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Metabarcoding analysis of the composition and spatial–temporal dynamics of Pseudo-nitzschia species in Jiaozhou Bay, China

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Abstract

Pseudo-nitzschia is a species-rich genus with many species able to induce harmful algae blooms (HABs) associated with the toxin, domoic acid (DA), production. Despite their high diversity revealed by taxonomical studies, the composition and spatial–temporal dynamics of Pseudo-nitzschia species in marine ecological systems are often inadequately resolved due to the insufficient resolution associated with morphology-based approaches applied in ecological studies. In this study, metabarcoding analysis was applied to identify Pseudo-nitzschia species and track their spatial–temporal dynamics in Jiaozhou Bay (JZB), a model marine ecosystem located in Qingdao, China. This metabarcoding analysis potentially uncovered 18 Pseudo-nitzschia species, including three Pseudo-nitzschia species identified in JZB in previous microscopy-based studies, four Pseudo-nitzschia species (P. micropora, P. multistriata, P. galaxiae, and P. fraudulenta) that have not been identified in JZB, and 11 potential Pseudo-nitzschia species whose molecular marker sequences are identical, demonstrating the strength of metabarcoding analysis in ecological research. Furthermore, this metabarcoding analysis also revealed differential spatial–temporal dynamics of many Pseudo-nitzschia species. While P. galaxiae was found to show a strong preference for summer months, P. pungens showed relatively high abundance in later summer and early autumn, P. delicatissima and P. multistriata showed higher abundance in autumn and winter, and P. micropora was more common in July. To ascertain driving forces for such differential seasonal preferences, we evaluated the impact of environmental factors on the spatial–temporal preferences of the Pseudo-nitzschia species, which revealed that temperature and other factors together contributed to the differential dynamic changes. This study demonstrated that metabarcoding analysis is an effective approach for tracking the composition and spatial–temporal dynamics of Pseudo-nitzschia species in marine ecological systems.

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Data availability

The sequencing results (raw data) have been submitted to NCBI, and the BioProject numbers are PRJNA577777 and PRJNA733859.

References

  • Ajani PA, Larsson ME, Woodcock S, Rubio A, Farrell H, Brett S, Murray SA (2020) Fifteen years of Pseudo-nitzschia in an Australian estuary, including the first potentially toxic P. delicatissima bloom in the southern hemisphere. Estuar Coast Shelf Sci 236:106651

  • Baird DJ, Hajibabaei M (2012) Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next-generation DNA sequencing. Mol Ecol 21:2039–2044

    PubMed  Google Scholar 

  • Barkallah M, Elleuch J, Smith KF, Chaari S, Ben Neila I, Fendri I, Michaud P, Abdelkafi S (2020) Development and application of a real-time PCR assay for the sensitive detection of diarrheic toxin producer Prorocentrum lima. J Microbiol Meth 178:106081

    CAS  Google Scholar 

  • Bates SS, Bird CJ, Defreitas ASW, Foxall R, Gilgan M, Hanic LA, Johnson GR, Mcculloch AW, Odense P, Pocklington R, Quilliam MA, Sim PG, Smith JC, Rao DVS, Todd ECD, Walter JA, Wright JLC (1989) Pennate diatom Nitzschia-Pungens as the primary source of domoic acid, a toxin in shellfish from Eastern Prince Edward Island, Canada. Can J Fish Aquat Sci 46:1203–1215

    CAS  Google Scholar 

  • Bates SS, Hubbard KA, Lundholm N, Montresor M, Leaw CP (2018) Pseudo-nitzschia, Nitzschia, and domoic acid: new research since 2011. Harmful Algae 79:3–43

    PubMed  Google Scholar 

  • Bresnan E, Arevalo F, Belin C, Branco MAC, Cembella AD, Clarke D, Correa J, Davidson K, Dhanji-Rapkova M, Lozano RF, Fernandez-Tejedor M, Guofinnsson H, Carbonell DJ, Laza-Martinez A, Lemoine M, Lewis AM, Menedez LM, Maskrey BH, McKinney A, Pazos Y, Revilla M, Siano R, Silva A, Swan S, Turner AD, Schweibold L, Provoost P, Enevoldsen H (2021) Diversity and regional distribution of harmful algal events along the Atlantic margin of Europe. Harmful Algae 102:101976

    CAS  PubMed  Google Scholar 

  • Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643

    PubMed  PubMed Central  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Meth 13:581–583

    CAS  Google Scholar 

  • Chen N, Chen Y (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (II): the East China Sea (Chinese with English abstract). Oceanol Limnol Sinica 52:363–384

    CAS  Google Scholar 

  • Chen N, Cui Z, Xu Q (2021a) Advances in the study of biodiversity of phytoplankton and red tide species in China (IV): the Changjiang Estuary (Chinese with English abstract). Oceanol Limnol Sinica 52:402–417

    ADS  Google Scholar 

  • Chen N, Huang H (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (I): the Bohai Sea (Chinese with English abstract). Oceanol Limnol Sinica 52:346–362

    Google Scholar 

  • Chen N, Zhang M (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (III): the South China Sea (Chinese with English abstract). Oceanol Limnol Sinica 52:385–401

    Google Scholar 

  • Chen XM, Pang JX, Huang CX, Lundholm N, Teng ST, Li A, Li Y (2021b) Two new and nontoxigenic Pseudo-nitzschia species (Bacillariophyceae) from Chinese southeast coastal waters. J Phycol 57:335–344

    CAS  PubMed  Google Scholar 

  • Chen Y, Wang Y, Liu K, Liu F, Chen N (2021c) 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

    CAS  Google Scholar 

  • Cipolletta F, Russo AA, D’Alelio D, Margiotta F, Sarno D, Zingone A, Montresor M (2022) Vertical distribution of Pseudo-nitzschia in the Gulf of Naples across the seasons. Med Mar Sci 23:525–535

    Google Scholar 

  • Clark S, Hubbard KA, Anderson DM, McGillicuddy DJ Jr, Ralston DK, Townsend DW (2019) Pseudo-nitzschia bloom dynamics in the Gulf of Maine: 2012–2016. Harmful Algae 88:101656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clement MJ, Snell Q, Walker P, Posada D, Crandall KA (2002) TCS: Estimating Gene Genealogies, 16th International Parallel and Distributed Processing Symposium (IPDPS 2002), 15–19 April 2002, Fort Lauderdale, FL, USA, CD-ROM/Abstracts Proceedings

  • Delegrange A, Lefebvre A, Gohin F, Courcot L, Vincent D (2018) Pseudo-nitzschia sp. diversity and seasonality in the southern North Sea, domoic acid levels and associated phytoplankton communities. Estuar Coast Shelf Sci 214:194–206

    CAS  ADS  Google Scholar 

  • Dermastia TT, Cerino F, Stankovic D, France J, Ramsak A, Tusek MZ, Beran A, Natali V, Cabrini M, Mozetič P (2020) Ecological time series and integrative taxonomy unveil seasonality and diversity of the toxic diatom Pseudo-nitzschia H. Peragallo in the northern Adriatic Sea. Harmful Algae 93:101773

  • Dong HC, Lundholm N, Teng ST, Li AF, 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

    CAS  PubMed  Google Scholar 

  • Downes-Tettmar N, Rowland S, Widdicombe C, Woodward M, Llewellyn C (2013) Seasonal variation in Pseudo-nitzschia spp. and domoic acid in the Western English Channel. Cont Shelf Res 53:40–49

    ADS  Google Scholar 

  • Fu ZX, Piumsomboon A, Punnarak P, Uttayarnmanee P, Leaw CP, Lim PT, Wang AJ, Gu HF (2021) Diversity and distribution of harmful microalgae in the Gulf of Thailand assessed by DNA metabarcoding. Harmful Algae 106:102063

    CAS  PubMed  Google Scholar 

  • Giulietti S, Romagnoli T, Campanelli A Totti C, Accoroni S (2021) Ecology and seasonality of Pseudo-nitzschia species (Bacillariophyceae) in the northwestern Adriatic Sea over a 30-year period (1988-2020). Med Mar Sci 22:505-520

  • Gong W, Marchetti A (2019) Estimation of 18S gene copy number in marine eukaryotic plankton using a next-generation sequencing approach. Front Mar Sci 6:219

    Google Scholar 

  • Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, Boutte C, Burgaud G, de Vargas C, Decelle J, del Campo J, Dolan JR, Dunthorn M, Edvardsen B, Holzmann M, Kooistra WHCF, Lara E, Le Bescot N, Logares R, Mahe F, Massana R, Montresor M, Morard R, Not F, Pawlowski J, Probert I, Sauvadet AL, Siano R, Stoeck T, Vaulot D, Zimmermann P, Christen R (2013) The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41:D597–D604

    CAS  PubMed  Google Scholar 

  • Guiry MD, Guiry GM (2022) AlgaeBase. World-wide Electronic Publication, National University of Ireland, Galway. Accessed at https://www.algaebase.org on 2022–08–30

  • Guo S, Zhu M, Zhao Z, Liang J, Zhao Y, Du J, Sun X (2019) Spatial-temporal variation of phytoplankton community structure in Jiaozhou Bay, China. J Oceanol Limnol 37:1611–1624

    CAS  Google Scholar 

  • Harrison JG, John Calder W, Shuman B, Alex Buerkle C (2021) The quest for absolute abundance: The use of internal standards for DNA-based community ecology. Mol Ecol Resour 21:30–43

    PubMed  Google Scholar 

  • He Z, Chen Y, Wang Y, Liu K, Xu Q, Li Y, Chen N (2022) Comparative analysis of Pseudo-nitzschia chloroplast genomes revealed extensive inverted region variation and Pseudo-nitzschia speciation. Front Mar Sci 9:784579

    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

    CAS  PubMed  Google Scholar 

  • Husson B, Hernández-Fariñas T, Le Gendre R, Schapira M, Chapelle A (2016) Two decades of Pseudo-nitzschia spp. blooms and king scallop (Pecten maximus) contamination by domoic acid along the French Atlantic and English Channel coasts: Seasonal dynamics, spatial heterogeneity and interannual variability. Harmful Algae 51:26–39

    CAS  PubMed  Google Scholar 

  • Keck F, Vasselon V, Tapolczai K, Rimet F, Bouchez A (2017) Freshwater biomonitoring in the Information Age. Front Ecol Environ 15:266–274

    Google Scholar 

  • Kolde R, Kolde MR (2015) Package 'pheatmap'. R Package 1:790

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    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

    CAS  Google Scholar 

  • Li Y (2006) Ecological characteristics and taxonomic studies on nano-diatoms in coastal waters of China. Doctor Thesis, Xiamen University

  • Li Y, Dong HC, Teng ST, Bates SS, Lim PT (2018) Pseudo-nitzschia nanaoensis sp. nov. (Bacillariophyceae) from the Chinese coast of the South China Sea. J Phycol 54:918–922

    CAS  PubMed  Google Scholar 

  • Li Y, Huang CX, Xu GS, Lundholm N, Teng ST, Wu H, Tan Z (2017) Pseudo-nitzschia simulans sp. nov. (Bacillariophyceae), the first domoic acid producer from Chinese waters. Harmful Algae 67:119–130

    CAS  PubMed  Google Scholar 

  • Lin Y, Gifford S, Ducklow H, Schofield O, Cassar N (2019) Towards quantitative microbiome community profiling using internal standards. Appl Environ Microbiol 85:e02634-e2618

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Liu DY, Jiang JJ, Wang Y, Zhang Y, Di BP (2012) Large scale northward expansion of warm water species Skeletonema tropicum (Bacillariophyceae) in China seas. Chin J Oceanol Limnol 30:519–527

    Google Scholar 

  • Liu FG, Zhang CY, Wang YY, Chen GF (2022a) A review of the current and emerging detection methods of marine harmful microalgae. Sci Total Environ 815:152913

    CAS  PubMed  ADS  Google Scholar 

  • Liu S, Chen N (2021) Advances in biodiversity analysis of phytoplankton and harmful algal bloom species in Jiaozhou Bay (Chinese with English abstract). Mar Sci 45:170–188

    Google Scholar 

  • Liu S, Cui Z, Zhao Y, Chen N (2022b) Composition and spatial-temporal dynamics of phytoplankton community shaped by environmental selection and interactions in the Jiaozhou Bay. Water Res 218:118488

    CAS  PubMed  Google Scholar 

  • Liu S, Gibson K, Cui Z, Chen Y, Sun X, Chen N (2020) Metabarcoding analysis of harmful algal species in Jiaozhou Bay. Harmful Algae 92:101772

    CAS  PubMed  Google Scholar 

  • Lundholm N, Churro C, Fraga S, Hoppenrath M, Iwataki M, Larsen J, Mertens K, Moestrup Ø, Zingone A (2009) IOC-UNESCO taxonomic reference list of harmful micro algae. Accessed at http://www.marinespecies.org/hab on 2022–08–23

  • Luo M, Ji Y, Warton D, Yu DW (2023) Extracting abundance information from DNA-based data. Mol Ecol Resour 23:174–189

    CAS  PubMed  Google Scholar 

  • Lü S, Li Y, Lundholm N, Ma Y, Ho K (2012) Diversity, taxonomy and biogeographical distribution of the genus Pseudo-nitzschia (Bacillariophyceae) in Guangdong coastal waters, South China Sea. Nova Hedwigia 95:123–152

    Google Scholar 

  • Madeira F, Pearce M, Tivey ARN, Basutkar P, Lee J, Edbali O, Madhusoodanan N, Kolesnikov A, Lopez R (2022) Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res 50:W276–W279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17:10–12

    Google Scholar 

  • McCabe RM, Hickey BM, Kudela RM, Lefebvre KA, Adams NG, Bill BD, Gulland FMD, Thomson RE, Cochlan WP, Trainer VL (2016) An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett 43:10366–10376

    PubMed  PubMed Central  ADS  Google Scholar 

  • Niu BB, Zheng QX, Liu Y, Lundholm N, Teng ST, Lu XD, Ran RW, Zhang L, Li Y (2023) Morphology, molecular phylogeny and biogeography revealed two new Pseudo‐nitzschia (Bacillariophyceae) species in Chinese waters. J Syst Evol (Early view version)

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: community ecology package, version 2:0–10. http://CRAN.R-project.org/package=vegan

  • Percopo I, Ruggiero MV, Sarno D, Longobardi L, Rossi R, Piredda R, Zingone A (2022) Phenological segregation suggests speciation by time in the planktonic diatom Pseudo-nitzschia allochrona sp. nov. Ecol Evol 12:e9155

  • Qian S, Wang X, Chen G (1983) The phytoplankton of the Jiaozhou Bay (Chinese with English abstract). J Shandong Ocean Univ 13:39–56

    Google Scholar 

  • Qian GD, Han HY, Liu J, Liang SK, Shi XY, Wang XL (2009) Spatiotemporal changes of main chemical pollutants for the last thirty years in the Jiaozhou Bay (Chinese with English abstract). Period Ocean Univ China 39:781–788

    Google Scholar 

  • Qiao L, Liang S, Song D, Wu W, Wang XH (2019) Jiaozhou Bay. In: Wang XH (ed) Sediment Dynamics of Chinese Muddy Coasts and Estuaries. Academic Press, Amsterdam, pp 5–23

    Google Scholar 

  • Quijano-Scheggia SI, Garcés E, Lundholm N, Moestrup Ø, Andree K, Camp J (2009) Morphology, physiology, molecular phylogeny and sexual compatibility of the cryptic Pseudo-nitzschia delicatissima complex (Bacillariophyta), including the description of P. arenysensis sp. nov. Phycologia 48:492–509

    CAS  Google Scholar 

  • Rees HC, Maddison BC, Middleditch DJ, Patmore JRM, Gough KC (2014) The detection of aquatic animal species using environmental DNA - a review of eDNA as a survey tool in ecology. J Appl Ecol 51:1450–1459

    CAS  Google Scholar 

  • Revelle W (2016) psych: Procedures for Psychological, Psychometric, and Personality Research. Northwestern University, Evanston, Illinois. R package version 1.6.12

  • Ruggiero MV, Kooistra WH, Piredda R, Sarno D, Zampicinini G, Zingone A, Montresor M (2022) Temporal changes of genetic structure and diversity in a marine diatom genus discovered via metabarcoding. Environ DNA 4:763–775

    CAS  Google Scholar 

  • Saeed AF, Awan SA, Ling SM, Wang RZ, Wang S (2017) Domoic acid: Attributes, exposure risks, innovative detection techniques and therapeutics. Algal Res 24:97–110

    Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shelton AO, Gold ZJ, Jensen AJ, D’Agnese E, Andruszkiewicz Allan E, Van Cise A, Gallego R, Ramón-Laca A, Garber-Yonts M, Parsons K (2023) Toward quantitative metabarcoding. Ecology 104:e3906

    PubMed  Google Scholar 

  • SOA (1989–2021) State Oceanic Administration: Marine Disaster Bulletin (1989–2021). Accessed at https://www.mnr.gov.cn/sj/sjfw/hy/gbgg/zghyzhgb on 2022–08–30

  • Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:21–31

    CAS  PubMed  Google Scholar 

  • Thessen AE, Dortch Q, Parsons ML, Morrison W (2005) Effect of salinity on Pseudo-nitzschia species (Bacillariophyceae) growth and distribution. J Phycol 41:21–29

    Google Scholar 

  • Totti C, Romagnoli T, Accoroni S, Coluccelli A, Pellegrini M, Campanelli A, Grilli F, Marini M (2019) Phytoplankton communities in the northwestern Adriatic Sea: Interdecadal variability over a 30-years period (1988–2016) and relationships with meteoclimatic drivers. J Mar Syst 193:137–153

    Google Scholar 

  • 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

    Google Scholar 

  • Trebitz AS, Hoffman JC, Darling JA, Pilgrim EM, Kelly JR, Brown EA, Chadderton WL, Egan SP, Grey EK, Hashsham SA, Klymus KE, Mahon AR, Ram JL, Schultz MT, Stepien CA, Schardt JC (2017) Early detection monitoring for aquatic non-indigenous species: Optimizing surveillance, incorporating advanced technologies, and identifying research needs. J Environ Manage 202:299–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang Y, Wang Y, Liu DY (2013) Spatial and temporal characteristics of phytoplankton and its relation with the environmental factors in Jiaozhou Bay (Chinese with English abstract). J Saf Environ 13:163–170

    Google Scholar 

  • Yao Y, Chen N (2021) Biodiversity of phytoplankton and red tide species in the Pearl River Estuary (Chinese with English abstract). Mar Sci 45:75–90

    Google Scholar 

  • Zheng S, Sun X, Zhao Y, Sun S (2014) Annual variation of species composition and abundance distribution of phytoplankton in 2010 in the Jiaozhou Bay (Chinese with English abstract). Mar Sci 38:1–6

    CAS  ADS  Google Scholar 

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Acknowledgements

We are grateful to colleagues from the Jiaozhou Bay Marine Ecosystem Research Station for the opportunity to participate in the investigation expeditions. Data analysis was supported by Oceanographic Data Center, IOCAS.

Funding

This research was supported by the Natural Science Foundation of China (42176162, 41906118), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB42000000), the Chinese Academy of Sciences Pioneer Hundred Talents Program (to Nansheng Chen), the Taishan Scholar Project Special Fund (to Nansheng Chen), the Qingdao Innovation and Creation Plan (Talent Development Program—5th Annual Pioneer and Innovator Leadership Award to Nansheng Chen, 19–3-2–16-zhc), and the Natural Sciences and Engineering Research Council of Canada (NSERC).

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Z.H. ,S.L. and N.C. designed the research. Z.H. drafted the manuscript. N.C. revised the manuscript. S.L., Z.C. and Y.Z. assisted with the samples collection. Z.H. and S.L. conducted the data analysis. All authors reviewed the manuscript.

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Correspondence to Nansheng Chen.

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He, Z., Liu, S., Cui, Z. et al. Metabarcoding analysis of the composition and spatial–temporal dynamics of Pseudo-nitzschia species in Jiaozhou Bay, China. J Appl Phycol 36, 259–272 (2024). https://doi.org/10.1007/s10811-023-03127-4

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