Blooms of <i>Prorocentrum donghaiense</i> reduced the species diversity of dinoflagellate community

Huan Wang; Zhangxi Hu; Zhaoyang Chai; Yunyan Deng; Zifeng Zhan; Ying Zhong Tang

doi:10.1007/s13131-020-1585-1

Volume 39 Issue 4

Apr. 2020

Turn off MathJax

Article Contents

Abstract

References

Article Navigation > Acta Oceanologica Sinica > 2020 > 39(4): 110-119

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

Citation:

PDF( 688 KB)

Blooms of Prorocentrum donghaiense reduced the species diversity of dinoflagellate community

doi: 10.1007/s13131-020-1585-1

Huan Wang^{1, 3},
Zhangxi Hu^{1, 2, 4},
Zhaoyang Chai^{1, 2, 4},
Yunyan Deng^{1, 2, 4},
Zifeng Zhan⁵,
Ying Zhong Tang^{1, 2, 4
,
,}

1.
CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
2.
Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
3.
University of Chinese Academy of Sciences, Beijing 100049, China
4.
Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
5.
Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China

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

Abstract

Abstract

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.
- Prorocentrum donghaiense,
- dinoflagellate community,
- diversity,
- pyrosequencing,
- East China Sea

FullText(HTML)

References(40)

References

[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

Relative Articles

Relative Articles

Supplements(0)

Cited By

Cited by

Periodical cited type(16)

1.	Zhe Tao, Xiaohan Liu, Xiaoying Song, et al. Species and genetic diversity of notorious dinoflagellates Pfiesteria piscicida, Luciella masanensis, and relatives in marine sediments of China. Harmful Algae, 2024, 140: 102746. doi:10.1016/j.hal.2024.102746
2.	Huatao Yuan, Ling Li, Yujie Wang, et al. Succession of diversity, assembly mechanisms, and activities of the microeukaryotic community throughout Scrippsiella acuminata (Dinophyceae) bloom phases. Harmful Algae, 2024, 134: 102626. doi:10.1016/j.hal.2024.102626
3.	Yu Jin Kim, Hyun-Jung Kim, Taek-Kyun Lee, et al. Determining ecological interactions of key dinoflagellate species using an intensive metabarcoding approach in a semi-closed coastal ecosystem of South Korea. Harmful Algae, 2024, 138: 102698. doi:10.1016/j.hal.2024.102698
4.	Gao Meng, Zhao Chen, Yuzhen Wang, et al. Effect of Picochlorum sp. addition on water quality, microalgae community composition and production performance in the culture of Litopenaeus vannamei. Aquaculture International, 2024, 32(7): 10159. doi:10.1007/s10499-024-01655-5
5.	Hao Wang, Alexander F. Bouwman, Junjie Wang, et al. Competitive advantages of HAB species under changing environmental conditions in the coastal waters of the Bohai Sea, Yellow Sea and East China Sea. Continental Shelf Research, 2023, 259: 104991. doi:10.1016/j.csr.2023.104991
6.	Hao Wang, Alexander F. Bouwman, Junjie Wang, et al. Competitive Advantages of Hab Species Under Changing Environmental Conditions in the Coastal Waters of the Bohai Sea, Yellow Sea and East China Sea. SSRN Electronic Journal, 2022. doi:10.2139/ssrn.4123868
7.	You Zhou, Jiyun She, Xiongmei Zhu. Dynamic analysis of biodiversity, carbon storage and environmental factors of coniferous forest in Loudi City, Hunan Province. International Journal of Low-Carbon Technologies, 2022, 17: 831. doi:10.1093/ijlct/ctac037
8.	Liyan He, Zhiming Yu, Jianan Zhu, et al. Nanostructure and Nanomechanics of Prorocentrum donghaiense and Their Changes Under Nitrogen Limitation by Atomic Force Microscopy. Frontiers in Marine Science, 2022, 9 doi:10.3389/fmars.2022.874888
9.	Yongjun Wei, Shan Jiang, Lingmin Tian, et al. Benthic microbial biogeography along the continental shelf shaped by substrates from the Changjiang River plume. Acta Oceanologica Sinica, 2022, 41(1): 118. doi:10.1007/s13131-021-1861-8
10.	Jinju Ma, Chunyun Zhang, Fuguo Liu, et al. Easy detection of Prorocentrum donghaiense by polymerase chain reaction-nucleic acid chromatography strip. Environmental Science and Pollution Research, 2022, 30(4): 10346. doi:10.1007/s11356-022-22856-6
11.	Bi‐Lin Lai, Zhi‐Hui Xiao, Peng‐Yang Jiang, et al. Two‐Dimensional Ag−Fe−N/C Nanosheets as Efficient Cathode Catalyst to Improve Power‐Generation Performance of Microbial Fuel Cells. ChemElectroChem, 2022, 9(6) doi:10.1002/celc.202101699
12.	Zhangxi Hu, Yuyang Liu, Yunyan Deng, et al. The Notorious Harmful Algal Blooms-Forming Dinoflagellate Prorocentrum donghaiense Produces Sexual Resting Cysts, Which Widely Distribute Along the Coastal Marine Sediment of China. Frontiers in Marine Science, 2022, 9 doi:10.3389/fmars.2022.826736
13.	Zhangxi Hu, Ning Xu, Haifeng Gu, et al. Morpho-molecular description of a new HAB species, Pseudocochlodinium profundisulcus gen. et sp. nov., and its LSU rRNA gene based genetic diversity and geographical distribution. Harmful Algae, 2021, 108: 102098. doi:10.1016/j.hal.2021.102098
14.	Yuyang Liu, Zhangxi Hu, Yunyan Deng, et al. Dependence of genome size and copy number of rRNA gene on cell volume in dinoflagellates. Harmful Algae, 2021, 109: 102108. doi:10.1016/j.hal.2021.102108
15.	Jihen Elleuch, Mohamed Barkallah, Kirsty F. Smith, et al. Quantitative PCR assay for the simultaneous identification and enumeration of multiple Karenia species. Environmental Science and Pollution Research, 2020, 27(29): 36889. doi:10.1007/s11356-020-09739-4
16.	Tiantian Chen, Yun Liu, Sha Xu, et al. Variation of Amoebophrya community during bloom of Prorocentrum donghaiense Lu in coastal waters of the East China Sea. Estuarine, Coastal and Shelf Science, 2020, 243: 106887. doi:10.1016/j.ecss.2020.106887