Blooms of Prorocentrum donghaiense reduced the species diversity of dinoflagellate community
-
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.-
Key words:
- Prorocentrum donghaiense /
- dinoflagellate community /
- diversity /
- pyrosequencing /
- East China Sea
-
Figure 3. Relative abundance of the top 20 genera (a) and species (b) of dinoflagellates in the 50 samples. The abundance is presented as percentage of each taxon in the total reads of valid sequences of all dinoflagellates in a sample. Note that “others” indicates the total of all other taxa except for the top 20 taxa (genera or species), which will allow a 100 percentage for all taxa. The annotations “uncultured dinofalgellate” was the original annotation of a reference sequence in the GenBank that was not convincingly identified to any particular genus or species.
Table 1. Categorization of samples according to sampling timing (pre-, during, and after blooms) and locations
0331 Non-blooming 0422 Blooming 0503 Blooming 0513 Blooming 0531 Non-bloomig 0719 Non-blooming Sample ID A0331a A0422a E0503a A0513a A0531a A0719a A0331b A0422b E0503b A0513b A0531b A0719b B0331a B0422a A0503a B0513a B0531a B0719A B0331b B0422b A0503b B0513b B0531b B0719b C0331a C0422a B0503a C0513a C0531a C0719a C0331b C0422b B0503b C0513b C0531b C0719b D0331a D0422a C0503a D0513a D0531a D0719a D0331b D0422b C0503b D0513b D0531b D0719b D0503a D0503b Table 2. The ratio of dissolved inorganic nitrogen (DIN) to dissolved inorganic phosphorus (as
${\rm{PO}}_4^{3-} $ -P) (DIN/DIP)Date Max Min Mean±SD 0331 21.5 18.8 20.4±1.2 0422 17.8 4.0 8.3±6.4 0503 14.6 3.4 6.9±5.2 0513 5.8 3.4 4.1±1.2 0531 46.9 7.4 27.4±19.7 0719 9.9 4.7 7.0±2.2 Table 3. Correlations between P. donghaiense cell density and other environmental variables and diversity indices of dinoflagellate community, as measured with the rank correlation coefficient or Spearman’s rho
Number of OTUs Shannon-Wiener index Gini-Simpson index Chao1 index Spearman rho (p-level) Spearman rho (p-level) Spearman rho (p-level) Spearman rho (p-level) P. donghaiense vs. diversity indices –0.52 (<0.000 1***) –0.67 (<0.000 1***) –0.609 (0.001**) –0.37 (0.001**) Chl a vs. diversity indices –0.43 (0.031*) –0.51 (0.009*) –0.56 (0.004*) 0.01 (0.007**) Temperature vs. diversity indices 0.29 (0.156) 0.37 (0.069) 0.35 (0.088) 0.38 (0.059) Salinity vs. diversity indices 0.16 (0.452) 0.23 (0.26) 0.22 (0.0286*) 0.37 (0.069) Nitrite vs. diversity indices 0.62 (0.001**) 0.57 (0.003**) 0.53 (0.007**) 0.29 (0.15) Nitrate vs. diversity indices 0.48 (0.015*) 0.48 (0.013*) 0.48 (0.014*) 0.07 (0.756) TN vs. diversity indices –0.62 (0.001**) –0.72 (0.001**) –0.76 (0.001**) –0.43 (0.034*) TP vs. diversity indices –0.52 (0.007**) –0.64 (0.001**) –0.67 (<0.000 1***) 0.37 (0.73) Phosphate vs. diversity indices –0.009 (0.967) 0.01 (0.968) –0.01 (0.971) –0.29 (0.159) Ammonium vs. diversity indices 0.24 (0.328) 0.03 (0.900) –0.04 (0.85) 0.007 (0.97) Note: The sample sizes for all were 50 (n=50). * 0.01<p<0.05; ** 0.001<p<0.01; *** p<0.001. -
[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