Spatial-temporal dynamics of bacterioplankton communities in the breeding area of large yellow croaker <i>Larimichthys crocea</i> in Sansha Bay, China -- Journal of Oceanology and Limnology,2023,41(4):1481-1492

	Cite this paper:
	Shizhan ZHENG, Shouheng ZHOU, Wen YANG, Betina LUKWAMBE, Regan NICHOLAUS, Jinyong ZHU, Zhongming ZHENG. Spatial-temporal dynamics of bacterioplankton communities in the breeding area of large yellow croaker Larimichthys crocea in Sansha Bay, China[J]. Journal of Oceanology and Limnology, 2023, 41(4): 1481-1492

Spatial-temporal dynamics of bacterioplankton communities in the breeding area of large yellow croaker Larimichthys crocea in Sansha Bay, China

Shizhan ZHENG^1,2, Shouheng ZHOU^1,2, Wen YANG^1,2, Betina LUKWAMBE³, Regan NICHOLAUS⁴, Jinyong ZHU^1,2, Zhongming ZHENG^1,2

1 School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Key Laboratory of Marine Bioengineering of Zhejiang Province, Ningbo University, Ningbo 315211, China;
3 School of Aquatic Sciences and Fisheries Technology, University of Dares Salaam, Dares Salaam 999132, Tanzania;
4 Department of Natural Sciences, Mbeya University of Science and Technology, Mbeya 53119, Tanzania

Abstract:

As an important spawning ground for large yellow croaker Larimichthys crocea, Sansha Bay, South China Sea has been a research hotspot. However, studies on the influence of the bacterioplankton community and assessments of its seasonal succession of bacterioplankton in different sea areas in Sansha Bay are still limited. To address the issue, we use 16S rRNA gene amplicon sequencing and functional prediction to investigate the spatial-temporal dynamics of the bacterioplankton community in three distinct areas, i.e., Breeding Area (BA), Yantian Harbor (YH), and Bay Margin (BM) of Sansha Bay. Results show that the structure of the bacterioplankton community in Sansha Bay had a significant seasonal succession. Moreover, the representative zero-radius Operation Taxon Units in different seasons were significantly different among the three selected sea areas. Specifically, during the breeding season, bacterioplankton communities in BA were characterized by compound-degrading bacteria, such as Rhodococcus and Owenweeksia, while in YH and BM, animal parasites or symbionts such as Vibrio and Arcobacter were dominant. Furthermore, the redundancy analysis and Spearman correlation analysis further explained that water temperature, dissolved oxygen, and ammonia nitrogen were the main environmental factors responsible for the difference. In addition, the bioindicator functions screened by Functional Annotation of Prokaryotic Taxa and random forest machine learning mainly relied on compound degradation, nitrite oxidation, and photoheterotrophy. The compound-degradation-corresponded bacterioplankton genera such as Rhodococcus had relatively higher abundance in BM, while Nitrospina corresponding to nitrite oxidation tended to be abundant in YH and BA. Based on the spatial and temporal variation in the composition and function of bacterioplankton, our findings provide a basis for understanding the theory of bacterioplankton community structure in the inner-bay habitat of the large yellow croaker in Sansha Bay.

Key words: microbial ecology|bacterioplankton|large yellow croaker|breeding area|functional prediction

Received: 2021-12-18 Revised:

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Articles by Shizhan ZHENG

Articles by Shouheng ZHOU

Articles by Wen YANG

Articles by Betina LUKWAMBE

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Articles by Jinyong ZHU

Articles by Zhongming ZHENG

References:
Brown M V, Ostrowski M, Grzymski J J et al. 2014. A trait based perspective on the biogeography of common and abundant marine bacterioplankton clades. Marine Genomics, 15: 17-28, https://doi.org/10.1016/j.margen. 2014.03.002.
Canion A, Prakash O, Green S J et al. 2013. Isolation and physiological characterization of psychrophilic denitrifying bacteria from permanently cold Arctic fjord sediments(Svalbard, Norway). Environmental Microbiology, 15(5):1606-1618, https://doi.org/10.1111/1462-2920.12110.
Caporaso J G, Lauber C L, Walters W A et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America, 108(S1): 4516-4522, https://doi.org/10.1073/pnas.10000 80107.
Chen Y J, Xu D P, Shi W G. 2015. Effects of environmental factors on behavior preference of aquatic animal.Chinese Agricultural Science Bulletin, 31(20): 18-24, https://doi.org/10.11924/j.issn.1000-6850.casb15010028.(in Chinese with English abstract)
Duarte L N, Coelho F J R C, Cleary D F R et al. 2019.Bacterial and microeukaryotic plankton communities in a semi-intensive 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. 2016. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, https://doi.org/10.1101/081257.
Enns A A, Vogel L J, Abdelzaher A M et al. 2012. Spatial and temporal variation in indicator microbe sampling is influential in beach management decisions. Water Research, 46(7): 2237-2246, https://doi.org/10.1016/j.watres.2012.01.040.
Fryer J L, Lannan C N, Garces L H et al. 1990. Isolation of a rickettsiales-like organism from diseased coho salmon(Oncorhynchus kisutch) in Chile. Fish Pathology, 25(2):107-114, https://doi.org/10.3147/jsfp.25.107.
Fuhrman J. 1992. Bacterioplankton roles in cycling of organic matter: the microbial food web. In: Falkowski P G, Woodhead A D, Vivirito K eds. Primary Productivity and Biogeochemical Cycles in the Sea. Springer, New York.p.361-383, https://doi.org/10.1007/978-1-4899-0762-2_20.
Fuhrman J A, Steele J A. 2008. Community structure of marine bacterioplankton: patterns, networks, and relationships to function. Aquatic Microbial Ecology, 53(1): 69-81, https://doi.org/10.3354/ame01222.
General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China, Standardization Administration. 2008. GB 17378.4-2007 The specification for marine monitoring—Part 4: seawater analysis. Beijing: Standards Press of China. (in Chinese)
Gómez-Pereira P R, Fuchs B M, Alonso C et al. 2010.Distinct Flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME Journal, 4(4):472-487, https://doi.org/10.1038/ismej.2009.142.
Ho H T K, Lipman L J A, Gaastra W. 2006. Arcobacter, what is known and unknown about a potential foodborne zoonotic agent! Veterinary Microbiology, 115(1-3): 1-13, https://doi.org/10.1016/j.vetmic.2006.03.004.
Hu C J, Xiong J B, Chen H P et al. 2015. Distribution of bacterioplankton communities in cage culture and noncultured areas of Xiangshan Bay, Ningbo, China. Acta Ecologica Sinica, 35(24): 8053-8061, https://doi.org/10.5846/stxb201406171263. (in Chinese with English abstract)
Huang M R. 2018. Study on Species Diversity of Marine Bacterial Community in Xiamen Coast and Predict Their Function. Xiamen University, Xiamen. (in Chinese with English abstract)
Jing X Y, Gou H L, Gong Y H et al. 2019. Seasonal dynamics of the coastal bacterioplankton at intensive fish-farming areas of the Yellow Sea, China revealed by highthroughput sequencing. Marine Pollution Bulletin, 139:366-375, https://doi.org/10.1016/j.marpolbul.2018.12.052.
Kan J J, Crump B C, Wang K et al. 2006. Bacterioplankton community in Chesapeake Bay: predictable or random assemblages. Limnology and Oceanography, 51(5):2157-2169, https://doi.org/10.4319/lo.2006.51.5.2157.
Kataoka T, Hodoki Y, Suzuki K et al. 2009. Tempo-spatial patterns of bacterial community composition in the western North Pacific Ocean. Journal of Marine Systems, 77(1-2): 197-207, https://doi.org/10.1016/j.jmarsys.2008. 12.006.
Levipan H A, Molina V, Fernandez C. 2014. Nitrospina-like bacteria are the main drivers of nitrite oxidation in the seasonal upwelling area of the eastern south pacific (central Chile ~36°S). Environmental Microbiology Reports, 6(6):565-573, https://doi.org/10.1111/1758-2229.12158.
Li X F, Xu J, Shi Z et al. 2019. Regulation of protist grazing on bacterioplankton by hydrological conditions in coastal waters. Estuarine, Coastal and Shelf Science, 218: 1-8, https://doi.org/10.1016/j.ecss.2018.11.013.
Lin H Y, Chen Z Z, Hu J Y et al. 2019. Impact of cage aquaculture on water exchange in Sansha Bay.Continental Shelf Research, 188: 103963, https://doi.org/10.1016/j.csr.2019.103963.
Liu J F. 2004. Study on twice maturity characteristic of cultured large yellow croaker in one year. Journal of Fujian Fisheries, (1): 4-8, https://doi.org/10.3969/j.issn. 1006-5601.2005.01.003. (in Chinese with English abstract)
Louca S, Parfrey L W, Doebeli M. 2016. Decoupling function and taxonomy in the global ocean microbiome.Science, 353(6305): 1272-1277, https://doi.org/10.1126/science.aaf4507.
Lücker S, Nowka B, Rattei T et al. 2013. The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Frontiers in Microbiology, 4: 27, https://doi.org/10.3389/fmicb.2013. 00027.
Murray A E, Peng V, Tyler C et al. 2011. Marine bacterioplankton biomass, activity and community structure in the vicinity of Antarctic icebergs. Deep-Sea Research Part II: Topical Studies in Oceanography, 58(11-12):1407-1421, https://doi.org/10.1016/j.dsr2.2010.11.021.
Partensky F, Blanchot J, Vaulot D. 1999. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Bulletin de l’Institut Océanographique, 19: 457-476.
Porsby C H, Nielsen K F, Gram L. 2008. Phaeobacter and Ruegeria species of the Roseobacter clade colonize separate niches in a Danish turbot (Scophthalmus maximus)-rearing farm and antagonize Vibrio anguillarum under different growth conditions. Applied and Environmental Microbiology, 74(23): 7356-7364, https://doi.org/10.1128/AEM.01738-08.
Prabagaran S R, Manorama R, Delille D et al. 2007.Predominance of Roseobacter, Sulfitobacter, Glaciecola and Psychrobacter in seawater collected off Ushuaia, Argentina, Sub-Antarctica. FEMS Microbiology Ecology, 59(2): 342-355, https://doi.org/10.1111/j.1574-6941.2006. 00213.x.
Prado S, Montes J, Romalde J L et al. 2009. Inhibitory activity of Phaeobacter strains against aquaculture pathogenic bacteria. International Microbiology, 12(2):107-114.
Qu C F, Song J M, Li N. 2014. Causes of jellyfish blooms and their influence on marine environment. Chinese Journal of Applied Ecology, 25(12): 3701-3712, https://doi.org/10.13287/j.1001-9332.20141009.005. (in Chinese with English abstract)
Shen C C. 2011. Fish community composition and diversity in Sansha Bay of Fujian. Marine Fisheries, 33(3): 258-264, https://doi.org/10.13233/j.cnki.mar.fish.2011.03.011.(in Chinese with English abstract)
Soelberg K K, Danielsen T K L, Martin-Iguacel R et al. 2020. Arcobacter butzleri is an opportunistic pathogen:recurrent bacteraemia in an immunocompromised patient without diarrhoea. Access Microbiology, 2(8):acmi000145, https://doi.org/10.1099/acmi.0.000145.
Sunagawa S, Coelho L P, Chaffron S et al. 2015. Structure and function of the global ocean microbiome. Science, 348(6237): 1261359, https://doi.org/10.1126/science.1261 359.
Tapia-Paniagua S T, Vidal S, Lobo C et al. 2014. The treatment with the probiotic Shewanella putrefaciens Pdp11 of specimens of Solea senegalensis exposed to high stocking densities to enhance their resistance to disease. Fish & Shellfish Immunology, 41(2): 209-221, https://doi.org/10.1016/j.fsi.2014.08.019.
Xie B, Huang J J, Huang C et al. 2020. Stable isotopic signatures (δ¹³C and δ¹⁵N) of suspended particulate organic matter as indicators for fish cage culture pollution in Sansha Bay, China. Aquaculture, 522: 735081, https://doi.org/10.1016/j.aquaculture.2020.735081.
Xie H Y. 2018. Risk Assessment of Harmful Algal Blooms:Taking Ningde Coast as an Example. Shanghai Ocean University, Shanghai. (in Chinese with English abstract)
Xiong J B, Chen H P, Hu C J et al. 2015. Evidence of bacterioplankton community adaptation in response to long-term mariculture disturbance. Scientific Reports, 5:15274, https://doi.org/10.1038/srep15274.
Xu J Y, Xu Z L. 2013. Seasonal succession of zooplankton in Sansha Bay, Fujian. Acta Ecologica Sinica, 33(5): 1413-1424, https://doi.org/10.5846/stxb201207241050. (in Chinese with English abstract)
Xu Z L, Chen J J. 2011. Analysis of migratory route of Larimichthys crocea in the East China Sea and Yellow Sea. Journal of Fisheries of China, 35(3): 429-437. (in Chinese with English abstract)
Yan Z C, Chen Y L. 1998. Habitat selection in animals.Chinese Journal of Ecology, 17(2): 43-49. (in Chinese)
Yang W, Zheng S Z, Zhou S H et al. 2020. Structure and functional diversity of Surface bacterioplankton communities in an overwintering habitat for large yellow croaker, Pseudosciaena crocea, of the southern East China Sea. Frontiers in Marine Science, 7: 472, https://doi.org/10.3389/fmars.2020.00472.
Zhang D M, Wang X, Xiong J B et al. 2014.Bacterioplankton assemblages as biological indicators of shrimp health status. Ecological Indicators, 38: 218-224, https://doi.org/10.1016/j.ecolind.2013.11.002.
Zhang L B, Yang H S. 2012. Advances in principles and techniques of marine habitat restoration and biological resource conservation. Chinese Bulletin of Life Sciences, 24(9): 1062-1069. (in Chinese with English abstract)
Zheng Y, Yang J M. 1965. Feeding habits of larva, and juvenile large yellow croaker in Zhejiang coastal waters. Oceanologia et Limnologia Sinica, 7(4): 355-372. (in Chinese with English abstract)
Zhou L, Wang P F, Huang S H et al. 2021. Environmental filtering dominates bacterioplankton community assembly in a highly urbanized estuarine ecosystem.Environmental Research, 96: 110934, https://doi.org/10.1016/j.envres.2021.110934.