Development and evaluation of a DNA microarray assay for the simultaneous detection of nine harmful algal species in ship ballast and seaport waters
Tóm tắt
Rapid, high-throughput and reliable methods are urgently required to accurately detect and monitor harmful algae, which are responsible for algal blooms, such as red and green tides. In this study, we successfully developed a multiplex PCR-based DNA microarray method capable of detecting nine harmful algal species simultaneously, namely Alexandrium tamarense, Gyrodinium instriatum, Heterosigma akashiwo, Karenia mikimotoi, Prorocentrum donghaiense, Prorocentrum minimum, Ulva compressa, Ulva ohnoi and Ulva prolifera. This method achieved a limit of detection (LOD) of 0.5 ng of genomic DNA (orders of magnitude of the deci-nanogram range) in the tested algae cultures. Altogether, 230 field samples from ship ballast waters and seaport waters were used to evaluate the DNA microarray. The clinical sensitivity and specificity of the DNA microarray assay in detecting field samples were 96.4% and 90.9%, respectively, relative to conventional morphological methods. This indicated that this high-throughput, automatic, and specific method is well suited for the detection of algae in water samples.
Tài liệu tham khảo
citation_journal_title=Applied and Environmental Microbiology; citation_title=Fiber-optic microarray for simultaneous detection of multiple harmful algal bloom species; citation_author=S Ahn, D Kulis, D L Erdner, D M Anderson, D R Walt; citation_volume=72; citation_issue=9; citation_publication_date=2006; citation_pages=5 742-5 749; citation_doi=10.1128/AEM.00332-06; citation_id=CR1
citation_journal_title=Environmental Science and Pollution Research; citation_title=The quantitative real-time PCR applications in the monitoring of marine harmful algal bloom (HAB) species; citation_author=P Antonella, G Luca; citation_volume=20; citation_issue=10; citation_publication_date=2013; citation_pages=6 851-6 862; citation_doi=10.1007/s11356-012-1377-z; citation_id=CR2
citation_journal_title=Annual Review of Marine Science; citation_title=Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management; citation_author=D M Anderson, A D Cembella, G M Hallegraeff; citation_volume=4; citation_publication_date=2012; citation_pages=143-176; citation_doi=10.1146/annurev-marine-120308-081121; citation_id=CR3
citation_journal_title=Molecular and Cellular Probes; citation_title=Rapid, multiplex-tandem PCR assay for automated detection and differentiation of toxigenic cyanobacterial blooms; citation_author=L Baker, B C Sendall, R B Gasser, T Menjivar, B A Neilan, A R Jex; citation_volume=27; citation_issue=5-6; citation_publication_date=2013; citation_pages=208-214; citation_doi=10.1016/j.mcp.2013.07.001; citation_id=CR4
citation_journal_title=European Journal of Clinical Microbiology & Infectious Diseases; citation_title=Performance of a novel microarray multiplex PCR for the detection of 23 respiratory pathogens (SYMP-ARI study); citation_author=S Bierbaum, N Königsfeld, N Besazza, K Blessing, G Rücker, U Kontny, R Berner, M Schumacher, J Forster, V v d Falcone, C Sand, A Essig, D Huzly, G Rohde, D Neumann-Haefelin, M Panning; citation_volume=31; citation_issue=10; citation_publication_date=2012; citation_pages=2 851-2 861; citation_doi=10.1007/s10096-012-1639-1; citation_id=CR5
citation_journal_title=compressa (Chlorophyta) in the British Isles. Journal of Phycology; citation_title=Molecular and morphological analysis of Enteromorpha intestinalis and E; citation_author=J Blomster, C A Maggs, M J Stanhope; citation_volume=34; citation_issue=2; citation_publication_date=1998; citation_pages=319-340; citation_id=CR6
citation_journal_title=Marine Pollution Bulletin; citation_title=Potential risk of harmful algae transport by ballast waters: the case of Bilbao Harbour; citation_author=A Butrón, E Orive, I Madariaga; citation_volume=62; citation_issue=4; citation_publication_date=2011; citation_pages=747-757; citation_doi=10.1016/j.marpolbul.2011.01.008; citation_id=CR7
citation_journal_title=Limnology and Oceanography: Methods; citation_title=Improved quantitative real-time PCR assays for enumeration of harmful algal species in field samples using an exogenous DNA reference standard; citation_author=K J Coyne, S M Handy, E Demir, E B Whereat, D A Hutchins, K J Portune, M A Doblin, S Cary; citation_volume=3; citation_issue=9; citation_publication_date=2005; citation_pages=381-391; citation_doi=10.4319/lom.2005.3.381; citation_id=CR8
citation_journal_title=Marine Ecology Progress Series; citation_title=Automatic classification of field-collected dinoflagellates by artificial neural network; citation_author=P F Culverhouse, R G Simpson, R Ellis, J A Lindley, R Williams, T Parisini, B Reguera, I Bravo, R Zoppoli, G Earnshaw, H McCall, G Smith; citation_volume=139; citation_issue=1; citation_publication_date=1996; citation_pages=281-287; citation_doi=10.3354/meps139281; citation_id=CR9
citation_journal_title=Journal of Marine Sciences; citation_title=Analysis of the population structure of dinoflagellate cysts in the sediment of ballast tank of four cargo boats at Zhoushan Port; citation_author=X F Dai, D D Lu, C S Wang, P Xia, L Huang, C D Wang, H X Wang, H Y Huang, P X He; citation_volume=30; citation_issue=1; citation_publication_date=2012; citation_pages=11-18; citation_id=CR10
citation_journal_title=Parasitology; citation_title=Molecular characterization of the ribosomal RNA gene region of Perkinsus atlanticus: its use in phylogenetic analysis and as a target for a molecular diagnosis; citation_author=R De la Herrán, M A Garrido-Ramos, J I Navas, C Ruiz Rejón, M Ruiz Rejón; citation_volume=120; citation_issue=4; citation_publication_date=2000; citation_pages=345-353; citation_doi=10.1017/S003118209900565X; citation_id=CR11
citation_journal_title=Limnology and Oceanography: Methods; citation_title=Molecular detection of harmful algal blooms (HABs) using locked nucleic acids and bead array technology; citation_author=M R Diaz, J W Jacobson, K D Goodwin, S A Dunbar, J W Fell; citation_volume=8; citation_issue=6; citation_publication_date=2010; citation_pages=269-284; citation_doi=10.4319/lom.2010.8.269; citation_id=CR12
citation_journal_title=Journal of Applied Phycology; citation_title=Evaluation of locked nucleic acids for signal enhancement of oligonucleotide probes for microalgae immobilised on solid surfaces; citation_author=S Diercks, C M Gescher, K es, L K Medlin; citation_volume=21; citation_issue=6; citation_publication_date=2009; citation_pages=657-668; citation_doi=10.1007/s10811-008-9399-0; citation_id=CR13
citation_title=Pfiesteria species identified in ships’ ballast water and residuals: a possible vector for introductions to coastal areas; citation_inbook_title=Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission; citation_publication_date=2002; citation_pages=317-319; citation_id=CR14; citation_author=M A Doblin; citation_author=L A Drake; citation_author=K J Coyne; citation_author=P A Rublee; citation_author=F C Dobbs; citation_publisher=Florida Institute of Oceanography and Inter-governmental Oceanographic Commission of UNESCO.
citation_journal_title=in the Yellow Sea of China. Journal of Applied Phycology; citation_title=Morphological and molecular characterization of free-floating and attached green macroalgae Ulva spp; citation_author=W J Duan, L X Guo, D Sun, S F Zhu, X F Chen, W R Zhu, T Xu, C F Chen; citation_volume=24; citation_issue=1; citation_publication_date=2012; citation_pages=97-108; citation_doi=10.1007/s10811-011-9654-7; citation_id=CR15
citation_title=The Utermöhl method for quantitative phytoplankton analysis; citation_inbook_title=Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis. UNESCO; citation_publication_date=2010; citation_pages=13-20; citation_id=CR16; citation_author=L Edler; citation_author=M Elbrächter
citation_journal_title=Pattern Recognition Letters; citation_title=An introduction to ROC analysis; citation_author=T Fawcett; citation_volume=27; citation_issue=8; citation_publication_date=2006; citation_pages=861-874; citation_doi=10.1016/j.patrec.2005.10.010; citation_id=CR17
citation_journal_title=Marine Pollution Bulletin; citation_title=Macroalgal survival in ballast water tanks; citation_author=M M Flagella, M Verlaque, A Soria, M C Buia; citation_volume=54; citation_issue=9; citation_publication_date=2007; citation_pages=1 395-1 401; citation_doi=10.1016/j.marpolbul.2007.05.015; citation_id=CR18
citation_journal_title=Journal of Microbiological Methods; citation_title=Development of an oligonucleotide microarray for the detection and monitoring of marine dinoflagellates; citation_author=L Galluzzi, A Cegna, S Casabianca, A Penna, N Saunders, M Magnani; citation_volume=84; citation_issue=2; citation_publication_date=2011; citation_pages=234-242; citation_doi=10.1016/j.mimet.2010.11.024; citation_id=CR19
citation_journal_title=Journal of Plankton Research; citation_title=Assessment of cryptic species diversity within blooms and cyst bank of the Alexandrium tamarense complex (Dinophyceae) in a Mediterranean lagoon facilitated by semi-multiplex PCR; citation_author=B Genovesi, M S Shin-Grzebyk, D Grzebyk, M Laabir, P A Gagnaire, A Vaquer, A Pastoureaud, B Lasserre, Y Collos, P Berrebi, E Masseret; citation_volume=33; citation_issue=3; citation_publication_date=2011; citation_pages=405-414; citation_doi=10.1093/plankt/fbq127; citation_id=CR20
citation_journal_title=Limnology and Oceanography: Methods; citation_title=Field applications of the secondgeneration Environmental Sample Processor (ESP) for remote detection of harmful algae: 2006–2007; citation_author=D I Greenfield, I R Marin, G J Doucette, C M Mikulski, K L Jones, S Jensen, B Roman, N Alvarado, J Feldman, C A Scholin; citation_volume=6; citation_issue=12; citation_publication_date=2008; citation_pages=667-679; citation_doi=10.4319/lom.2008.6.667; citation_id=CR21
citation_journal_title=Journal of Phycology; citation_title=Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge; citation_author=G M Hallegraeff; citation_volume=46; citation_issue=2; citation_publication_date=2010; citation_pages=220-235; citation_doi=10.1111/j.1529-8817.2010.00815.x; citation_id=CR22
citation_title=Bloom dynamics of the toxic dinoflagellate Gymnodinium catenatum, with emphasis on Tasmanian and Spanish coastal waters; citation_inbook_title=Physiological Ecology of Harmful Algal Blooms; citation_publication_date=1998; citation_pages=59-80; citation_id=CR23; citation_author=G M Hallegraeff; citation_author=S Fraga; citation_publisher=Springer-Verlag
citation_journal_title=Phycologia; citation_title=Harmful dinoflagellate resting cysts in ships’ ballast tank sediments: potential for introduction into English and Welsh waters; citation_author=J P Hamer, I A N Lucas, T A McCollln; citation_volume=40; citation_issue=3; citation_publication_date=2001; citation_pages=246-255; citation_doi=10.2216/i0031-8884-40-3-246.1; citation_id=CR24
citation_journal_title=Harmful Algae; citation_title=Using quantitative real-time PCR to study competition and community dynamics among Delaware Inland Bays harmful algae in field and laboratory studies; citation_author=S M Handy, E Demir, D A Hutchins, K J Portune, E B Whereat, C E Hare, J M Rose, M Warner, M Farestad, S C Cary, K J Coyne; citation_volume=7; citation_issue=5; citation_publication_date=2008; citation_pages=599-613; citation_doi=10.1016/j.hal.2007.12.018; citation_id=CR25
citation_journal_title=Limnology and Oceanography: Methods; citation_title=Simultaneous enumeration of multiple raphidophyte species by quantitative real-time PCR: capabilities and limitations; citation_author=S M Handy, D A Hutchins, S C Cary, K J Coyne; citation_volume=4; citation_issue=6; citation_publication_date=2006; citation_pages=193-204; citation_doi=10.4319/lom.2006.4.193; citation_id=CR26
citation_journal_title=European Journal of Phycology; citation_title=Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera; citation_author=H S Hayden, J Blomster, C A Maggs, P C Silva, M J Stanhope, J R Waaland; citation_volume=38; citation_issue=3; citation_publication_date=2003; citation_pages=277-294; citation_doi=10.1080/1364253031000136321; citation_id=CR27
citation_journal_title=European Journal of Phycology; citation_title=Ulva, Umbraulva and Gemina: genetic survey of New Zealand taxa reveals diversity and introduced species; citation_author=S Heesch, J E Broom, K F Neill, T J Farr, J L Dalen, W A Nelson; citation_volume=44; citation_issue=2; citation_publication_date=2009; citation_pages=143-154; citation_doi=10.1080/09670260802422477; citation_id=CR28
citation_journal_title=Phycological Research; citation_title=The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae); citation_author=M Hiraoka, S Enomoto; citation_volume=46; citation_issue=3; citation_publication_date=1998; citation_pages=199-203; citation_doi=10.1111/j.1440-1835.1998.tb00114.x; citation_id=CR29
citation_journal_title=Limnology and Oceanography; citation_title=Green algae blooms caused by Ulva prolifera in the southern Yellow Sea: identification of the original bloom location and evaluation of biological processes occurring during the early northward floating period; citation_author=Y Z Huo, J S Zhang, L P Chen, M Hu, K F Yu, Q F Chen, Q He, P M He; citation_volume=58; citation_issue=6; citation_publication_date=2013; citation_pages=2 206-2 218; citation_doi=10.4319/lo.2013.58.6.2206; citation_id=CR30
citation_journal_title=Marine Pollution Bulletin; citation_title=Inter-and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007-2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China; citation_author=J K Keesing, D Y Liu, P Fearns, R Garcia; citation_volume=62; citation_issue=6; citation_publication_date=2011; citation_pages=1 169-1 182; citation_doi=10.1016/j.marpolbul.2011.03.040; citation_id=CR31
citation_journal_title=Environmental Science and Pollution Research; citation_title=Introduction to project MIDTAL: its methods and samples from Arcachon Bay, France; citation_author=J U D Kegel, Y Amo, L K Medlin; citation_volume=20; citation_issue=10; citation_publication_date=2013; citation_pages=6 690-6 704; citation_doi=10.1007/s11356-012-1299-9; citation_id=CR32
citation_journal_title=Biosensors and Bioelectronics; citation_title=A low-density oligonucleotide array study for parallel detection of harmful algal species using hybridization of consensus PCR products of LSU rDNA D2 domain; citation_author=J S Ki, M S Han; citation_volume=21; citation_issue=9; citation_publication_date=2006; citation_pages=1 812-1 821; citation_doi=10.1016/j.bios.2005.09.006; citation_id=CR33
citation_journal_title=Molecular Ecology; citation_title=Molecular analysis of predation: a review of best practice for DNA-based approaches; citation_author=R A King, D S Read, M Traugott, W O C Symondson; citation_volume=17; citation_issue=4; citation_publication_date=2008; citation_pages=947-963; citation_doi=10.1111/j.1365-294X.2007.03613.x; citation_id=CR34
citation_journal_title=Agardh and its spores in darkness: implications for ballast water management. Aquatic Botany; citation_title=Fate of Enteromorpha flexuosa (Wulfen) J; citation_author=J P Kolwalkar, S S Sawant, V K Dhargalkar; citation_volume=86; citation_issue=1; citation_publication_date=2007; citation_pages=86-88; citation_id=CR35
citation_journal_title=Harmful Algae; citation_title=Physical-biological coupling induced aggregation mechanism for the formation of high biomass red tides in low nutrient waters; citation_author=Z G Lai, K D Yin; citation_volume=31; citation_publication_date=2014; citation_pages=66-75; citation_doi=10.1016/j.hal.2013.09.011; citation_id=CR36
citation_journal_title=Journal of Plankton Research; citation_title=Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: evidence from DNA and toxin analysis; citation_author=E L Lilly, D M Kulis, P Gentien, D M Anderson; citation_volume=24; citation_issue=5; citation_publication_date=2002; citation_pages=443-452; citation_doi=10.1093/plankt/24.5.443; citation_id=CR37
citation_journal_title=Marine Environmental Research; citation_title=Understanding the recurrent large-scale green tide in the Yellow Sea: temporal and spatial correlations between multiple geographical, aquacultural and biological factors; citation_author=F Liu, S J Pang, T Chopin, S Q Gao, T F Shan, X B Zhao, J Li; citation_volume=83; citation_publication_date=2013; citation_pages=38-47; citation_doi=10.1016/j.marenvres.2012.10.007; citation_id=CR38
citation_journal_title=Marine Pollution Bulletin; citation_title=Temporal and spatial distribution of red tide outbreaks in the Yangtze River Estuary and adjacent waters, China; citation_author=L S Liu, J Zhou, B H Zheng, W Q Cai, K X Lin, J L Tang; citation_volume=72; citation_issue=1; citation_publication_date=2013; citation_pages=213-221; citation_doi=10.1016/j.marpolbul.2013.04.002; citation_id=CR39
citation_journal_title=Phycologia; citation_title=Morphology, rbc L phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain; citation_author=C J Loughnane, L M McIvor, F Rindi, D B Stengel, M D Guiry; citation_volume=47; citation_issue=4; citation_publication_date=2008; citation_pages=416-429; citation_doi=10.2216/PH07-61.1; citation_id=CR40
citation_journal_title=Journal of Clinical Laboratory Analysis; citation_title=Multiplex polymerase chain reaction: a practical approach; citation_author=P Markoulatos, N Siafakas, M Moncany; citation_volume=16; citation_issue=1; citation_publication_date=2002; citation_pages=47-51; citation_doi=10.1002/jcla.2058; citation_id=CR41
citation_journal_title=Journal of Clinical Microbiology; citation_title=18S Ribosomal DNABased PCR for Diagnosis of Trichomonas vaginalis; citation_author=H Mayta, R H Gilman, M M Calderon, A Gottlieb, G Soto, I Tuero, S Sanchez, A Vivar; citation_volume=38; citation_issue=7; citation_publication_date=2000; citation_pages=2 683-2 687; citation_id=CR42
citation_journal_title=Harmful Algae; citation_title=The efficiency of regional ballast water exchange: changes in phytoplankton abundance and diversity; citation_author=T McCollin, A M Shanks, J Dunn; citation_volume=6; citation_issue=4; citation_publication_date=2007; citation_pages=531-546; citation_doi=10.1016/j.hal.2006.04.015; citation_id=CR43
citation_journal_title=Environmental Science and Pollution Research; citation_title=An evaluation of the applicability of microarrays for monitoring toxic algae in Irish coastal waters; citation_author=G R McCoy, N Touzet, G T Fleming, R Raine; citation_volume=20; citation_issue=10; citation_publication_date=2013; citation_pages=6 751-6 764; citation_doi=10.1007/s11356-012-1294-1; citation_id=CR44
citation_journal_title=Current Opinion in Infectious Diseases; citation_title=Defining the causes of diarrhea: novel approaches; citation_author=D J Operario, E Houpt; citation_volume=24; citation_issue=5; citation_publication_date=2011; citation_pages=464-471; citation_doi=10.1097/QCO.0b013e32834aa13a; citation_id=CR45
citation_journal_title=Journal of Applied Phycology; citation_title=Induction of fastgrowing and morphologically different strains through intergeneric protoplast fusions of Ulva and Enteromorpha (Ulvales, Chlorophyta); citation_author=C R K Reddy, M Iima, Y Fujita; citation_volume=4; citation_issue=1; citation_publication_date=1992; citation_pages=57-65; citation_doi=10.1007/BF00003961; citation_id=CR46
citation_journal_title=Journal of Laboratory Automation; citation_title=Controlling a robotic marine environmental sampler with the Ruby scripting language; citation_author=B Roman, C Scholin, S Jensen, E Massion, R Marin, C Preston, D Greenfield, W Jones, K Wheeler; citation_volume=12; citation_issue=1; citation_publication_date=2007; citation_pages=56-61; citation_doi=10.1016/j.jala.2006.07.013; citation_id=CR47
citation_journal_title=Oceanography; citation_title=Remote detection of marine microbes, small invertebrates, harmful algae, and biotoxins using the Environmental Sample Processor (ESP); citation_author=C Scholin, G Doucette, S Jensen, B Roman, D Pargett, I R Marin, C Preston, W Jones, J Feldman, C Everlove, A Harris, N Alvarado, E Massion, J Birch, D Greenfield, R Vrijenhoek, C Mikulski, K Jones; citation_volume=22; citation_issue=2; citation_publication_date=2009; citation_pages=158-167; citation_doi=10.5670/oceanog.2009.46; citation_id=CR48
citation_journal_title=Harmful Algae; citation_title=Multiple simultaneous detection of Harmful Algal Blooms (HABs) through a high throughput bead array technology, with potential use in phytoplankton community analysis; citation_author=G Scorzetti, L E Brand, G L Hitchcock, K S Rein, C D Sinigalliano, J W Fell; citation_volume=8; citation_issue=2; citation_publication_date=2009; citation_pages=196-211; citation_doi=10.1016/j.hal.2008.05.003; citation_id=CR49
citation_journal_title=Food and Bioprocess Technology; citation_title=Advances in DNA microarray technology for the detection of foodborne pathogens; citation_author=M Severgnini, P Cremonesi, C Consolandi, G De Bellis, B Castiglioni; citation_volume=4; citation_issue=6; citation_publication_date=2011; citation_pages=936-953; citation_doi=10.1007/s11947-010-0430-5; citation_id=CR50
citation_journal_title=Journal of Applied Phycology; citation_title=Effects of germanium dioxide, an inhibitor of diatom growth, on the microscopic laboratory cultivation stage of the kelp, Laminaria saccharina; citation_author=R Shea, T Chopin; citation_volume=19; citation_issue=1; citation_publication_date=2007; citation_pages=27-32; citation_doi=10.1007/s10811-006-9107-x; citation_id=CR51
citation_journal_title=Aquaculture; citation_title=Detection of bacterial pathogens in aquaculture samples by DNA microarray analysis; citation_author=Y H Shi, J Chen, C H Li, X J Lu, D M Zhang, H Y Li, Z X Zhao, M Y Li; citation_volume=338-341; citation_publication_date=2012; citation_pages=29-35; citation_doi=10.1016/j.aquaculture.2012.01.009; citation_id=CR52
citation_journal_title=Nature; citation_title=Green and golden seaweed tides on the rise; citation_author=V Smetacek, A Zingone; citation_volume=504; citation_issue=7478; citation_publication_date=2013; citation_pages=84-88; citation_doi=10.1038/nature12860; citation_id=CR53
citation_title=2008 China Marine Calamities Bulletin; citation_publication_date=2009; citation_id=CR54
citation_title=2012 China Marine Calamities Bulletin; citation_publication_date=2013; citation_id=CR55
citation_journal_title=Journal of Anhui Agricultural Sciences; citation_title=Combined Morphological and Molecular Approach to the Ulva (Chlorophyta, Ulvophyceae) in the Ningbo Area; citation_author=D Sun, C H Sun, W J Duan, J J Shi, B W Li, D Wang; citation_volume=39; citation_issue=12; citation_publication_date=2011; citation_pages=6 936-6 938; citation_id=CR56
citation_journal_title=Experimental Parasitology; citation_title=Simple, rapid, inexpensive platform for the diagnosis of malaria by loop mediated isothermal amplification (LAMP); citation_author=R Surabattula, M P Vejandla, P C Mallepaddi, K Faulstich, R Polavarapu; citation_volume=134; citation_issue=3; citation_publication_date=2013; citation_pages=333-340; citation_doi=10.1016/j.exppara.2013.03.031; citation_id=CR57
citation_journal_title=International Dairy Journal; citation_title=Development and validation of a multiplex PCR-based DNA microarray hybridisation method for detecting bacterial antibiotic resistance genes in cheese; citation_author=D Susana, F Fabio, M Baltasar, T Sandra; citation_volume=21; citation_issue=3; citation_publication_date=2011; citation_pages=149-157; citation_doi=10.1016/j.idairyj.2010.10.005; citation_id=CR58
citation_journal_title=Food Science; citation_title=Accumulation features and immuno-stimulative effects of ß-glucans from six species of marine microalgae; citation_author=T Tian, C X Zhou, B N Liu, H M Chen, X J Yan; citation_volume=34; citation_issue=3; citation_publication_date=2013; citation_pages=188-192; citation_id=CR59
citation_journal_title=Acta Biophysica Sinica; citation_title=Screening of oilproducing microalgae and detecting dynamics of neutral lipid accumulation; citation_author=J N Wang, X J Yan, C X Zhou, J L Xu; citation_volume=26; citation_issue=6; citation_publication_date=2010; citation_pages=472-480; citation_id=CR60
citation_journal_title=Journal of Clinical Microbiology; citation_title=Differentiation of the seven major lyssavirus species by oligonucleotide microarray; citation_author=J Xi, H C Guo, Y Feng, Y B Xu, M F Shao, N Su, J Y Wan, J P Li, C C Tu; citation_volume=50; citation_issue=3; citation_publication_date=2012; citation_pages=619-625; citation_doi=10.1128/JCM.00848-11; citation_id=CR61
citation_journal_title=at Yatsu tidal flat, Japan. Limnology; citation_title=Green tide formed by free-floating Ulva spp; citation_author=T Yabe, Y Ishii, Y Amano, T Koga, S Hayashi, S Nohara, H Tatsumoto; citation_volume=10; citation_issue=3; citation_publication_date=2009; citation_pages=239-245; citation_id=CR62
citation_journal_title=Marine Sciences; citation_title=Plankton found in ballast waters of foreign ships harboring in ports of Southeast China; citation_author=Q L Yang, L H Cai, Y H Gao, Z Su, C P Chen, G M Lin, M Z Huang, B Q Li, P Xiang, C Y Xu, H D Zheng, J R Liang, X L Xiang, M J Fang; citation_volume=35; citation_issue=1; citation_publication_date=2011; citation_pages=22-28; citation_id=CR63
citation_journal_title=Molecular Biology and Evolution; citation_title=Tertiary endosymbiosis driven genome evolution in dinoflagellate algae; citation_author=H S Yoon, J D Hackett, F M Van Dolah, T Nosenko, K L Lidie, D Bhattacharya; citation_volume=22; citation_issue=5; citation_publication_date=2005; citation_pages=1 299-1 308; citation_doi=10.1093/molbev/msi118; citation_id=CR64
citation_journal_title=Harmful Algae; citation_title=Development of a rapid detection and quantification method of Karenia mikimotoi by real-time quantitative PCR; citation_author=J Yuan, T Z Mi, Y Zhen, Z G Yu; citation_volume=17; citation_publication_date=2012; citation_pages=83-91; citation_doi=10.1016/j.hal.2012.03.004; citation_id=CR65
citation_journal_title=Harmful Algae; citation_title=Simultaneous detection of harmful algae by multiple polymerase chain reaction coupled with reverse dot blot hybridization; citation_author=C Y Zhang, G F Chen, Y Liu, Y Y Wang, Z Xu, B Y Zhang, G C Wang; citation_volume=35; citation_publication_date=2014; citation_pages=9-19; citation_doi=10.1016/j.hal.2014.03.004; citation_id=CR66
citation_journal_title=Asian Journal of Ecotoxicology; citation_title=Hemolytic activity studies of several harmful Alga strains; citation_author=C X Zhou, Y J Fu, X J Yan; citation_volume=2; citation_issue=1; citation_publication_date=2007; citation_pages=78-82; citation_id=CR67
citation_journal_title=Marine Sciences; citation_title=The population growth and variation of nitrate-N and phosphate-P in the mix-culture of Phaeodactylum tricornutum Bohl and Prorocentrum micans; citation_author=C X Zhou, B Ma, F X Wang, B Xu, X J Yan; citation_volume=30; citation_issue=12; citation_publication_date=2006; citation_pages=58-61; citation_id=CR68
citation_journal_title=Journal of Microbiological Methods; citation_title=Development and evaluation of a real-time fluorogenic loop-mediated isothermal amplification assay integrated on a microfluidic disc chip (on-chip LAMP) for rapid and simultaneous detection of ten pathogenic bacteria in aquatic animals; citation_author=Q J Zhou, L Wang, J Chen, R N Wang, Y H Shi, C H Li, D M Zhang, X J Yan, Y J Zhang; citation_volume=104; citation_publication_date=2014; citation_pages=26-35; citation_doi=10.1016/j.mimet.2014.06.008; citation_id=CR69
citation_journal_title=Plant Quarantine; citation_title=The investigation and risk analysis of the red tide species in ballast waters of foreign ships harboring in Shanghai port; citation_author=S H Zhou, J Wu, Q S Meng, W J Ma, Y T Qin, X F Gu, Y G Huang, G P Cao, J Z Chen; citation_volume=26; citation_issue=3; citation_publication_date=2012; citation_pages=40-43; citation_id=CR70
citation_journal_title=Journal of Clinical Microbiology; citation_title=Use of a DNA microarray for simultaneous detection of antibiotic resistance genes among staphylococcal clinical isolates; citation_author=L X Zhu, Z W Zhang, C Wang, H W Yang, D Jiang, Q Zhang, K Mitchelson, J Cheng; citation_volume=45; citation_issue=11; citation_publication_date=2007; citation_pages=3 514-3 521; citation_doi=10.1128/JCM.02340-06; citation_id=CR71