. , 2012, Environmental science & technology.

[8]  Marisa Silva,et al.  Bacterial diversity and tetrodotoxin analysis in the viscera of the gastropods from Portuguese coast. , 2016, Toxicon : official journal of the International Society on Toxinology.

[9]  Z. Yin,et al.  Synthesis of few-layer MoS2 nanosheet-coated TiO2 nanobelt heterostructures for enhanced photocatalytic activities. , 2013, Small.

[10]  M. Mascini,et al.  Electrochemical nucleic acid-based biosensors: Concepts, terms, and methodology (IUPAC Technical Report) , 2010 .

[11]  Guohua Zhao,et al.  A simple highly sensitive and selective aptamer-based colorimetric sensor for environmental toxins microcystin-LR in water samples. , 2016, Journal of hazardous materials.

[12]  Aldo Roda,et al.  Smartphone-based biosensors: A critical review and perspectives , 2016 .

[13]  V. Vasconcelos Global changes and the new challenges in the research on cyanotoxin risk evaluation , 2015 .

[14]  Chunhai Fan,et al.  Single-layer MoS2-based nanoprobes for homogeneous detection of biomolecules. , 2013, Journal of the American Chemical Society.

[15]  Makoto Shirai,et al.  Usage of a DNA Aptamer as a Ligand Targeting Microcystin , 2001 .

[16]  B. Hu,et al.  A saxitoxin-binding aptamer with higher affinity and inhibitory activity optimized by rational site-directed mutagenesis and truncation. , 2015, Toxicon : official journal of the International Society on Toxinology.

[17]  Zhouping Wang,et al.  Upconversion nanoparticles grafted molybdenum disulfide nanosheets platform for microcystin-LR sensing. , 2017, Biosensors & bioelectronics.

[18]  C. Bernard,et al.  Microcystins and Nodularins , 2017 .

[19]  J. Wengel,et al.  Improved thrombin binding aptamer by incorporation of a single unlocked nucleic acid monomer , 2010, Nucleic acids research.

[20]  David C. Szlag,et al.  A review of cyanobacteria and cyanotoxins removal/inactivation in drinking water treatment , 2010, Analytical and bioanalytical chemistry.

[21]  Nuo Duan,et al.  Simultaneous detection of microcysin-LR and okadaic acid using a dual fluorescence resonance energy transfer aptasensor , 2015, Analytical and Bioanalytical Chemistry.

[22]  D. Ramaiah,et al.  Efficient reaction based colorimetric probe for sensitive detection, quantification, and on-site analysis of nitrite ions in natural water resources. , 2013, Analytical chemistry.

[23]  Yu-Chung Chang,et al.  A multichannel smartphone optical biosensor for high-throughput point-of-care diagnostics. , 2017, Biosensors & bioelectronics.

[24]  C. Tuerk,et al.  SELEXION. Systematic evolution of ligands by exponential enrichment with integrated optimization by non-linear analysis. , 1991, Journal of molecular biology.

[25]  T. Smayda Reflections on the ballast water dispersal- : harmful algal bloom paradigm , 2007 .

[26]  M. Twiner,et al.  Extraction and analysis of lipophilic brevetoxins from the red tide dinoflagellate Karenia brevis. , 2007, Analytical biochemistry.

[27]  Mohamed Siaj,et al.  In vitro selection, characterization, and biosensing application of high-affinity cylindrospermopsin-targeting aptamers. , 2014, Analytical chemistry.

[28]  L. Botana,et al.  New Invertebrate Vectors for PST, Spirolides and Okadaic Acid in the North Atlantic , 2013, Marine drugs.

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

[30]  Guohua Zhao,et al.  Photoelectrochemical Aptasensor for the Sensitive Detection of Microcystin-LR Based on Graphene Functionalized Vertically-aligned TiO2 Nanotubes , 2016 .

[31]  J. Froines,et al.  UNITED STATES ENVIRONMENTAL PROTECTION AGENCY , 1995 .

[32]  Xing Chen,et al.  Nanomaterial-Assisted Signal Enhancement of Hybridization for DNA Biosensors: A Review , 2009, Sensors.

[33]  Youyu Zhang,et al.  Sensitive electrochemical aptamer biosensor for dynamic cell surface N-glycan evaluation featuring multivalent recognition and signal amplification on a dendrimer-graphene electrode interface. , 2014, Analytical chemistry.

[34]  Dudley H. Williams,et al.  Structural studies on cyanoginosins-LR, -YR, -YA, and -YM, peptide toxins from Microcystis aeruginosa , 1985 .

[35]  L. Botana,et al.  Emergent Toxins in North Atlantic Temperate Waters: A Challenge for Monitoring Programs and Legislation , 2015, Toxins.

[36]  S. Gopinath,et al.  Aptamers as a replacement for antibodies in enzyme-linked immunosorbent assay. , 2015, Biosensors & bioelectronics.

[37]  He Li,et al.  Colorimetric detection of microcystin-LR based on disassembly of orient-aggregated gold nanoparticle dimers. , 2015, Biosensors & bioelectronics.

[38]  A. Humpage,et al.  Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male Swiss albino mice: Determination of no observed adverse effect level for deriving a drinking water guideline value , 2003, Environmental toxicology.

[39]  R. Mitchell,et al.  The toxicity of cyanobacterial toxins in the mouse: II Anatoxin-a , 1999, Human & experimental toxicology.

[40]  A. Radenović,et al.  Single-layer MoS2 transistors. , 2011, Nature nanotechnology.

[41]  L. Dai,et al.  Fabricating photoelectrochemical aptasensor for selectively monitoring microcystin-LR residues in fish based on visible light-responsive BiOBr nanoflakes/N-doped graphene photoelectrode. , 2016, Biosensors & bioelectronics.

[42]  Man Bock Gu,et al.  Immobilization-free screening of aptamers assisted by graphene oxide. , 2012, Chemical communications.

[43]  Koichi Abe,et al.  Affinity improvement of a VEGF aptamer by in silico maturation for a sensitive VEGF-detection system. , 2013, Analytical chemistry.

[44]  B. D. Chandler,et al.  Nanocomposite catalysts: Dendrimer encapsulated nanoparticles immobilized in sol–gel silica , 2005 .

[45]  Anna Zhu,et al.  Recent Advances in Optical Biosensors for Environmental Monitoring and Early Warning , 2013, Sensors.

[46]  Danfeng Yao,et al.  Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization. , 2009, Combinatorial chemistry & high throughput screening.

[47]  Tao Yang,et al.  A label-free ultrasensitive electrochemical DNA sensor based on thin-layer MoS2 nanosheets with high electrochemical activity. , 2015, Biosensors & bioelectronics.

[48]  A. Hirao,et al.  Dendrimer-like star-branched polymers: novel structurally well-defined hyperbranched polymers , 2011 .

[49]  R. Stoltenburg,et al.  SELEX--a (r)evolutionary method to generate high-affinity nucleic acid ligands. , 2007, Biomolecular engineering.

[50]  Lianghua Wang,et al.  Enzyme-linked, aptamer-based, competitive biolayer interferometry biosensor for palytoxin. , 2017, Biosensors & bioelectronics.

[51]  K. James,et al.  Hepatotoxins: Context and Chemical Determination , 2008 .

[52]  C. O. O' Sullivan,et al.  Facile and Cost-Effective Detection of Saxitoxin Exploiting Aptamer Structural Switching. , 2015, Food technology and biotechnology.

[53]  Y. Niu,et al.  Improving the stability of aptamers by chemical modification. , 2011, Current medicinal chemistry.

[54]  Teresa A. P. Rocha-Santos,et al.  Recent Progress in Biosensors for Environmental Monitoring: A Review , 2017, Sensors.

[55]  Grant C. Pitcher,et al.  Non-Traditional Vectors for Paralytic Shellfish Poisoning , 2008, Marine drugs.

[56]  Christine Edwards,et al.  Rapid detection of microcystins in cells and water. , 2010, Toxicon : official journal of the International Society on Toxinology.

[57]  M. Zourob,et al.  Selection and identification of DNA aptamers against okadaic acid for biosensing application. , 2013, Analytical chemistry.

[58]  Q. Zhang,et al.  Multiplexed fluorescence resonance energy transfer aptasensor between upconversion nanoparticles and graphene oxide for the simultaneous determination of mycotoxins. , 2012, Analytical chemistry.

[59]  Hongyu Wang,et al.  X-Aptamer Selection and Validation. , 2017, Methods in molecular biology.

[60]  Xiong Zhang,et al.  Recent Progress in Optical Biosensors Based on Smartphone Platforms , 2017, Sensors.

[61]  Hua Zhang,et al.  Single-layer MoS2 phototransistors. , 2012, ACS nano.

[62]  A. Antunes,et al.  Phylogeny and Biogeography of Cyanobacteria and Their Produced Toxins , 2013, Marine drugs.

[63]  G. S. Wilson,et al.  Electrochemical Biosensors: Recommended Definitions and Classification , 1999, Biosensors & bioelectronics.

[64]  Qingjun Liu,et al.  Biosensors and bioelectronics on smartphone for portable biochemical detection. , 2016, Biosensors & bioelectronics.

[65]  Zhen Zhao,et al.  A label-free electrochemical impedance aptasensor for cylindrospermopsin detection based on thionine-graphene nanocomposites. , 2015, The Analyst.

[66]  J. Burkholder,et al.  Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences , 2002 .

[67]  Kun Han,et al.  Design Strategies for Aptamer-Based Biosensors , 2010, Italian National Conference on Sensors.

[68]  John J. Perona,et al.  Tertiary core rearrangements in a tight binding transfer RNA aptamer , 2000, Nature Structural Biology.

[69]  Qixing Zhou,et al.  Immobilized smart RNA on graphene oxide nanosheets to specifically recognize and adsorb trace peptide toxins in drinking water. , 2012, Journal of hazardous materials.

[70]  Lianghua Wang,et al.  Gonyautoxin 1/4 aptamers with high-affinity and high-specificity: From efficient selection to aptasensor application. , 2016, Biosensors & bioelectronics.

[71]  Uda Hashim,et al.  Advances in biosensors: Principle, architecture and applications ☆ , 2014 .

[72]  Hua-Zhong Yu,et al.  Design and testing of aptamer-based electrochemical biosensors for proteins and small molecules. , 2009, Bioelectrochemistry.

[73]  Y. Chai,et al.  Dendrimer functionalized reduced graphene oxide as nanocarrier for sensitive pseudobienzyme electrochemical aptasensor. , 2013, Biosensors & bioelectronics.

[74]  S. Nie,et al.  Quantum dot bioconjugates for ultrasensitive nonisotopic detection. , 1998, Science.

[75]  Mohamed Siaj,et al.  DNA aptamers selection and characterization for development of label-free impedimetric aptasensor for neurotoxin anatoxin-a. , 2015, Biosensors & bioelectronics.

[76]  J. Švitel,et al.  Optical biosensors , 2016, Essays in biochemistry.

[77]  Xi Chen,et al.  Determination of microcystin-LR in water by a label-free aptamer based electrochemical impedance biosensor. , 2013, Talanta.

[78]  D. Balding,et al.  HLA Sequence Polymorphism and the Origin of Humans , 2006 .

[79]  Genxi Li,et al.  Effect of Silver Nanoparticles on the Electron Transfer Reactivity and the Catalytic Activity of Myoglobin , 2004, Chembiochem : a European journal of chemical biology.

[80]  Cyanobacterial toxins: Microcystin-LR in Drinking-water Background document for development of WHO Guidelines for Drinking-water Quality , 2003 .

[81]  L. Dai,et al.  Building a Three-Dimensional Nano-Bio Interface for Aptasensing: An Analytical Methodology Based on Steric Hindrance Initiated Signal Amplification Effect. , 2016, Analytical chemistry.

[82]  Jun Wang,et al.  Label-free okadaic acid detection using growth of gold nanoparticles in sensor gaps as a conductive tag , 2017, Biomedical microdevices.

[83]  Zeng-Shan Liu,et al.  Preparation of a Specific ssDNA Aptamer for Brevetoxin-2 Using SELEX , 2016, Journal of analytical methods in chemistry.

[84]  Ming Zhou,et al.  A homogeneous signal-on strategy for the detection of rpoB genes of Mycobacterium tuberculosis based on electrochemiluminescent graphene oxide and ferrocene quenching. , 2014, Analytical chemistry.

[85]  Katrina Campbell,et al.  First report of the use of a saxitoxin-protein conjugate to develop a DNA aptamer to a small molecule toxin. , 2013, Toxicon : official journal of the International Society on Toxinology.

[86]  Mohamed Siaj,et al.  Label-free voltammetric aptasensor for the sensitive detection of microcystin-LR using graphene-modified electrodes. , 2014, Analytical chemistry.

[87]  A. Furey,et al.  Assessment of emerging biotoxins (pinnatoxin G and spirolides) at Europe's first marine reserve: Lough Hyne. , 2015, Toxicon : official journal of the International Society on Toxinology.

[88]  L. Botana,et al.  New Gastropod Vectors and Tetrodotoxin Potential Expansion in Temperate Waters of the Atlantic Ocean , 2012, Marine drugs.

[89]  E. Garcés,et al.  Harmful microalgae blooms (HAB); problematic and conditions that induce them. , 2006, Marine pollution bulletin.

[90]  Priscilla G. L. Baker,et al.  Aptameric Recognition-Modulated Electroactivity of Poly(4-Styrenesolfonic Acid)-Doped Polyaniline Films for Single-Shot Detection of Tetrodotoxin , 2015, Sensors.

[91]  J. Szostak,et al.  In vitro selection of RNA molecules that bind specific ligands , 1990, Nature.

[92]  L. Botana,et al.  New Invertebrate Vectors of Okadaic Acid from the North Atlantic Waters—Portugal (Azores and Madeira) and Morocco , 2015, Toxins.

[93]  D. Volmer,et al.  Intriguing Differences in the Gas-Phase Dissociation Behavior of Protonated and Deprotonated Gonyautoxin Epimers , 2011, Journal of the American Society for Mass Spectrometry.

[94]  S. M. Taghdisi,et al.  A novel fluorescent aptasensor for ultrasensitive detection of microcystin-LR based on single-walled carbon nanotubes and dapoxyl. , 2017, Talanta.

[95]  Rijun Gui,et al.  Facilely self-assembled magnetic nanoparticles/aptamer/carbon dots nanocomposites for highly sensitive up-conversion fluorescence turn-on detection of tetrodotoxin. , 2018, Talanta.

[96]  Qiyi Lu,et al.  A signal-on electrochemiluminescence biosensor for detecting Con A using phenoxy dextran-graphite-like carbon nitride as signal probe. , 2015, Biosensors & bioelectronics.

[97]  T. Sampson,et al.  Aptamers and SELEX: the technology , 2003 .

[98]  Guangming Wang,et al.  Selection and identification of a DNA aptamer that mimics saxitoxin in antibody binding. , 2013, Journal of agricultural and food chemistry.

[99]  Elena Korotkaya,et al.  Biosensors: design, classification, and applications in the food industry , 2014 .

[100]  Mohamed Siaj,et al.  Aptamer-based competitive electrochemical biosensor for brevetoxin-2. , 2015, Biosensors & bioelectronics.

[101]  Yanfen Fang,et al.  Unique ability of BiOBr to decarboxylate d-Glu and d-MeAsp in the photocatalytic degradation of microcystin-LR in water. , 2011, Environmental science & technology.