Cite this paper:
Hang LAI, Li ZHAO, Wen YANG, Regan NICHOLAUS, Betina LUKWAMBE, Jinyong ZHU, Zhongming ZHENG. Eukaryotic microbial distribution pattern and its potential effects on fisheries in the fish reserves of Qiantang River in breeding season[J]. Journal of Oceanology and Limnology, 2021, 39(2): 566-581

Eukaryotic microbial distribution pattern and its potential effects on fisheries in the fish reserves of Qiantang River in breeding season

Hang LAI1, Li ZHAO1, Wen YANG1, Regan NICHOLAUS1,2, Betina LUKWAMBE1,3, Jinyong ZHU1, Zhongming ZHENG1
1 School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Department of Natural Sciences, Mbeya University of Science and Technology, Mbeya 53000, Tanzania;
3 Department of Food Science and Technology, University of Dar es Salaam, Dar es Salaam 11000, Tanzania
Abstract:
To examine the eukaryotic biodiversity of aquatic ecosystems in the Qiantang River, China, eukaryotic microbes in the river were investigated using 18S rRNA gene sequencing during the breeding season (July to August 2018). Four distinct distribution patterns (1. Jiande; 2. Tonglu and Fuyang; 3. Jiubao; 4. Yanguan) of the microbial community and their potential effects on fishery activities were observed. Results show lower abundances of Dinophyta and Fungi and higher abundances of Cryptophyta and Chlorophyta in Tonglu and Fuyang than those in the other three sections. In addition, the reserves (Tonglu and Fuyang) destabilized the original eukaryotic microbial co-occurrence network. Among all the environmental factors measured, nitrogen (nitrite, nitrate, ammonium), water temperature and total chlorophyll a acted as major driving factors that controlled the eukaryotic microbial distribution. Furthermore, the existence of some algae (e.g., Chrysophyceae, Cryptophytes, and Chlorophyceae) and fungi (e.g., Rhizophydium) in Tonglu and Fuyang was beneficial to juvenile fish growth and water quality, although some detrimental species (e.g., Aphanomyces) needed attention. This study provides further insights into the sustainable protection and utilization of rivers.
Key words:    Qiantang River|fish reserves|18S rRNA|asymmetric eigenvector maps|molecular ecological network analyses|biological indicators   
Received: 2020-01-03   Revised: 2020-01-03
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Articles by Hang LAI
Articles by Li ZHAO
Articles by Wen YANG
Articles by Regan NICHOLAUS
Articles by Betina LUKWAMBE
Articles by Jinyong ZHU
Articles by Zhongming ZHENG
References:
Abell J M, Özkundakci D, Hamilton D P. 2010. Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes:implications for eutrophication control. Ecosystems, 13(7):966-977, https://doi.org/10.1007/s10021-010-9367-9.
Andrews S W, Gross E S, Hutton P H. 2017. Modeling salt intrusion in the San Francisco Estuary prior to anthropogenic influence. Cont. Shelf Res., 146:58-81, https://doi.org/10.1016/j.csr.2017.07.010.
Anthony E J, Brunier G, Besset M, Goichot M, Dussouillez P, Nguyen V L. 2015. Linking rapid erosion of the Mekong River delta to human activities. Sci. Rep., 5:14 745, https://doi.org/10.1038/srep14745.
Arrigo K R. 2004. Marine microorganisms and global nutrient cycles. Nature, 437(7057):349-355, https://doi.org/10.1038/nature04159.
Baird M E, Walker S J, Wallace B B, Webster I T, Parslow J S. 2003. The use of mechanistic descriptions of algal growth and zooplankton grazing in an estuarine eutrophication model. Estuar., Coast. Shelf Sci., 56(3-4):685-695, https://doi.org/10.1016/S0272-7714(02)00219-6.
Blanchet F G, Legendre P, Borcard D. 2008. Modelling directional spatial processes in ecological data. Ecol. Modell., 215(4):325-336, https://doi.org/10.1016/j.ecolmodel.2008.04.001.
Bokulich N A, Subramanian S, Faith J J, Gevers D, Gordon J I, Knight R, Mills D A, Caporaso J G. 2013. Qualityfiltering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods, 10(1):57-59, https://doi.org/10.1038/nmeth.2276.
Brown B L, Swan C M. 2010. Dendritic network structure constrains metacommunity properties in riverine ecosystems. J. Anim. Ecol., 79(3):571-580, https://doi.org/10.1111/j.1365-2656.2010.01668.x.
Chen J, Gao C, Zeng X F, Xiong M, Wang Y J, Jing C, Krysanova V, Huang J L, Zhao N, Su B D. 2017. Assessing changes of river discharge under global warming of 1.5℃ and 2℃ in the upper reaches of the Yangtze River Basin:approach by using multiple- GCMs and hydrological models. Quat. Int., 453:63-73, https://doi.org/10.1016/j.quaint.2017.01.017.
Chen W D, Ren K X, Isabwe A, Chen H H, Liu M, Yang J. 2019. Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome, 7:138, https://doi.org/10.1186/s40168-019-0749-8.
Chust G, Irigoien X, Chave J, Harris R P. 2013. Latitudinal phytoplankton distribution and the neutral theory of biodiversity. Global Ecol. Biogeogr., 22(5):531-543, https://doi.org/10.1111/geb.12016.
Clarke K R, Warwick R M. 2001. A further biodiversity index applicable to species lists:variation in taxonomic distinctness. Mar. Ecol. Prog. Ser., 216:265-278, https://doi.org/10.3354/meps216265.
Coyte K Z, Schluter J, Foster K R. 2015. The ecology of the microbiome:networks, competition, and stability. Science, 350(6261):663-666, https://doi.org/10.1126/science.aad2602.
De Nooijer L J, Toyofuku T, Kitazato H. 2009. Foraminifera promote calcification by elevating their intracellular pH. Proc. Natl. Acad. Sci. USA, 106(36):15 374-15 378, https://doi.org/10.1073/pnas.0904306106.
DeBoer J A, Webber C M, Dixon T A, Pope K L. 2016. The influence of a severe reservoir drawdown on springtime zooplankton and larval fish assemblages in Red Willow Reservoir, Nebraska. J. Freshwater Ecol., 31(1):131-146, https://doi.org/10.1080/02705060.2015.1055312.
Deng Y, Jiang Y H, Yang Y F, He Z L, Luo F, Zhou J Z. 2012. Molecular ecological network analyses. BMC Bioinf., 13:113, https://doi.org/10.1186/1471-2105-13-113.
Deng Y, Zhang P, Qin Y J, Tu Q C, Yang Y F, He Z L, Schadt C W, Zhou J Z. 2016. Network succession reveals the importance of competition in response to emulsified vegetable oil amendment for uranium bioremediation. Environ. Microbiol., 18(1):205-218, https://doi.org/10.1111/1462-2920.12981.
Duarte L N, Coelho F J R C, Cleary D F R, Bonifácio D, Martins P, Gomes N C M. 2019. Bacterial and microeukaryotic plankton communities in a semiintensive aquaculture system of sea bass (Dicentrarchus labrax):a seasonal survey. Aquaculture, 503:59-69, https://doi.org/10.1016/j.aquaculture.2018.12.066.
Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19):2 460-2 461, https://doi.org/10.1093/bioinformatics/btq461.
Faust K, Raes J. 2012. Microbial interactions:from networks to models. Nat. Rev. Microbiol., 10(8):538-550, https://doi.org/10.1038/nrmicro2832.
Foysal J, Lisa A K. 2018. Isolation and characterization of Bacillus sp. strain BC01 from soil displaying potent antagonistic activity against plant and fish pathogenic fungi and bacteria. J. Genet. Eng. Biotechnol., 16(2):387-392, https://doi.org/10.1016/j.jgeb.2018.01.005.
Frenken T, Alacid E, Berger S A, Bourne E C, Gerphagnon M, Grossart H P, Gsell A S, Ibelings B W, Kagami M, Küpper F C, Letcher P M, Loyau A, Miki T, Nejstgaard J C, Rasconi S, Reñé A, Rohrlack T, Rojas-Jimenez K, Schmeller D S, Scholz B, Seto K, Sime-Ngando T, Sukenik A, Van de Waal D B, Van den Wyngaert S, Van Donk E, Wolinska J, Wurzbacher C, Agha R. 2017. Integrating chytrid fungal parasites into plankton ecology:research gaps and needs. Environ. Microbiol., 19(10):3 802-3 822, https://doi.org/10.1111/1462-2920.13827.
Gong J, Dong J, Liu X H, Massana R. 2013. Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist, 164(3):369-379, https://doi.org/10.1016/j.protis.2012.11.006.
Guimerà R, Sales-Pardo M, Amaral L A N. 2007. Classes of complex networks defined by role-to-role connectivity profiles. Nat. Phys., 3(1):63-69, https://doi.org/10.1038/nphys489.
Hong B, Sun Z Z, Zhang Y P, Zeng Z C, Tian Z Q. 2009. Evaluation on effect of fishery resource enhancement and release in Huangpujiang upstream. Fish. Sci. Technol. Inf., 36(4):178-181. (in Chinese)
Hu A Y, Li S, Zhang L P, Wang H J, Yang J, Luo Z X, Rashid A, Chen S Q, Huang W X, Yu C P. 2018. Prokaryotic footprints in urban water ecosystems:a case study of urban landscape ponds in a coastal city, China. Environ. Pollut., 242:1 729-1 739, https://doi.org/10.1016/j.envpol.2018.07.097.
Huang Y L, Huang J L. 2019. Coupled effects of land use pattern and hydrological regime on composition and diversity of riverine eukaryotic community in a coastal watershed of Southeast China. Sci. Total Environ., 660:787-798, https://doi.org/10.1016/j.scitotenv.2019.01.063.
Huisman J, Matthijs H C P, Visser P M. 2005. Harmful Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3022-3.
Ibelings B W, De Bruin A, Kagami M, Rijkeboer M, Brehm M, Van Donk E. 2004. Host parasite interactions between freshwater phytoplankton and chytrid fungi(Chytridiomycota). J. Phycol., 40(3):437-453, https://doi.org/10.1111/j.1529-8817.2004.03117.x.
Isabwe A, Ren K X, Wang Y M, Peng F, Chen H H, Yang J. 2019. Community assembly mechanisms underlying the core and random bacterioplankton and microeukaryotes in a river-reservoir system. Water, 11(6):1127, https://doi.org/10.3390/w11061127.
Isabwe A, Yang J R, Wang Y M, Liu L M, Chen H H, Yang J. 2018. Community assembly processes underlying phytoplankton and bacterioplankton across a hydrologic change in a human-impacted river. Sci. Total Environ., 630:658-667, https://doi.org/10.1016/j.scitotenv.2018.02.210.
James T Y, Letcher P M, Longcore J E, Mozley-Standridge S E, Porter D, Powell M J, Griffith G W, Vilgalys R. 2006. A molecular phylogeny of the flagellated fungi(Chytridiomycota) and description of a new phylum(Blastocladiomycota). Mycologia, 98(6):860-871, https://doi.org/10.3852/mycologia.98.6.860.
Kinnula H, Mappes J, Valkonen J K, Pulkkinen K, Sundberg L R. 2017. Higher resource level promotes virulence in an environmentally transmitted bacterial fish pathogen. Evol. Appl., 10(5):462-470, https://doi.org/10.1111/eva.12466.
Lefèvre E, Roussel B, Amblard C, Sime-Ngando T. 2008. The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS One, 3(6):e2324, https://doi.org/10.1371/journal.pone.0002324.
Liu J, Soininen J, Han B P, Declerck S A J. 2013a. Effects of connectivity, dispersal directionality and functional traits on the metacommunity structure of river benthic diatoms. J. Biogeogr., 40(12):2 238-2 248, https://doi.org/10.1111/jbi.12160.
Liu L M, Chen H H, Liu M, Yang J R, Xiao P, Wilkinson D M, Yang J. 2019. Response of the eukaryotic plankton community to the cyanobacterial biomass cycle over 6
years in two subtropical reservoirs. ISME J., 13(9):2 196-2 208, https://doi.org/10.1038/s41396-019-0417-9.
Liu L M, Yang J, Lv H, Yu X Q, Wilkinson D M, Yang J. 2015. Phytoplankton communities exhibit a stronger response to environmental changes than bacterioplankton in three subtropical reservoirs. Environ. Sci. Technol., 49(18):10 850-10 858, https://doi.org/10.1021/acs.est.5b02637.
Liu L M, Yang J, Yu X Q, Chen G J, Yu Z. 2013b. Patterns in the composition of microbial communities from a subtropical river:effects of environmental, spatial and temporal factors. PLoS One, 8(11):e81232, https://doi.org/10.1371/journal.pone.0081232.
Lv H, Yang J, Liu L M. 2013. Temporal pattern prevails over spatial variability in phytoplankton communities from a subtropical water supply reservoir. Oceanol. Hydrobiol. Stud., 42(4):420-430, https://doi.org/10.2478/s13545-013-0098-3.
May R M. 2001. Stability and Complexity in Model Ecosystems. Princeton University Press, Princeton.
Meyers S D, Linville A J, Luther M E. 2014. Alteration of residual circulation due to large-scale infrastructure in a coastal plain estuary. Estuar. Coast., 37(2):493-507, https://doi.org/10.1007/s12237-013-9691-3.
Neutel A M, Heesterbeek J A P, Van De Koppel J, Hoenderboom G, Vos A, Kaldeway C, Berendse F, De Ruiter P C. 2007. Reconciling complexity with stability in naturally assembling food webs. Nature, 449(7162):599-602, https://doi.org/10.1038/nature06154.
Ortiz-Cañavate B K, Wolinska J, Agha R. 2019. Fungicides at environmentally relevant concentrations can promote the proliferation of toxic bloom-forming cyanobacteria by inhibiting natural fungal parasite epidemics. Chemosphere, 229:18-21, https://doi.org/10.1016/j.chemosphere.2019.04.203.
Peng B, Wang Y N, Zhang H J, Chen C, Luo H L, Wang M. 2019. Ecological assessment of phytoplankton community via microscopic method and 18S rRNA gene sequencing in Pearl River Estuary. E3S Web Conf., 131:01043, https://doi.org/10.1051/e3sconf/201913101043.
Priscu J C. 1995. Phytoplankton nutrient deficiency in lakes of the McMurdo Dry Valleys, Antarctica. Freshwater Biol., 34(2):215-227, https://doi.org/10.1111/j.1365-2427.1995.tb00882.x.
Saylor R K, Miller D L, Vandersea M W, Bevelhimer M S, Schofield P J, Bennett W A. 2010. Epizootic ulcerative syndrome caused by Aphanomyces invadans in captive bullseye snakehead Channa marulius collected from South Florida, USA. Dis. Aquat. Org., 88(2):169-175, https://doi.org/10.3354/dao02158.
Shade A, Peter H, Allison S D, Baho D L, Berga M, Bürgmann H, Huber D H, Langenheder S, Lennon J T, Martiny J B H, Matulich K L, Schmidt T M, Handelsman1 J. 2012. Fundamentals of microbial community resistance and resilience. Front. Microbiol., 3:417, https://doi.org/10.3389/fmicb.2012.00417.
Shetye S S, Kurian S, Naik H, Gauns M, Chndrasekhararao A V, Kumar A, Naik B. 2019. Variability of organic nitrogen and its role in regulating phytoplankton in the eastern Arabian Sea. Mar. Pollut. Bull., 141:550-560, https://doi.org/10.1016/j.marpolbul.2019.02.036.
Steele J A, Countway P D, Xia L, Vigil P D, Beman J M, Kim D Y, Chow C E T, Sachdeva R, Jones A C, Schwalbach M S, Rose J M, Hewson I, Patel A, Sun F Z, Caron D A, Fuhrman J A. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J., 5(9):1 414-1 425, https://doi.org/10.1038/ismej.2011.24.
Su Z F, Wu J M, Liu W Y, He J J, Xu J H. 2014. Study on assessment of enhancement effect of fishery stock in Changzhou City. Mod. Agric. Sci. Technol., (12):261-262, 264. (in Chinese with English abstract)
Sun W, Xia C Y, Xu M Y, Guo J, Sun G P, Wang A J. 2014. Community structure and distribution of planktonic ammonia-oxidizing Archaea and bacteria in the Dongjiang River, China. Res. Microbiol., 165(8):657-670, https://doi.org/10.1016/j.resmic.2014.08.003.
Tasevska O, Jersabek C D, Kostoski G, Gušeska D. 2012. Differences in rotifer communities in two freshwater bodies of different trophic degree (Lake Ohrid and Lake Dojran, Macedonia). Biologia, 67(3):565-572, https://doi.org/10.2478/s11756-012-0041-x.
Tong Y Y. 2001. Analysis on the status and constraints of fishery resources development and utilization in the lower reaches of the Qiantang River. Chin. Fish., (4):18-19. (in Chinese)
Vrebos D, Beauchard O, Meire P. 2017. The impact of land use and spatial mediated processes on the water quality in a river system. Sci. Total Environ., 601-602:365-373, https://doi.org/10.1016/j.scitotenv.2017.05.217.
Wan Y, Xu L L, Hu J, Xu C, Wan A, An S Q, Chen Y S. 2015. The role of environmental and spatial processes in structuring stream macroinvertebrates communities in a large river basin. Clean-Soil, Air, Water, 43(12):1 633-1 639, https://doi.org/10.1002/clen.201300861.
Wang Z H. 1995. Protection and exploition of fishery resources in the Qiantang River. Chin. J. Fish., 8(2):9-17, 8. (in Chinese)
Wen X L, Xi Y L, Qian F P, Zhang G, Xiang X L. 2011. Comparative analysis of rotifer community structure in five subtropical shallow lakes in East China:role of physical and chemical conditions. Hydrobiologia, 661(1):303-316, https://doi.org/10.1007/s10750-010-0539-6.
Xue Y Y, Chen H H, Yang J R, Liu M, Huang B Q, Yang J. 2018. Distinct patterns and processes of abundant and rare eukaryotic plankton communities following a reservoir cyanobacterial bloom. ISME J., 12(9):2 263-2 277, https://doi.org/10.1038/s41396-018-0159-0.
Zhang A J, Liu J D, Yang Y J, Guo A H, Gu Z M. 2016. Analysis of community characteristics of macrozoobenthos in enhancement and releasing zone in Tonglu section of Qiantang River. Acta Agric. Zhejiang, 28(8):1 323-1 331.(in Chinese with English abstract)
Zhang H J, Huang X L, Huang L, Bao F J, Xiong S L, Wang K, Zhang D M. 2018a. Microeukaryotic biogeography in the typical subtropical coastal waters with multiple environmental gradients. Sci. Total Environ., 635:618-628, https://doi.org/10.1016/j.scitotenv.2018.04.142.
Zhang K, Jiang F Y, Chen H, Dibar D T, Wu Q L, Zhou Z Z. 2019. Temporal and spatial variations in zooplankton communities in relation to environmental factors in four floodplain lakes located in the middle reach of the Yangtze River, China. Environ. Pollut., 251:277-284, https://doi.org/10.1016/j.envpol.2019.04.139.
Zhang X M, Wang X J, Tu Z, Zhang P D, Wang Y Z, Gao T X, Wang S J. 2009. Current status and prospect of fisheries resource enhancement in Shandong Province. Chin. Fish. Econ., 27(2):51-58. (in Chinese with English abstract)
Zhang Y Z, Zheng S J, Zhang W P. 2018b. The assessment of releasing and enhancement of fishery resources in the Qiantang River. J. Zhejiang Norm. Univ. (Nat. Sci.), 41(1):97-101. (in Chinese with English abstract)
Zhao K, Song K, Pan Y D, Wang L Z, Da L J, Wang Q X. 2017. Metacommunity structure of zooplankton in river networks:roles of environmental and spatial factors. Ecol. Indic., 73:96-104, https://doi.org/10.1016/j.ecolind.2016.07.026.
Zorzal-Almeida S, Salim A, Andrade M R M, de Novaes Nascimento M, Bini L M, Bicudo D C. 2018. Effects of land use and spatial processes in water and surface sediment of tropical reservoirs at local and regional scales. Sci. Total Environ., 644:237-246, https://doi.org/10.1016/j.scitotenv.2018.06.361.
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