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Development of a high-resolution molecular marker for tracking Pseudo-nitzschia pungens genetic diversity through comparative analysis of mitochondrial genomes

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Abstract

The harmful algal bloom (HAB) species Pseudo-nitzschia pungens is widely distributed in almost all continents. Accumulating evidence suggests that P. pungens has high genetic diversity and many strains can produce the toxin domoic acid (DA) that harms animals and humans. Nevertheless, different P. pungens strains cannot be distinguished using morphological features or using common molecular markers including 18S rDNA, 28S rDNA, ITS, cox1, and rbcL. As such, high-resolution molecular markers need to be developed to resolve P. pungens genetic diversity, facilitating accurate tracking of toxic P. pungens strains. We hypothesized that molecular markers with high resolution and high specificity can be designed through identifying regions with high genomic variations in the mitochondrial genome. Here, we describe the development of a new molecular marker Pseudo-nitzschia pungens mitochondrial 1 (ppmt1) with high resolution and high specificity through comparative analysis of mitochondrial genomes of nine P. pungens strains isolated from coastal regions of China. In conclusion, we have developed ppmt1 as a high-resolution and high-specificity molecular marker for tracking strains and genetic diversity of the HAB species P. pungens.

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References

  • An SM, Noh JH, Lee HR, Choi DH, Lee JH, Yang EC (2016) Complete mitochondrial genome of biraphid benthic diatom, Navicula ramosissima (Naviculales, Bacillariophyceae). Mitochondrial DNA B 1:549–550

    Article  Google Scholar 

  • An SM, Kim SY, Noh JH, Yang EC (2017) Complete mitochondrial genome of Skeletonema marinoi (Mediophyceae, Bacillariophyta), a clonal chain forming diatom in the west coast of Korea. Mitochondrial DNA A 28:19–20

    Article  CAS  Google Scholar 

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Aunins AW, Hamilton D, King TL (2018) The complete mitochondrial genome of the stalk-forming diatom Didymosphenia geminata. Mitochondrial DNA B 3:676–677

    Article  Google Scholar 

  • Barra L, Ruggiero MV, Chen J, Kooistra WHCF (2014) Specificity of LSU rRNA-targeted oligonucleotide probes for Pseudo-nitzschia species tested through dot-blot hybridisation. Environ Sci Pollut Res 21:548–557

    Article  CAS  Google Scholar 

  • Bates SS, Garrison DL, Horner RA (1998) Bloom dynamics and physiology of domoic acid producing Pseudo-nitzschia species. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Heidelberg, pp 267–292

    Google Scholar 

  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Casteleyn G, Chepurnov VA, Leliaert F, Mann DG, Bates SS, Lundholm N, Rhodes L, Sabbe K, Vyverman W (2008) Pseudo-nitzschia pungens (Bacillariophyceae): a cosmopolitan diatom species? Harmful Algae 7:241–257

    Article  CAS  Google Scholar 

  • Casteleyn G, Adams NG, Vanormelingen P, Debeer A-E, Sabbe K, Vyverman W (2009) Natural hybrids in the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae): Genetic and morphological evidence. Protist 160:343–354

    Article  CAS  PubMed  Google Scholar 

  • Chepurnov VA, Mann DG, Sabbe K, Vannerum K, Casteleyn G, Verleyen E, Peperzak L, Vyverman W (2005) Sexual reproduction, mating system, chloroplast dynamics and abrupt cell size reduction in Pseudo-nitzschia pungens from the North Sea (Bacillariophyta). Eur J Phycol 40:379–395

    Article  Google Scholar 

  • Churro CI, Carreira CC, Rodrigues FJ, Craveiro SC, Calado AJ, Casteleyn G, Lundholm N (2009) Diversity and abundance of potentially toxic Pseudo-nitzschia Peragallo in Aveiro coastal lagoon, Portugal and description of a new variety, P. pungens var. aveirensis var. nov. Diatom Res 24:35–62

  • Crowell RM, Nienow JA, Cahoon AB (2019) The complete chloroplast and mitochondrial genomes of the diatom Nitzschia palea (Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotom Durinskia baltica. J Phycol 55:352–364

    Article  CAS  PubMed  Google Scholar 

  • Cunningham C (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14:733–740

    Article  CAS  PubMed  Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dong H, Huang C, Xu G, Li Y (2018) Studies on intraspecies diversity of Pseudo-nitzschia pungens from Chinese coastal waters. J Trop Oceanogr 37:12–19

    Google Scholar 

  • Dong HC, Lundholm N, Teng ST, Li A, Wang C, Hu Y, Li Y (2020) Occurrence of Pseudo-nitzschia species and associated domoic acid production along the Guangdong coast, South China Sea. Harmful Algae 98:101899

    Article  CAS  PubMed  Google Scholar 

  • Famà P, Wysor B, Kooistra WHCF, Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J Phycol 38:1040–1050

    Article  Google Scholar 

  • Gastineau R, Kim S-Y, Lemieux C, Turmel M, Witkowski A, Park J-G, Kim B-S, Mann DG, Theriot EC (2019) Complete mitochondrial genome of a rare diatom (Bacillariophyta) Proschkinia and its phylogenetic and taxonomic implications. Mitochondrial DNA B 4:25–26

    Article  Google Scholar 

  • Ghosh S, Love NG (2011) Application of rbcL based molecular diversity analysis to algae in wastewater treatment plants. Bioresour Technol 102:3619–3622

    Article  CAS  PubMed  Google Scholar 

  • Grayburn WS, Hudspeth DSS, Gane MK, Hudspeth MES (2004) The mitochondrial genome of Saprolegnia ferax: organization, gene content and nucleotide sequence. Mycologia 96:981–989

    Article  CAS  PubMed  Google Scholar 

  • Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47:W59–W64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillard RRL, Hargreaves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236

    Article  Google Scholar 

  • Guillory WX, Onyshchenko A, Ruck EC, Parks M, Nakov T, Wickett NJ, Alverson AJ (2018) Recurrent loss, horizontal transfer, and the obscure origins of mitochondrial introns in diatoms (Bacillariophyta). Genome Biol Evol 10:1504–1515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guiry MD, Guiry GM (2020) Pseudo-nitzschia pungens (Grunow ex Cleve) Hasle,1993. http://www.algaebase.org/search/species/detail/?species_id=39547

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hasle GR (1994) Pseudo-nitzschia as a genus distinct from Nitzschia (Bacillariophyceae). J Phycol 30:1036–1039

    Article  Google Scholar 

  • Hauth AM, Maier UG, Lang BF, Burger G (2005) The Rhodomonas salina mitochondrial genome: bacteria-like operons, compact gene arrangement and complex repeat region. Nucleic Acids Res 33:4433–4442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Hu Y, Xing W, Song H, Liu G, Hu Z (2019) Analysis of mitochondrial and chloroplast genomes in two volvocine algae: Eudorina elegans and Eudorina cylindrica (Volvocaceae, Chlorophyta). Eur J Phycol 54:193–205

    Article  CAS  Google Scholar 

  • Huang CX, Dong HC, Lundholm N, Teng ST, Zheng GC, Tan ZJ, Lim PT, Li Y (2019) Species composition and toxicity of the genus Pseudo-nitzschia in Taiwan Strait, including P. chiniana sp. nov. and P. qiana sp. nov. Harmful Algae 84:195–209

    Article  CAS  PubMed  Google Scholar 

  • Imanian B, Pombert J-F, Dorrell RG, Burki F, Keeling PJ (2012) Tertiary endosymbiosis in two dinotoms has generated little change in the mitochondrial genomes of their dinoflagellate hosts and diatom endosymbionts. PLoS One 7:e43763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kajitani R, Yoshimura D, Okuno M, Minakuchi Y, Kagoshima H, Fujiyama A, Kubokawa K, Kohara Y, Toyoda A, Itoh T (2019) Platanus-allee is a de novo haplotype assembler enabling a comprehensive access to divergent heterozygous regions. Nature Comm 10:1702

    Article  CAS  Google Scholar 

  • Kamikawa R, Azuma T, K-i I, Matsuno Y, Miyashita H (2018) Diversity of organellar genomes in non-photosynthetic diatoms. Protist 169:351–361

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim E, Lane CE, Curtis BA, Kozera C, Bowman S, Archibald JM (2008) Complete sequence and analysis of the mitochondrial genome of Hemiselmis andersenii CCMP644 (Cryptophyceae). BMC Genomics 9:215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim JH, Park BS, Kim J-H, Wang P, Han M-S (2015) Intraspecific diversity and distribution of the cosmopolitan species Pseudo-nitzschia pungens (Bacillariophyceae): morphology, genetics, and ecophysiology of the three clades. J Phycol 51:159–172

    Article  PubMed  Google Scholar 

  • Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22:568–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lelong A, Hégaret H, Soudant P, Bates SS (2012) Pseudo-nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: revisiting previous paradigms. Phycologia 51:168–216

    Article  CAS  Google Scholar 

  • Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26:589–595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu L, He Y, Wang K, Miao J, Zheng Z (2020) The complete mitochondrial genome of Antarctic Phaeodactylum tricornutum ICE-H. Mitochondrial DNA B 5:2754–2755

    Article  Google Scholar 

  • Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu SH, Qi YZ (1992) Main red tide causative species of Da Peng Bay, South China Sea. J Jinan Univ 13:130–133

    Google Scholar 

  • Mackenzie AL, White DA, Sim PG, Holland AJ (1993) Domoic acid and the New Zealand greenshell mussel (Perna canaliculus). In: Smayada TJ, Shimizu Y (eds) Toxic Phytoplankton Blooms in the Sea, vol 3. Elsevier, New York, pp 607–612

    Google Scholar 

  • Martin FN (2008) Mitochondrial haplotype determination in the oomycete plant pathogen Phytophthora ramorum. Curr Genet 54:23–34

    Article  CAS  PubMed  Google Scholar 

  • Niu YD, Li M, Wei FW, Feng ZJ (2001) Reliability of mtDNA as molecular marker and its perspective. Hereditas 23:593–598

    CAS  Google Scholar 

  • Oudot-Le Secq M-P, Green BR (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476:20–26

    Article  CAS  PubMed  Google Scholar 

  • Patrick L, Nicolas C, Hess P, Elisabeth N (2016) Toxic and harmful microalgae of the world ocean. The International Society for the Study of Harmful Algae and UNESCO, Denmark

    Google Scholar 

  • Pogoda CS, Keepers KG, Hamsher SE, Stepanek JG, Kane NC, Kociolek JP (2019) Comparative analysis of the mitochondrial genomes of six newly sequenced diatoms reveals group II introns in the barcoding region of cox1. Mitochondrial DNA A 30:43–51

    Article  CAS  Google Scholar 

  • Prasetiya FS, Gastineau R, Poulin M, Lemieux C, Turmel M, Syakti AD, Hardivillier Y, Widowati I, Risjani Y, Iskandar I, Subroto T, Falaise C, Arsad S, Safitri I, Mouget J-L, Leignel V (2019) Haslea nusantara (Bacillariophyceae), a new blue diatom from the Java Sea, Indonesia: morphology, biometry and molecular characterization. Plant Ecol Evol 152:188–202

    Article  Google Scholar 

  • Qi YZ, Wang J, Zheng L (1994) The taxonomy and bloom ecology of Pseudo-nitzschia on the coasts of China. Proceedings IOC-WESTPAC Third International Scientific Symposium. Bali, Indonesia: Indonesia Institute of Sciences

  • Ravin NV, Galachyants YP, Mardanov AV, Beletsky AV, Petrova DP, Sherbakova TA, Zakharova YR, Likhoshway YV, Skryabin KG, Grachev MA (2010) Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Curr Genet 56:215–223

    Article  CAS  PubMed  Google Scholar 

  • Rhodes L, White D, Syhre M, Atkinson M (1996) Pseudo-nitzschia species isolated from New Zealand coastal waters: domoic acid production in vitro and links with shellfish toxicity. Harmful and toxic algal blooms. IOC UNESCO, Paris

    Google Scholar 

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secq M-PO-L, Green BR (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476:20–26

    Article  CAS  Google Scholar 

  • Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319

    Article  CAS  PubMed  Google Scholar 

  • Smith SA, Dunn CW (2008) Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24:715–716

    Article  CAS  PubMed  Google Scholar 

  • Song H, Liu F, Li Z, Xu Q, Chen Y, Yu Z, Chen N (2020) Development of a high-resolution molecular marker for tracking Phaeocystis globosa genetic diversity through comparative analysis of chloroplast genomes. Harmful Algae 99:101911

    Article  CAS  PubMed  Google Scholar 

  • Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10

    Article  CAS  PubMed  Google Scholar 

  • Swofford D (2002) PAUP*: Phylogenetic Analysis Using Parsimony. Version 40b10 Sinauer Associates, Sunderland

  • Tan SN, Lim HC, Teng ST, Lim PT, Leaw CP (2015) Pseudo-nitzschia species (Bacillariophyceae) identification and delineation using mitochondrial cox1 gene sequences as compared to LSU rDNA. Fish Sci 81:831–838

    Article  CAS  Google Scholar 

  • Tang X, Bi G (2016) Complete mitochondrial genome of Fistulifera solaris (Bacillariophycidae). Mitochondrial DNA A 27:4405–4406

    Article  CAS  Google Scholar 

  • Teng ST, Leaw CP, Lim HC, Lim PT (2013) The genus Pseudo-nitzschia (Bacillariophyceae) in Malaysia, including new records and a key to species inferred from morphology-based phylogeny. Bot Mar 56:375–398

    Article  Google Scholar 

  • Trainer VL, Wekell JC, Horner RA, Hatfield CL, Stein JE (1998) Domoic acid production by Pseudo-nitzschia pungens. Harmful Algae:337–340

  • Trainer VL, Bates SS, Lundholm N, Thessen AE, Cochlan WP, Adams NG, Trick CG (2012) Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae 14:271–300

    Article  Google Scholar 

  • Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valach M, Burger G, Gray MW, Lang BF (2014) Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res 42:13764–13777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villac MC, Fryxell GA (1998) Pseudo-nitzschia pungens var. cingulata var. nov. (Bacillariophyceae) based on field and culture observations. Phycologia 37:269

    Article  Google Scholar 

  • Villain A, Kojadinovic M, Puppo C, Prioretti L, Hubert P, Zhang Y, Grégori G, Roulet A, Roques C, Claverie J-M, Gontero B, Blanc G (2017) Complete mitochondrial genome sequence of the freshwater diatom Asterionella formosa. Mitochondrial DNA B 2:97–98

    Article  Google Scholar 

  • Yamaguchi H, Nakayama T, Hongoh Y, Kawachi M, Inouye I (2014) Molecular diversity of endosymbiotic Nephroselmis (Nephroselmidophyceae) in Hatena arenicola (Katablepharidophycota). J Plant Res 127:241–247

    Article  PubMed  Google Scholar 

  • Yang ZB, Hodgkiss IJ (2002) Potentially harmful Pseudo-nitzschia species in Hong Kong coastal waters. In: KC HO, Lin HY, Yu ZX (eds) Prevention and Management of Harmful Algal Blooms in the South China Sea. Hong Kong. Association on Harmful Algal Blooms in the South China Sea (AoHABSCS), Hong Kong, pp 123–128

    Google Scholar 

  • Yuan XL, Cao M, Bi GQ (2016) The complete mitochondrial genome of Pseudo-nitzschia multiseries (Bacillariophyta). Mitochondrial DNA A 27:2777–2778

    Article  CAS  Google Scholar 

  • Zhang MJ, Cui ZM, Liu F, Chen NS (2021) Definition of a high-resolution molecular marker for tracking the genetic diversity of the harmful algal species Eucampia zodiacus through comparative analysis of mitochondrial genomes. Front Microbiol 12:631144

    Article  PubMed  PubMed Central  Google Scholar 

  • Zou JZ, Zhou MJ, Zhang C (1993) Ecological features of toxic Nitzschia pungens Grunow in Chinese coastal water. In: Smayada TJ, Shimizu Y (eds) Toxic Phytoplankton Blooms in the Sea, vol 3. Elsevier, New York, pp 651–657

    Google Scholar 

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Acknowledgements

We are grateful to colleagues from the Jiaozhou Bay Marine Ecosystem Research Station for their help in field sampling. The samples from the Bohai Sea were supported by the National Natural Science Foundation of China, Bohai and Yellow Sea Oceanography Expedition (NORC2019-01). Data acquisition and sample collections from the East China Sea were supported by National Natural Science Foundation of China (NSFC) Open Research Cruise (Cruise No. NORC2019-2), funded by Shiptime Sharing Project of NSFC. This cruise was conducted onboard R/V “Xiang Yang Hong 18” by The First Institute of Oceanography, Ministry of Natural Resources, China.

Funding

This research was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB42000000), Chinese Academy of Sciences Pioneer Hundred Talents Program (to Nansheng Chen), Taishan Scholar Project Special Fund (to Nansheng Chen), Qingdao Innovation and Creation Plan (Talent Development Program-5th Annual Pioneer and Innovator Leadership Award to Nansheng Chen, 19-3-2-16-zhc), the Key Research Program of Frontier Sciences, Chinese Academy of Sciences (No. QYZDB-SSW-DQC023) (to Feng Liu), and the Major Scientific and Technological Innovation Project of Shandong Province (No. 2019JZZY020706) (to Feng Liu).

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  1. CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Yang Chen, Yichao Wang, Kuiyan Liu, Feng Liu & Nansheng Chen

  2. Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266200, China

    Yang Chen, Yichao Wang, Kuiyan Liu, Feng Liu & Nansheng Chen

  3. University of Chinese Academy of Sciences, Beijing, 10039, China

    Yang Chen, Yichao Wang & Kuiyan Liu

  4. Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, 266071, China

    Yang Chen, Yichao Wang, Kuiyan Liu, Feng Liu & Nansheng Chen

  5. Department of Molecular Biology and Biochemistry, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, V5A 1S6, Canada

    Nansheng Chen

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Fig. S1

The collection sites of nine Pseudo-nitzschia pungens strains. In the Bohai Sea, five strains (CNS00110 and CNS00153 - CNS00156) were isolated from site A, and strain CNS00141 was isolated from site B. Strain CNS00055 was isolated from site C in the Jiaozhou Bay. In the East China Sea, strain CNS00089 was isolated from site D and strain CNS00043 was isolated from site E (PDF 1453 kb)

Fig. S2

Phylogenetic trees based on maximum likelihood (ML) analysis of five common markers 18S rDNA, 28S rDNA D1-3 domain, cox1, and rbcL. (a) ML phylogenetic tree based on the marker 18S rDNA; (b) ML phylogenetic tree based on the marker 28S rDNA D1-3 domain; (c) ML phylogenetic tree based on the marker cox1 partial sequence; (d) ML phylogenetic tree based on the marker rbcL (PDF 398 kb)

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Chen, Y., Wang, Y., Liu, K. et al. Development of a high-resolution molecular marker for tracking Pseudo-nitzschia pungens genetic diversity through comparative analysis of mitochondrial genomes. J Appl Phycol 33, 2283–2298 (2021). https://doi.org/10.1007/s10811-021-02461-9

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