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Recombinase-aided amplification combined with lateral flow dipstick for the rapid detection of Amphidinium carterae

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Abstract

In the context of global climate change, the frequency and duration of harmful algal blooms (HABs) due to eutrophic coastal waters have increased. HABs can cause marine ecological imbalance, massive socio-economic damage, and potential public health problems. Therefore, accurate and specific techniques that can rapidly detect harmful algae are critical to expedite early monitoring and prediction of HABs. Although some methods based on amplification have previously been described, limitations associated with limited popularity and high costs still exist. In this study, the partial sequence of nuclear ribosomal DNA from Amphinidium carterae was selected as the target region. The biotin-labeled recombinase-aided amplification (RAA) products and the 6-carboxyfluorescein-labeled probe were specifically conjugated, which formed double-labeled RAA products analyzed by lateral flow dipstick (LFD). A rapid RAA–LFD assay aimed at visually detecting A. carterae was established and optimized. The specificity and sensitivity of RAA–LFD were determined. The nucleic acid test with other control algal species yielded negative results, which indicated that RAA–LFD assay can specifically detect A. carterae. The detection limit of RAA–LFD assay for A. carterae was 8.49 ng μL−1 genomic DNA and 1 cell mL−1. The whole detection process of RAA–LFD could be completed within 50 min. In conclusion, the proposed RAA–LFD assay may be promising for the efficient, specific, and rapid detection of A. carterae in monitoring efforts.

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References

  • Abreu AC, Molina-Miras A, Aguilera-Sáez LM, López-Rosales L, Cerón-García MC, Sánchez-Mirón A, Olmo-García L, Carrasco-Pancorbo A, García-Camacho F, Molina-Grima E, Fernández I (2019) Production of amphidinols and other bioproducts of interest by the marine microalga Amphidinium carterae unraveled by nuclear magnetic resonance metabolomics approach coupled to multivariate data analysis. J Agric Food Chem 67:9667–9682

    Article  CAS  PubMed  Google Scholar 

  • Accoroni S, Totti C, Romagnoli T, Giulietti S, Glibert PM (2020) Distribution and potential toxicity of benthic harmful dinoflagellates in waters of Florida Bay and the Florida Keys. Mar Environ Res 155:104891

    Article  CAS  PubMed  Google Scholar 

  • Ahmed N, Al-Madhagi S, Ortiz M, O'Sullivan CK, Katakis I (2020) Direct electrochemical detection of enzyme labelled, isothermally amplified DNA. Anal Biochem 598:113705

    Article  CAS  PubMed  Google Scholar 

  • Bai J, Lin HS, Li HJ, Zhou Y, Liu JS, Zhong GR, Wu LT, Jiang WF, Du HL, Yang JY, Xie QM, Huang LZ (2019) Cas12a-based on-site and rapid nucleic acid detection of African swine fever. Front Microbiol 10:2830

    Article  PubMed  PubMed Central  Google Scholar 

  • Baig HS, Saifullah SM, Dar A (2006) Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae 5:133–140

    Article  CAS  Google Scholar 

  • Boisnoir A, Pavaux AS, Schizas NV, Marro S, Blasco T, Lemée R, Pascal PY (2020) The use of stable isotopes to measure the ingestion rate of potentially toxic benthic dinoflagellates by harpacticoid copepods. J Exp Mar Biol Ecol 524:151285

    Article  Google Scholar 

  • Chai YM, Deng WJ, Qin X, Xu XR (2017) Occurrence of four species of algae in the marine water of Hong Kong. Mar Pollut Bull 124:890–896

    Article  CAS  PubMed  Google Scholar 

  • Chen ZC, Yang HJ, Pavletich PN (2008) Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures. Nature 453:489–494

    Article  CAS  PubMed  Google Scholar 

  • Chen GF, Ma CS, Zhang CY, Zhou J, Wang YY, Wang GC, Zhang BY, Xu Z, Lu DD (2013) A rapid and sensitive method for field detection of Prorocentrum donghaiense using reverse transcription-coupled loop-mediated isothermal amplification. Harmful Algae 29:31–39

    Article  CAS  Google Scholar 

  • Chen GF, Cai PP, Zhang CY, Wang YY, Zhang SB, Guo CL, Lu DD (2015) Hyperbranched rolling circle amplification as a novel method for rapid and sensitive detection of Amphidinium carterae. Harmful Algae 47:66–74

    Article  CAS  Google Scholar 

  • Cheng KH, Chan SN, Lee JHW (2020) Remote sensing of coastal algal blooms using unmanned aerial vehicles (UAVs). Mar Pollut Bull 152:110889

    Article  CAS  PubMed  Google Scholar 

  • Doucette GJ, Mikulski CM, Jones KL, King KL, Greenfield DI, Marin R-III, Jensen S, Roman B, Elliott CRT, Scholin CA (2009) Remote, subsurface detection of the algal toxin domoic acid onboard the environmental sample processor: assay development and field trials. Harmful Algae 8:880–888

    Article  CAS  Google Scholar 

  • Echigoya R, Rhodes L, Oshima Y, Satake M (2005) The structures of five new antifungal and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand. Harmful Algae 4:383–389

    Article  CAS  Google Scholar 

  • Engesmo A, Strand D, Gran-Stadniczeñko S, Edvardsen B, Medlin LK, Eikrem W (2018) Development of a qPCR assay to detect and quantify ichthyotoxic flagellates along the Norwegian coast, and the first Norwegian record of Fibrocapsa japonica (Raphidophyceae). Harmful Algae 75:105–117

    Article  CAS  PubMed  Google Scholar 

  • Fu MQ, Chen GF, Zhang CY, Wang YY, Sun R, Zhou J (2019a) Rapid and sensitive detection method for Karlodinium veneficum by recombinase polymerase amplification coupled with lateral flow dipstick. Harmful Algae 84:1–9

    Article  CAS  PubMed  Google Scholar 

  • Fu YH, Sun WL, Huang ZJ, Cheng Q (2019b) Preparation of Klenow (exo-) Protein and its preliminary application in RAA detection system. Curr Biotechnol 9:409–415 (in Chinese)

    Google Scholar 

  • Gárate-Lizárraga I, González-Armas R, Verdugo-Díaz G, Okolodkov YB, Pérez-Cruz B, Díaz Ortíz JA (2019) Seasonality of the dinoflagellate Amphidinium cf. carterae (Dinophyceae: Amphidiniales) in Bahía de la Paz, Gulf of California. Mar Pollut Bull 146:532–541

    Article  PubMed  Google Scholar 

  • Glibert PM (2020) Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae 91:101583

    Article  PubMed  Google Scholar 

  • Gobler CJ (2020) Climate change and harmful algal blooms: insights and perspective. Harmful Algae 91:101731

    Article  PubMed  Google Scholar 

  • Gokul EA, Shanmugam P (2016) An optical system for detecting and describing major algal blooms in coastal and oceanic waters around India. J Geophys Res 121:4097–4127

    Article  Google Scholar 

  • Goodwin KD, Cotton SA, Scorzetti G, Fell JW (2005) A DNA hybridization assay to identify toxic dinoflagellates in coastal waters: detection of Karenia brevis in the Rookery Bay National Estuarine Research Reserve. Harmful Algae 4:411–422

    Article  CAS  Google Scholar 

  • Griffith AW, Goblera CJ (2020) Harmful algal blooms: a climate change co-stressor in marine and freshwater ecosystems. Harmful Algae 91:101590

    Article  PubMed  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates, In: Smith, W.L, Chanley, M.H. (Ed.), Culture of Marine Invertebrate Animals. Plenum Press, New York, pp. 29–60

  • Hattenrath-Lehmann TK, Zhen Y, Wallace RB, Tang YZ, Gobler CJ (2016) Mapping the distribution of cysts from the toxic dinoflagellate Cochlodinium polykrikoides in bloom-prone estuaries by a novel fluorescence in situ hybridization assay. Appl Environ Microbiol 82:1114–1125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosoi-Tanabe S, Sako Y (2005) Rapid detection of natural cells of Alexandrium tamarense and A. catenella (Dinophyceae) by fluorescence in situ hybridization. Harmful Algae 4:319–328

    Article  Google Scholar 

  • Huang HL, Zhu P, Zhou CX, He S, Yan XJ (2017) The development of loop-mediated isothermal amplification combined with lateral flow dipstick for detection of Karlodinium veneficum. Harmful Algae 62:20–29

    Article  CAS  PubMed  Google Scholar 

  • Ismael AAH, Halim Y, Khalil AG (1999) Optimum growth conditions for Amphidinium carterae Hulburt from eutrophic waters in Alexandria (Egypt) and its toxicity to the brine shrimp Artemia salina. Grana 38:179–185

    Article  Google Scholar 

  • Karthik K, Rathore R, Thomas P, Arun TR, Viswas KN, Dhama K, Agarwal RK (2014) New closed tube loop mediated isothermal amplification assay for prevention of product cross-contamination. Methods X 1:137–143

    CAS  Google Scholar 

  • Kim JH, Kim H, Kang D, Lim YK, Ajani P, Jung SW, Baek SH (2019) Field application and validity of a red-tide acoustic sensing system (RASS) for monitoring and alerting of harmful algal blooms (HABs) in Korean coastal waters. J Appl Phycol 31:3737–3748

    Article  Google Scholar 

  • Kong XY, Han XR, Gao M, Su RG, Wang K, Li XZ, Lu W (2016) Antialgal and antilarval activities of bioactive compounds extracted from the marine dinoflagellate Amphidinium carterae. J Ocean Univ China 15:1014–1020

    Article  CAS  Google Scholar 

  • Lauritano C, Luca DD, Ferrarini A, Avanzato C, Minio A, Esposito F, Ianora A (2017) De novo transcriptome of the cosmopolitan dinoflagellate Amphidinium carterae to identify enzymes with biotechnological potential. Sci Rep 7:11701

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee JJ, Shpigel M, Freeman S, Zmora O, Mcleod S, Bowen S, Pearson M, Szostek A (2003) Physiological ecology and possible control strategy of a toxic marine dinoflagellate, Amphidinium sp., from the benthos of a mariculture pond. Aquaculture 217:351–371

    Article  Google Scholar 

  • Lee HG, Kim HM, Min J, Park C, Jeong HJ, Lee K, Kim KY (2020) Quantification of the paralytic shellfish poisoning dinoflagellate Alexandrium species using a digital PCR. Harmful Algae 92:101726

    Article  CAS  PubMed  Google Scholar 

  • Li T, Yang K (2019) Application of isothermal amplification technology for pathogen detection in parasitic and other diseases. Chin J Schisto Control 30:232–236 (in Chinese)

    Google Scholar 

  • Li MZ, Shi XG, Guo CT, Lin SJ (2016) Phosphorus deficiency inhibits cell division but not growth in the dinoflagellate Amphidinium carterae. Front Microbiol 7:826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li JJ, Wang CM, Yu X, Lin HR, Hui C, Shuai L, Zhang SH (2019a) Rapid detection of Cyanobacteria by recombinase polymerase amplification combined with lateral flow strips. Water Supply 19:1181–1186

    Article  Google Scholar 

  • Li XN, Shen XX, Li MH, Qi JJ, Wang RH, Duan QX, Zhang RQ, Fan T, Bai XD, Fan GH, Xie Y, Ma XJ (2019b) Applicability of duplex real time and lateral flow strip reverse-transcription recombinase aided amplification assays for the detection of Enterovirus 71 and Coxsackievirus A16. Virol J 16:1–10

    Article  Google Scholar 

  • López-Rodríguez M, Cerón-García MC, López-Rosales L, González-López CV, Molina-Miras A, Ramírez-González A, Sánchez-Mirón A, García-Camacho F, Molina-Grima E (2019) Assessment of multi-step processes for an integral use of the biomass of the marine microalga Amphidinium carterae. Bioresour Technol 282:370–377

    Article  PubMed  Google Scholar 

  • Loukas CM, McQuillan JS, Laouenan F, Tsaloglou MN, Ruano-Lopez JM, Mowlem MC (2017) Detection and quantification of the toxic microalgae Karenia brevis using lab on a chip mRNA sequence-based amplification. J Microbiol Methods 139:189–195

    Article  CAS  PubMed  Google Scholar 

  • Lü B, Cheng HR, Yan QF (2010) Recombinase-aid amplification: a novel technology of in vitro rapid nucleic acid amplification. Scientia Sinica Vitae 40:983–988 (in Chinese)

    Google Scholar 

  • Lü B, Cheng HR, Shen GF, Yan QF, Zhang ZF, Huang ZJ, Deng ZX, Lin M, Li YN, Luo D, Cheng Q (2011) The development and recent improvements of in vitro nucleic acid amplification technology. Chin Biotechnol 31:91–96 (in Chinese)

    Google Scholar 

  • Martinez KA, Lauritano C, Druka D, Romano G, Grohmann T, Jaspars M, Martin J, Diaz C, Cautain B, de la Cruz M, Ianora A, Reyes F (2019) Amphidinol 22, a new cytotoxic and antifungal amphidinol from the dinoflagellate Amphidinium carterae. Mar Drugs 17:385

    Article  CAS  PubMed Central  Google Scholar 

  • Meng YH, Van Wagoner RM, Misner I, Tomas C, Wright JLC (2010) Structure and biosynthesis of amphidinol 17, a hemolytic compound from Amphidinium carterae. J Nat Prod 73:409–415

    Article  CAS  PubMed  Google Scholar 

  • Miao L, Zhang XP, Wang JC, Wang YL, Cheng Q, Xu C, Zhang L (2019) Establishment and application of real-time recombinase-aided amplification assay to detect chicken-derived ingredients in meat products. Jiangsu J Agr Sci 35:954–959 (in Chinese)

    Google Scholar 

  • Molina-Miras A, López-Rosales L, Cerón-García MC, Sánchez-Mirón A, Olivera-Gálvez A, García-Camacho F, Molina-Grima E (2020) Acclimation of the microalga Amphidinium carterae to different nitrogen sources: potential application in the treatment of marine aquaculture effluents. J Appl Phycol 32:1075–1094

    Article  CAS  Google Scholar 

  • Mulholland MR, Morse R, Egerton T, Bernhardt PW, Filippino KC (2018) Blooms of dinoflagellate mixotrophs in a lower chesapeake bay tributary: carbon and nitrogen uptake over diurnal, seasonal, and interannual timescales. Estuar Coasts 41:1744–1765

    Article  CAS  Google Scholar 

  • Murray SA, Kohli GS, Farrell H, Spiers ZB, Place AR, Dorantes-Aranda JJ, Ruszczyk J (2015) A fish kill associated with a bloom of Amphidinium carterae in a coastal lagoon in Sydney, Australia. Harmful Algae 49:19–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakajima I, Oshima Y, Yasumoto T (1981) Toxicity of benthic dinoflagellates in Okinawa. Bull Jpn Soc Sci Fish 47:1029–1033

    Article  Google Scholar 

  • Nayak BB, Karunasagar I, Karunasagar I (1997) Influence of bacteria on growth and hemolysis production by the marine dinoflagellate Amphidinium carterae. Mar Biol 130:35–39

    Article  CAS  Google Scholar 

  • Ni BX, Wu XM, Liu YH, Xu XZ, Ying QJ, Cao J, Dai Y (2019) Establishment and evaluation of the detection method of Cryptosporidium specific DNA fragment by recombinase aided isothermal amplification. Chin J Schisto Control 31:388–392 (in Chinese)

    Google Scholar 

  • Nie XL, Zhang CY, Wang YY, Guo CL, Zhou J, Chen GF (2017) Application of hyper-branched rolling circle amplification (HRCA) and HRCA-based strip test for the detection of Chattonella marina. Environ Sci Pollut Res 24:15678–15688

    Article  CAS  Google Scholar 

  • Olson RJ, Sosik HM (2007) A submersible imaging-in-flow instrument to analyze nano-and microplankton: Imaging FlowCytobot. Limnol Oceanogr Methods 5:195–203

    Article  Google Scholar 

  • Pagliara P, Caroppo C (2012) Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon 60:1203–1214

    Article  CAS  PubMed  Google Scholar 

  • Prabowo DA, Agusti S (2019) Free-living dinoflagellates of the central Red Sea, Saudi Arabia: variability, new records and potentially harmful species. Mar Pollut Bull 141:629–648

    Article  CAS  PubMed  Google Scholar 

  • Qi JJ, Li XN, Zhang Y, Shen XX, Song GW, Pan J, Fan T, Wang RH, Li LX, Ma XJ (2019) Development of a duplex reverse transcription recombinase-aided amplification assay for respiratory syncytial virus incorporating an internal control. Arch Virol 164:1843–1850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin Y, Chen GF, Zhang CY, Wang YY, Zhou J (2019) Development of loop-mediated isothermal amplification combined with a chromatographic lateral-flow dipstick for rapid detection of Chattonella marina. Harmful Algae 89:101666

    Article  CAS  PubMed  Google Scholar 

  • Scholin CA, Herzog M, Sogin M, Anderson DM (1994) Identification of groupand strainspecific genetic markers for globally distributed Alexandrium (Dinophyceae). II. sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30:999–1011

    Article  CAS  Google Scholar 

  • Seto DS, Karp-Boss L, Wells ML (2019) Effects of increasing temperature and acidification on the growth and competitive success of Alexandrium catenella from the Gulf of Maine. Harmful Algae:101670

  • SOA (2005) HY/T069-2005 Thechnical specification for red tide minitoring. Standards Press of China, Beijing (in Chinese)

    Google Scholar 

  • Sun YJ, Chen GF, Zhang CY, Guo CL, Wang YY, Sun R (2019) Development of a multiplex polymerase chain reaction assay for the parallel detection of harmful algal bloom-forming species distributed along the Chinese coast. Harmful Algae 84:36–45

    Article  CAS  PubMed  Google Scholar 

  • Tang HJ, Dang ZH, Guo CN, Wang XJ, Miao XX, Guo BS, Xu C (2019) Rapid detection for Dysmicoccus neobrevipes by recombinase-aided amplification. Plant Quarantine 33:37–42 (in Chinese)

    Google Scholar 

  • Toldrà A, Jauset-Rubio M, Andree KB, Fernández-Tejedor M, Diogène J, Katakis I, O’Sullivan CK, Campas M (2018) Detection and quantification of the toxic marine microalgae Karlodinium veneficum and Karlodinium armiger using recombinase polymerase amplification and enzyme-linked oligonucleotide assay. Anal Chim Acta 1039:140–148

    Article  PubMed  Google Scholar 

  • Toldrà A, Alcaraz C, Andree KB, Fernández-Tejedor M, Diogène J, Katakis I, O’Sullivan CK, Campàs M (2019a) Colorimetric DNA-based assay for the specific detection and quantification of Ostreopsis cf. ovata and Ostreopsis cf. siamensis in the marine environment. Harmful Algae 84:27–35

    Article  PubMed  Google Scholar 

  • Toldrà A, O'Sullivan CK, Campàs M (2019b) Detecting harmful algal blooms with isothermal molecular strategies. Trends Biotechnol 37:1278–1281

    Article  PubMed  Google Scholar 

  • Wang L, Chen GF, Zhang CY, Wang YY, Sun R (2019a) Rapid and sensitive detection of Amphidinium carterae by loop-mediated isothermal amplification combined with a chromatographic lateral-flow dipstick. Mol Cell Probes 43:72–79

    Article  CAS  PubMed  Google Scholar 

  • Wang QY, Li F, Shen XX, Fu SH, He Y, Lei WW, Liang GD, Wang HY, Ma XJ (2019b) A reverse-transcription recombinase-aided amplification assay for the rapid detection of the Far-Eastern subtype of tick-borne encephalitis virus. Biomed Environ Sci 32:357–362

    PubMed  Google Scholar 

  • Wang RH, Zhang H, Zhang Y, Li XN, Shen XX, Qi JJ, Fan GH, Xiang XY, Zhan ZF, Chen ZW, Ma XJ (2019c) Development and evaluation of recombinase-aided amplification assays incorporating competitive internal controls for detection of human adenovirus serotypes 3 and 7. Virol J 16:1–9

    Article  Google Scholar 

  • Wang H, Hu ZX, Shang LX, Leaw CP, Lim PT, Tang YZ (2020a) Toxicity comparison among four strains of Margalefidinium polykrikoides from China, Malaysia, and USA (belonging to two ribotypes) and possible implications. J Exp Mar Biol Ecol 524:151293

    Article  Google Scholar 

  • Wang WJ, Wang CG, Zhang P, Yao SS, Liu JR, Zhai XH, Zhang T (2020b) Reverse transcription recombinase-aided amplification assay combined with a lateral flow dipstick for detection of avian infectious bronchitis virus. Poult Sci 99:89–94

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cui YQ, Yu ZR, Li YQ, Bai CX, Sun P, Zhu W, Li YD (2020c) Development of a recombinase-aided amplification assay for detection of orf virus. J Virol Methods 280:113861

    Article  CAS  PubMed  Google Scholar 

  • Zhang CY, Chen GF, Ma CS, Wang YY, Zhang BY, Wang GC (2014) Parallel detection of harmful algae using reverse transcription polymerase chain reaction labeling coupled with membrane-based DNA array. Environ Sci Pollut Res 21:4565–4575

    Article  CAS  Google Scholar 

  • Zhang CY, Chen GF, Wang YY, Sun R, Nie XL, Zhou J (2018) MHBMDAA: membrane-based DNA array with high resolution and sensitivity for toxic microalgae monitoring. Harmful Algae 80:107–116

    Article  CAS  PubMed  Google Scholar 

  • Zhang CY, Chen GF, Wang YY, Zhou J, Li CH (2019a) Establishment and application of hyperbranched rolling circle amplification coupled with lateral flow dipstick for the sensitive detection of Karenia mikimotoi. Harmful Algae 84:151–160

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Ding X, Wu XM, Liu YH, Liu JF, Xu XZ, Ying QJ, Ca J, Dai Y (2019b) Establishment and preliminary evaluation of recombinase aided isothermal amplification (RAA) assay for specific nucleic acid detection of Clonorchis sinensis. Chin J Schisto Control 31:468–473 (in Chinese)

    CAS  Google Scholar 

  • Zhen Y, Mi TZ, Yu ZG (2009) Detection of several harmful algal species by sandwich hybridization integrated with a nuclease protection assay. Harmful Algae 8:651–657

    Article  CAS  Google Scholar 

  • Zimmermann LA (2006) Environmental regulation of toxin production, comparison of hemolytic activity of Amphidinium carterae and Amphidinium klebsii. MSc Thesis, University of North Carolina, Wilmington

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Funding

This work was supported by Shandong Provincial Natural Science Foundation, China (ZR2020MD081); the National Scientific Foundation of China (No. 31600309, 41476086); HIT Scientific Research Innovation Fund/the Fundamental Research Funds for the Central Universities (No. HIT.NSRIF.201702 and HIT.NSRIF.201709); and HIT Environment and Ecology Innovation Special Funds (No. HSCJ201622).

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Xu, M., Zhang, C., Liu, F. et al. Recombinase-aided amplification combined with lateral flow dipstick for the rapid detection of Amphidinium carterae. J Appl Phycol 34, 435–447 (2022). https://doi.org/10.1007/s10811-021-02655-1

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