Volume 39 Issue 4
Apr.  2020
Turn off MathJax
Article Contents
Huan Wang, Zhangxi Hu, Zhaoyang Chai, Yunyan Deng, Zifeng Zhan, Ying Zhong Tang. Blooms of Prorocentrum donghaiense reduced the species diversity of dinoflagellate community[J]. Acta Oceanologica Sinica, 2020, 39(4): 110-119. doi: 10.1007/s13131-020-1585-1
Citation: Huan Wang, Zhangxi Hu, Zhaoyang Chai, Yunyan Deng, Zifeng Zhan, Ying Zhong Tang. Blooms of Prorocentrum donghaiense reduced the species diversity of dinoflagellate community[J]. Acta Oceanologica Sinica, 2020, 39(4): 110-119. doi: 10.1007/s13131-020-1585-1

Blooms of Prorocentrum donghaiense reduced the species diversity of dinoflagellate community

doi: 10.1007/s13131-020-1585-1
Funds:  The National Natural Science Foundation of China under contract Nos 61533011 and 41776125; the NSFC-Shandong Joint Fund for Marine Ecology and Environmental Sciences under contract No. U1606404; the Scientific and Technological Innovation Project of the Qingdao National Laboratory for Marine Science and Technology under contract No. 2016ASKJ02; the National Key R&D Program of China under contract No. 2017YFC1404300; the Creative Team Project of the Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology under contract No. LMEES-CTSP-2018-1.
More Information
  • Corresponding author: E-mail: yingzhong.tang@qdio.ac.cn
  • Received Date: 2018-11-24
  • Accepted Date: 2019-02-19
  • Available Online: 2020-12-28
  • Publish Date: 2020-04-25
  • Most of reported harmful algal blooms (HABs) of microalgae (75%) have been caused by dinoflagellates. Studies on the negative effects of HABs have generally focused on animals, valuable organisms in particular, and environmental factors such as dissolved oxygen and nutrients, but relatively fewer on community level, particularly that using metagenomic approach. In this study, we reported an investigation on the effects of a HAB caused by the dinoflagellate Prorocentrum donghaiense on the species diversity and community structure of the dinoflagellate sub-community via a pyrosequencing approach for the samples taken before, during, and after the bloom season of P. donghaiense in the East China Sea. We sequenced partial 28S rRNA gene of dinoflagellates for the field samples and evaluated the species richness and diversity indices of the dinoflagellate community, as a sub-community of the total phytoplankton. We obtained 800 185 valid sequences (categorized into 560 operational taxonomic units, OTUs) of dinoflagellates from 50 samples and found that the biodiversity of dinoflagellate community was significantly reduced during the blooming period in comparison to that in pre- and after-blooming periods, as reflected in the four diversity indices: the species richness expressed as the number of OTUs, Chao1 index, Shannon index (evenness), and Gini-Simpson index. These four indices were all found to be negatively correlated to the cell density of the bloom species P. donghaiense. Correlation analyses also revealed that the P. donghaiense cell abundance was correlated negatively with ${\rm{NO}}_3^- $-N, and ${\rm{NO}}_2^- $-N, but positively with total nitrogen (TN) and total phosphorus (TP). Principal coordinates analysis (PCoA) showed that the community structure of dinoflagellates was markedly different among the different sampling periods, while the redundancy analysis (RDA) revealed P. donghaiense abundance, salinity, ${\rm{NO}}_3^- $-N, and ${\rm{SiO}}_3^{2-} $ were the most four significant factors shaping the dinoflagellate community structure. Our results together demonstrated that HABs caused by the dinoflagellate P. donghaiense could strongly impact the aquatic ecosystem on the sub-community level which the blooming species belongs to.
  • loading
  • [1]
    Anderson D M, Cembella A D, Hallegraeff G M. 2012. Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annual Review of Marine Science, 4: 143–176. doi: 10.1146/annurev-marine-120308-081121
    [2]
    Anderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25: 704–726. doi: 10.1007/BF02804901
    [3]
    Aranda M, Li Y, Liew Y J, et al. 2016. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Scientific Reports, 6: 39734. doi: 10.1038/srep39734
    [4]
    Burkholder J M, Azanza R V, Sako Y. 2006. The ecology of harmful dinoflagellates. In: Granéli E, Turner J T, eds. Ecology of Harmful Algae. Berlin, Heidelberg: Springer, 53–66
    [5]
    Chai Zhaoyang, He Zhili, Deng Yunyan, et al. 2018. Cultivation of seaweed Gracilaria lemaneiformis enhanced biodiversity in a eukaryotic plankton community as revealed via metagenomic analyses. Molecular Ecology, 27(4): 1081–1093. doi: 10.1111/mec.14496
    [6]
    Chai Zhaoyang, Wang Huan, Deng Yunyan, et al. 2020. Harmful algal blooms significantly reduce the resource use efficiency in a coastal plankton community. Science of The Total Environment, 704: 135381. doi: 10.1016/j.scitotenv.2019.135381
    [7]
    Cui Lei, Lu Xinxin, Dong Yuelei, et al. 2018. Relationship between phytoplankton community succession and environmental parameters in Qinhuangdao coastal areas, China: a region with recurrent brown tide outbreaks. Ecotoxicology and Environmental Safety, 159: 85–93. doi: 10.1016/j.ecoenv.2018.04.043
    [8]
    Ens E J, French K, Bremner J B. 2009. Evidence for allelopathy as a mechanism of community composition change by an invasive exotic shrub, Chrysanthemoides monilifera spp. rotundata. Plant and Soil, 316(1–2): 125–137. doi: 10.1007/s11104-008-9765-3
    [9]
    Felpeto A B, Roy S, Vasconcelos V M. 2018. Allelopathy prevents competitive exclusion and promotes phytoplankton biodiversity. Oikos, 127(1): 85–98. doi: 10.1111/oik.04046
    [10]
    Huse S M, Dethlefsen L, Huber J A, et al. 2008. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genetics, 4(11): e1000255. doi: 10.1371/journal.pgen.1000255
    [11]
    JOGFS International Project Office. 1994. JGOFS report No. 19. protocols for the Joint Global Ocean Flux Studies (JGOFS) core measurements. Bergen, Norway: JGOFS International Project Office, Center for Studies of Environment and Resources
    [12]
    Jonsson P R, Pavia H, Toth G. 2009. Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proceedings of the National Academy of Sciences of the United States of America, 106(27): 11177–11182. doi: 10.1073/pnas.0900964106
    [13]
    Landsberg J H. 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10(2): 113–390. doi: 10.1080/20026491051695
    [14]
    Leão P N, Ramos V, Vale M, et al. 2012. Microbial community changes elicited by exposure to cyanobacterial allelochemicals. Microbial Ecology, 63(1): 85–95. doi: 10.1007/s00248-011-9939-z
    [15]
    Leão P N, Vasconcelos M T S D, Vasconcelos V M. 2009. Allelopathy in freshwater cyanobacteria. Critical Reviews in Microbiology, 35(4): 271–282. doi: 10.3109/10408410902823705
    [16]
    Leflaive J, Ten-Hage L. 2007. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biology, 52(2): 199–214. doi: 10.1111/j.1365-2427.2006.01689.x
    [17]
    Legendre P, Oksanen J, ter Braak C J F. 2011. Testing the significance of canonical axes in redundancy analysis. Methods in Ecology and Evolution, 2(3): 269–277. doi: 10.1111/j.2041-210X.2010.00078.x
    [18]
    Li Hongmei, Tang Hongjie, Shi Xiaoyong, et al. 2014. Increased nutrient loads from the Changjiang (Yangtze) River have led to increased Harmful Algal Blooms. Harmful Algae, 39: 92–101. doi: 10.1016/j.hal.2014.07.002
    [19]
    Li Ji, Glibert P M, Zhou Mingjiang, et al. 2009. Relationships between nitrogen and phosphorus forms and ratios and the development of dinoflagellate blooms in the East China Sea. Marine Ecology Progress Series, 383: 11–26. doi: 10.3354/meps07975
    [20]
    Lin Senjie, Cheng Shifeng, Song Bo, et al. 2015. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science, 350(6261): 691–694. doi: 10.1126/science.aad0408
    [21]
    Lin Jianing, Yan Tian, Zhang Qingchun, et al. 2014. In situ detrimental impacts of Prorocentrum donghaiense blooms on zooplankton in the East China Sea. Marine Pollution Bulletin, 88(1–2): 302–310. doi: 10.1016/j.marpolbul.2014.08.026
    [22]
    Lu Douding, Goebel J, Qi Yuzao, et al. 2005. Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae, 4(3): 493–505. doi: 10.1016/j.hal.2004.08.015
    [23]
    Miao Yu, Wang Zhu, Liao Runhua, et al. 2017. Assessment of phenol effect on microbial community structure and function in an anaerobic denitrifying process treating high concentration nitrate wastewater. Chemical Engineering Journal, 330: 757–763. doi: 10.1016/j.cej.2017.08.011
    [24]
    Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical & Biological Methods for Seawater Analysis. Oxford: Pergamon Press, 423–453
    [25]
    Ptacnik R, Solimini A G, Andersen T, et al. 2008. Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences of the United States of America, 105(13): 5134–5138. doi: 10.1073/pnas.0708328105
    [26]
    Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz S A, eds. Bioinformatics Methods and Protocols. Totowa: Humana Press, 365-386
    [27]
    Schneider A R, Gommeaux M, Duclercq J, et al. 2017. Response of bacterial communities to Pb smelter pollution in contrasting soils. Science of the Total Environment, 605-606: 436–444. doi: 10.1016/j.scitotenv.2017.06.159
    [28]
    Smayda T J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In: Granéli E, Sundström B, Edler L, et al., eds. Toxic Marine Phytoplankton. New York, USA: Elsevier, 29–40
    [29]
    Smayda T J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography, 42: 1137–1153. doi: 10.4319/lo.1997.42.5_part_2.1137
    [30]
    State Oceanic Administration. 2001–2015. Bulletin of marine disaster of China (in Chinese). http://www.mnr.gov.cn/sj/sjfw/hy/gbgg/zghyzhgb [2019-12-03/2020-02-24]
    [31]
    Sun Zhen, Li Guoping, Wang Chengwei, et al. 2014. Community dynamics of prokaryotic and eukaryotic microbes in an estuary reservoir. Scientific Reports, 4: 6966
    [32]
    Sunagawa S, Coelho L P, Chaffron S, et al. 2015. Structure and function of the global ocean microbiome. Science, 348(6237): 1261359. doi: 10.1126/science.1261359
    [33]
    Valderrama J C. 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry, 10(2): 109–122. doi: 10.1016/0304-4203(81)90027-X
    [34]
    Vaulot D, Eikrem W, Viprey M, et al. 2008. The diversity of small eukaryotic phytoplankton (≤3 μm) in marine ecosystems. FEMS Microbiology Reviews, 32(5): 795–820. doi: 10.1111/j.1574-6976.2008.00121.x
    [35]
    West T L, Marshall H G, Tester P A. 1996. Natural phytoplankton community responses to a bloom of the toxic dinoflagellate Gymnodinium breve Davis off the North Carolina coast. Castanea, 61(4): 356–368
    [36]
    Xu Ning, Duan Shunshan, Li Aifen, et al. 2010. Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae, 9(1): 13–17. doi: 10.1016/j.hal.2009.06.002
    [37]
    Xu Xin, Yu Zhiming, Cheng Fangjin, et al. 2017. Molecular diversity and ecological characteristics of the eukaryotic phytoplankton community in the coastal waters of the Bohai Sea, China. Harmful Algae, 61: 13–22. doi: 10.1016/j.hal.2016.11.005
    [38]
    Yao Weiming, Li Chao, Gao Junzhang. 2006. Red tide plankton along the south coastal area in Zhejiang province. Marine Science Bulletin (in Chinese), 25(3): 87–91
    [39]
    Zhang Chuansong, Wang Jiangtao, Zhu Dedi, et al. 2008. The preliminary analysis of nutrients in harmful algal blooms in the East China Sea in the spring and summer of 2005. Haiyang Xuebao (in Chinese), 30(3): 153–159
    [40]
    Zhou Jin, Richlen M L, Sehein T R, et al. 2018. Microbial community structure and associations during a marine dinoflagellate bloom. Frontiers in Microbiology, 9: 1201. doi: 10.3389/fmicb.2018.01201
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(5)  / Tables(3)

    Article Metrics

    Article views (263) PDF downloads(5) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return