Abstract
The Changjiang River Estuary (CRE) in the East China Sea suffers from seasonal hypoxia in summer. The vertical distributions and seasonal changes of microbial communities in the CRE were well documented. However, little is known about the diurnal changes of bacterial communities in the hypoxic zone of the CRE. Here, 16S rRNA gene analysis was used to explore the changes of bacterial communities in the oxic surface and hypoxic middle seawater layers during 24 h in the CRE. Significant differences between the hypoxic and oxic layers were observed: the phyla Cyanobacteria, Bacteroidetes and Acidimicrobiia were enriched in the oxic layer, whereas the phylum SAR406 and the class Deltaproteobacteria were more abundant in the hypoxic layer. In addition, some subtle diurnal variations of the bacterial relative abundance were found in both two layers. The relative abundance of Synechococcus increased at night, and this change was more obvious in the hypoxic layer. The similar trend was also found in some phototrophic and several heterotrophic bacteria, such as Rhodobacteraceae, OM60 and Flavobacteriaceae. Their relative abundances peaked at 16:00 in the oxic layer, while the relative abundances peaked at around 7:00 and decreased until 13:00 in the hypoxic layer. Together, the results of the present study suggest that some photosynthetic bacteria and several heterotrophic bacteria have similar diurnal variations implying the light and physicochemical heterogeneity in the course of a day are important for bacterial diurnal changes in the CRE.
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Ajani P A, Kahlke T, Siboni N, et al. 2018. The microbiome of the cosmopolitan diatom Leptocylindrus reveals significant spatial and temporal variability. Frontiers in Microbiology, 9: 2758, doi: https://doi.org/10.3389/fmicb.2018.02758
Alonso C, Warnecke F, Amann R, et al. 2007. High local and global diversity of Flavobacteria in marine plankton. Environmental Microbiology, 9(5): 1253–1266, doi: https://doi.org/10.1111/J.1462-2920.2007.01244.x
Alonso-Sáez L, Gasol J M. 2007. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in Northwestern Mediterranean coastal waters. Applied and Environmental Microbiology, 73(11): 3528–3535, doi: https://doi.org/10.1128/AEM.02627-06
Alonso-Sáez L, Gasol J M, Lefort T, et al. 2006. Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Applied and Environmental Microbiology, 72(9): 5806–5813, doi: https://doi.org/10.1128/AEM.00597-06
Béjà O, Aravind L, Koonin E V, et al. 2000. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science, 289(5486): 1902–1906, doi: https://doi.org/10.1126/science.289.5486.1902
Bernardet J F, Segers P, Vancanneyt M, et al. 1996. Cutting a Gordian knot: emended classification and description of the genus Flavobacterium, emended description of the family Flavobacteriaceae, and proposal of Flavobacterium hydatis nom. nov. (Basonym, Cytophaga aquatilis Strohl and Tait 1978). International Journal of Systematic Bacteriology, 46(1): 128–148, doi: https://doi.org/10.1099/00207713-46-1-128
Bianchi T S, Allison M A. 2009. Large-river delta-front estuaries as natural “recorders” of global environmental change. Proceedings of the National Academy of Sciences of the United States of America, 106(20): 8085–8092, doi: https://doi.org/10.1073/pnas.0812878106
Bouvier T, Del Giorgio P A. 2007. Key role of selective viral-induced mortality in determining marine bacterial community composition. Environmental Microbiology, 9(2): 287–297, doi: https://doi.org/10.1111/j.1462-2920.2006.01137.x
Bowman J P. 2014. The family Cryomorphaceae. In: Rosenberg E, De-Long E F, Lory S, et al., eds. The Prokaryotes: Other Major Lineages of Bacteria and the Archaea. Berlin, Heidelberg: Springer-Verlag, 539–550
Bray J R, Curtis J T. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs, 27(4): 325–349, doi: https://doi.org/10.2307/1942268
Broman E, Sachpazidou V, Pinhassi J, et al. 2017. Oxygenation of hypoxic coastal Baltic Sea sediments impacts on chemistry, microbial community composition, and metabolism. Frontiers in Microbiology, 8: 2453, doi: https://doi.org/10.3389/fmicb.2017.02453
Bryant D A. 1995. The molecular biology of cyanobacteria: Edited by Donald A. Bryant. 1994. 881 pp. Kluwer Academic Publishers, Dordrecht, The Netherlands. ISBN 0-7923-3222-9. Photosynthesis Research, 45(2): 177–179, doi: https://doi.org/10.1007/BF00032589
Campbell L G, Thrash J C, Rabalais N N, et al. 2019. Extent of the annual Gulf of Mexico hypoxic zone influences microbial community structure. PLoS One, 14(4): e0209055, doi: https://doi.org/10.1371/journal.pone.0209055
Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, doi: https://doi.org/10.1038/nmeth.f.303
Chauhan A, Cherrier J, Williams H N. 2009. Impact of sideways and bottom-up control factors on bacterial community succession over a tidal cycle. Proceedings of the National Academy of Sciences of the United States of America, 106(11): 4301–4306, doi: https://doi.org/10.1073/pnas.0809671106
Chen Chung-Chi, Gong Gwo-Ching, Shiah F K. 2007. Hypoxia in the East China Sea: one of the largest coastal low-oxygen areas in the world. Marine Environmental Research, 64(4): 399–408, doi: https://doi.org/10.1016/j.marenvres.2007.01.007
Chi Lianbao, Song Xiuxian, Yuan Yongquan, et al. 2017. Distribution and key influential factors of dissolved oxygen off the Changjiang River Estuary (CRE) and its adjacent waters in China. Marine Pollution Bulletin, 125(1–2): 440–450
Coleman M L, Hedrick D B, Lovley D R, et al. 1993. Reduction of Fe(III) in sediments by sulphate-reducing bacteria. Nature, 361(6411): 436–438, doi: https://doi.org/10.1038/361436a0
Conley D J, Carstensen J, Aigars J, et al. 2011. Hypoxia is increasing in the coastal zone of the Baltic Sea. Environmental Science & Technology, 45(16): 6777–6783
Cottrell M T, Kirchman D L. 2000. Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Applied and Environmental Microbiology, 66(4): 1692–1697, doi: https://doi.org/10.1128/AEM.66.4.1692-1697.2000
de Jesus Raposo M F, de Morais A M M B, de Morais R M S C. 2013. Bioactivity and applications of polysaccharides from marine microalgae. In: Ramawat K G, Mérillon J M, eds. Polysacharides: Bioactivity and Biotechnology. Cham: Springer International Publishing, 233–252
DeSantis T Z, Hugenholtz P, Larsen N, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72(7): 5069–5072, doi: https://doi.org/10.1128/AEM.03006-05
Devereux R, Mosher J J, Vishnivetskaya T A, et al. 2015. Changes in northern Gulf of Mexico sediment bacterial and archaeal communities exposed to hypoxia. Geobiology, 13(5): 478–493, doi: https://doi.org/10.1111/gbi.12142
Diaz R J. 2001. Overview of hypoxia around the world. Journal of Environmental Quality, 30(2): 275–281, doi: https://doi.org/10.2134/jeq2001.302275x
Diaz R J, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science, 321(5891): 926–929, doi: https://doi.org/10.1126/science.1156401
Dolan J R, Šimek K. 1999. Diel periodicity in Synechococcus populations and grazing by heterotrophic nanoflagellates: analysis of food vacuole contents. Limnology and Oceanography, 44(6): 1565–1570, doi: https://doi.org/10.4319/lo.1999.44.6.1565
Dong Yi, Zhao Yuan, Zhang Wenyan, et al. 2014. Bacterial diversity and community structure in the East China Sea by 454 sequencing of the 16S rRNA gene. Chinese Journal of Oceanology and Limnology, 32(3): 527–541, doi: https://doi.org/10.1007/s00343-014-3215-2
Drews G. 1981. Rhodospirillum salexigens, spec. nov., an obligatory halophilic phototrophic bacterium. Archives of Microbiology, 130(4): 325–327, doi: https://doi.org/10.1007/BF00425949
Edgar R C, Haas B J, Clemente J C, et al. 2011. Uchime improves sensitivity and speed of chimera detection. Bioinformatics, 27(16): 2194–2200, doi: https://doi.org/10.1093/bioinformatics/btr381
Elifantz H, Horn G, Ayon M, et al. 2013. Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiology Ecology, 85(2): 348–357, doi: https://doi.org/10.1111/15746941.12122
Fan Xin, Cheng Fangjin, Yu Zhiming, et al. 2019. The environmental implication of diatom fossils in the surface sediment of the Changjiang River Estuary (CRE) and its adjacent area. Journal of Oceanology and Limnology, 37(2): 552–567, doi: https://doi.org/10.1007/s00343-019-8037-9
Fuchs B M, Spring S, Teeling H, et al. 2007. Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 104(8): 2891–2896, doi: https://doi.org/10.1073/pnas.0608046104
Fuchs B M, Woebken D, Zubkov M V, et al. 2005. Molecular identification of picoplankton populations in contrasting waters of the Arabian Sea. Aquatic Microbial Ecology, 39(2): 145–157
Fuhrman J A, Eppley R W, Hagström Å, et al. 1985. Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern California Bight. Marine Ecology Progress Series, 27: 9–20, doi: https://doi.org/10.3354/meps027009
Füssel J, Lücker S, Yilmaz P, et al. 2017. Adaptability as the key to success for the ubiquitous marine nitrite oxidizer Nitrococcus. Science Advances, 3(11): e1700807, doi: https://doi.org/10.1126/sciadv.1700807
Gao Kunshan, Beardall J, Häder D P, et al. 2019. Effects of ocean acidification on marine photosynthetic organisms under the concurrent influences of warming, UV radiation, and deoxygenation. Frontiers in Marine Science, 6: 322, doi: https://doi.org/10.3389/fmars.2019.00322
Gao Xuelu, Song Jinming. 2005. Phytoplankton distributions and their relationship with the environment in the Changjiang Estuary, China. Marine Pollution Bulletin, 50(3): 327–335, doi: https://doi.org/10.1016/j.marpolbul.2004.11.004
Gao Xuelu, Song Jinming, Li Ning, et al. 2007. Spatial distribution and diurnal variation of chemical oxygen demand at the beginning of the rainy season in the Changjiang (Yangtze) River Estuary. Chinese Journal of Oceanology and Limnology, 25(3): 254–260, doi: https://doi.org/10.1007/s00343-007-0254-y
García F C, Calleja M L, Al-Otaibi N, et al. 2018. Diel dynamics and coupling of heterotrophic prokaryotes and dissolved organic matter in epipelagic and mesopelagic waters of the central Red Sea. Environmental Microbiology, 20(8): 2990–3000, doi: https://doi.org/10.1111/1462-2920.14336
General Administration of Quality Supervision Inspection and Quarantine, Standardization Administration of China. 2007. GB17378.5—2007. The specification for marine monitoring—Part 5: Sediment analysis (in Chinese). Beijing: Standards Press of China.
Gilbert J A, Field D, Swift P, et al. 2010. The taxonomic and functional diversity of microbes at a temperate coastal site: a “multi-omic” study of seasonal and diel temporal variation. PLoS One, 5(11): e15545, doi: https://doi.org/10.1371/journal.pone.0015545
Gómez-Pereira P R, Schüler M, Fuchs B M, et al. 2012. Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environmental Microbiology, 14(1): 52–66, doi: https://doi.org/10.1111/j.1462-2920.2011.02555.x
Gordon D A, Giovannoni S J. 1996. Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific Oceans. Applied and Environmental Microbiology, 62(4): 1171–1177, doi: https://doi.org/10.1128/AEM.62.4.1171-1177.1996
Grenz C, Denis L, Pringault O, et al. 2010. Spatial and seasonal variability of sediment oxygen consumption and nutrient fluxes at the sediment water interface in a sub-tropical lagoon (New Caledonia). Marine Pollution Bulletin, 61(7–12): 399–412
Guadayol Ò, Peters F, Marrasé C, et al. 2009. Episodic meteorological and nutrient-load events as drivers of coastal planktonic ecosystem dynamics: a time-series analysis. Marine Ecology Progress Series, 381: 139–155, doi: https://doi.org/10.3354/meps07939
Haro-Moreno J M, López-Pérez M, de la Torre J R, et al. 2018. Fine metagenomic profile of the Mediterranean stratified and mixed water columns revealed by assembly and recruitment. Microbiome, 6(1): 128, doi: https://doi.org/10.1186/s40168-018-0513-5
He Hui, Fu Lulu, Liu Qian, et al. 2019. Community structure, abundance and potential functions of bacteria and archaea in the Sansha Yongle Blue Hole, Xisha, South China Sea. Frontiers in Microbiology, 10: 2404, doi: https://doi.org/10.3389/fmicb.2019.02404
Hu Ping, Tom L, Singh A, et al. 2016. Genome-resolved metagenomic analysis reveals roles for candidate phyla and other microbial community members in biogeochemical transformations in oil reservoirs. mBio, 7(1): e01669–15
Isao K, Hara S, Terauchi K, et al. 1990. Role of sub-micrometre particles in the ocean. Nature, 345(6272): 242–244, doi: https://doi.org/10.1038/345242a0
Jacquet S, Lennon J F, Marie D, et al. 1998. Picoplankton population dynamics in coastal waters of the northwestern Mediterranean Sea. Limnology and Oceanography, 43(8): 1916–1931, doi: https://doi.org/10.4319/lo.1998.43.8.1916
Jessen G L, Lichtschlag A, Ramette A, et al. 2017. Hypoxia causes preservation of labile organic matter and changes seafloor microbial community composition (Black Sea). Science Advances, 3(2): e1601897, doi: https://doi.org/10.1126/sciadv.1601897
Jiao Nianzhi, Yang Yanhui, Koshikawa H, et al. 2002. Responses of picoplankton to nutrient perturbation in the South China Sea, with special reference to the coast-wards distribution of Prochlorococcus. Acta Botanica Sinica, 44(6): 731–739
Johan W, Rassoulzadegan F, Hagström Å. 1990. Periodic bacterivore activity balances bacterial growth in the marine environment. Limnology and Oceanography, 35(2): 313–324, doi: https://doi.org/10.4319/lo.1990.35.2.0313
Jørgensen B B, Bak F. 1991. Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Applied and Environmental Microbiology, 57(3): 847–856, doi: https://doi.org/10.1128/AEM.57.3.847-856.1991
Kirchman D L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology, 39(2): 91–100
Kirchman D L. 2008. Microbial Ecology of the Oceans. 2nd ed. Hoboken: John Wiley and Sons, 187–190
Kolber Z S, van Dover C L, Niederman R A, et al. 2000. Bacterial photosynthesis in surface waters of the open ocean. Nature, 407(6801): 177–179, doi: https://doi.org/10.1038/35025044
Lee S M, Chao Anne. 1994. Estimating population size via sample coverage for closed capture-recapture models. Biometrics, 50(1): 88–97, doi: https://doi.org/10.2307/2533199
Lefort T, Gasol J M. 2014. Short-time scale coupling of picoplankton community structure and single-cell heterotrophic activity in winter in coastal NW Mediterranean Sea waters. Journal of Plankton Research, 36(1): 243–258, doi: https://doi.org/10.1093/plankt/fbt073
Li Daoji, Zhang Jing, Huang Daji, et al. 2002. Oxygen depletion off the Changjiang (Yangtze River) estuary. Science in China Series D: Earth Sciences, 45(12): 1137–1146, doi: https://doi.org/10.1360/02yd9110
Lin Fengzhu, Wu Yulin, Yu Haicheng, et al. 2008. Phytoplankton community structure in the Changjiang Estuary and its adjacent waters in 2004. Oceanologia et Limnologia Sinica (in Chinese), 39(4): 401–410
Liu Jiwen, Fu Bingbing, Yang Hongmei, et al. 2015. Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients. Frontiers in Microbiology, 6: 64
Liu Min, Xiao Tian, Wu Ying, et al. 2012. Temporal distribution of bacterial community structure in the Changjiang Estuary hypoxia area and the adjacent East China Sea. Environmental Research Letters, 7(2): 025001, doi: https://doi.org/10.1088/1748-9326/7/2/025001
Liu Haijiao, Xue Bing, Feng Yuanyuan, et al. 2016. Size-fractionated chlorophyll a biomass in the northern South China Sea in summer 2014. Chinese Journal of Oceanology and Limnology, 34(4): 672–682, doi: https://doi.org/10.1007/s00343-016-5017-1
Llabrés M, Agustí S, Herndl G J. 2011. Diel in situ picophytoplankton cell death cycles coupled with cell division. Journal of Phycology, 47(6): 1247–1257, doi: https://doi.org/10.1111/j.1529-8817.2011.01072.x
Lohrenz S E, Redalje D G, Cai Weijun, et al. 2008. A retrospective analysis of nutrients and phytoplankton productivity in the Mississippi River plume. Continental Shelf Research, 28(12): 1466–1475, doi: https://doi.org/10.1016/j.csr.2007.06.019
Lou Xiulin, Hu Chuanmin. 2014. Diurnal changes of a harmful algal bloom in the East China Sea: observations from GOCI. Remote Sensing of Environment, 140: 562–572, doi: https://doi.org/10.1016/j.rse.2013.09.031
Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957–2963, doi: https://doi.org/10.1093/bioinformatics/btr507
Mann A J, Hahnke R L, Huang Sixing, et al. 2013. The genome of the alga-associated marine Flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides. Applied and Environmental Microbiology, 79(21): 6813–6822, doi: https://doi.org/10.1128/AEM.01937-13
Martha S, Fuchs B M, Rudolf A, et al. 2010. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environmental Microbiology, 11(8): 2078–2093. doi: https://doi.org/10.1111/j.1462-2920.2009.01929.x
McBride M, Xie G, Martens E C, et al. 2009. Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis. Applied and Environmental Microbiology, 75(21): 6864–6875, doi: https://doi.org/10.1128/AEM.01495-09
Naqvi S W A, Jayakumar D A, Narvekar P V, et al. 2000. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature, 408(6810): 346–349, doi: https://doi.org/10.1038/35042551
Oksanen J, Blanchet F G, Friendly M, et al. 2010. Vegan: community ecology package. R package version 2.5–7. http://CRAN.R-project.org/package=vegan [2020-11-28]
Olapade O A. 2012. Diel fluctuations in the abundance and community diversity of coastal bacterioplankton assemblages over a tidal cycle. Microbial Ecology, 63(1): 96–102, doi: https://doi.org/10.1007/s00248-011-9940-6
Olson R J, Chisholm S W, Zettler E R, et al. 1990. Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep Sea Research Part A: Oceanographic Research Papers, 37(6): 1033–1051, doi: https://doi.org/10.1016/0198-0149(90)90109-9
Ottesen E A, Young C R, Eppley J M, et al. 2013. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proceedings of the National Academy of Sciences of the United States of America, 110(6): E488–E497, doi: https://doi.org/10.1073/pnas.1222099110
Ottesen E A, Young C R, Gifford S M, et al. 2014. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science, 345(6193): 207–212, doi: https://doi.org/10.1126/science.1252476
Partensky F, Blanchot J, Lantoine F, et al. 1996. Vertical structure of picophytoplankton at different trophic sites of the tropical northeastern Atlantic Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 43(8): 1191–1213, doi: https://doi.org/10.1016/0967-0637(96)00056-8
Partensky F, Hess W R, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiology and Molecular Biology Reviews, 63(1): 106–127, doi: https://doi.org/10.1128/MMBR.63.1.106-127.1999
Pernthaler A, Pernthaler J. 2005. Diurnal variation of cell proliferation in three bacterial taxa from coastal North Sea waters. Applied and Environmental Microbiology, 71(8): 4638–4644, doi: https://doi.org/10.1128/AEM.71.8.4638-4644.2005
Pinhassi J, Sala M M, Havskum H, et al. 2004. Changes in bacterioplankton composition under different phytoplankton regimens. Applied and Environmental Microbiology, 70(11): 6753–6766, doi: https://doi.org/10.1128/AEM.70.11.6753-6766.2004
Pommier T, Neal P R, Gasol J M, et al. 2010. Spatial patterns of bacterial richness and evenness in the NW Mediterranean Sea explored by pyrosequencing of the 16S rRNA. Aquatic Microbial Ecology, 61(3): 221–233, doi: https://doi.org/10.3354/ame01484
Porter K G. 1996. Integrating the microbial loop and the classic food chain into a realistic planktonic food web. In: Polis G A, Winemiller K O, eds. Food Webs. Boston: Springer, 51–59
Pujalte M J, Lucena T, Ruvira M A, et al. 2014. The family Rhodobacteraceae. In: Rosenberg E, DeLong E F, Lory S, et al., eds. The Prokaryotes: Alphaproteobacteria and Betaproteobacteria. Berlin, Heidelberg: Springer, 439–512
Qin Qilong, Zhang Xiying, Wang Xumin, et al. 2010. The complete genome of Zunongwangia profunda SM-A87 reveals its adaptation to the deep-sea environment and ecological role in sedimentary organic nitrogen degradation. BMC Genomics, 11(1): 247, doi: https://doi.org/10.1186/1471-2164-11-247
Rabalais N N, Turner R E. 2001. Hypoxia in the northern Gulf of Mexico: description, causes and change. In: Rabalais N N, Turner R E, eds. Coastal Hypoxia: Consequences for Living Resources and Ecosystems. Washington: American Geophysical Union, 1–36
Rappé M S, Vergin K, Giovannoni S J. 2000. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiology Ecology, 33(3): 219–232, doi: https://doi.org/10.1111/j.1574-6941.2000.tb00744.x
Richardson T L, Jackson G A. 2007. Small phytoplankton and carbon export from the surface ocean. Science, 315(5813): 838–840, doi: https://doi.org/10.1126/science.1133471
Rinke C, Schwientek P, Sczyrba A, et al. 2013. Insights into the phylogeny and coding potential of microbial dark matter. Nature, 499(7459): 431–437, doi: https://doi.org/10.1038/nature12352
Ruiz-González C, Lefort T, Massana R, et al. 2012. Diel changes in bulk and single-cell bacterial heterotrophic activity in winter surface waters of the northwestern Mediterranean Sea. Limnology and Oceanography, 57(1): 29–42, doi: https://doi.org/10.4319/lo.2012.57.1.0029
Sato M, Horne J K, Parker-Stetter S L, et al. 2016. Hypoxia impacts on food web linkages in a pelagic ecosystem. https://ui.adsabs.harvard.edu/abs/2016AGUOSME24E0756S/abstract [2018-7-30]
Schattenhofer M, Fuchs B M, Amann R, et al. 2009. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environmental Microbiology, 11(8): 2078–2093, doi: https://doi.org/10.1111/j.1462-2920.2009.01929.x
Singh P, Teal T K, Marsh T L, et al. 2015. Intestinal microbial communities associated with acute enteric infections and disease recovery. Microbiome, 3(1): 45, doi: https://doi.org/10.1186/s40168-015-0109-2
Stevens H, Ulloa O. 2008. Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environmental Microbiology, 10(5): 1244–1259, doi: https://doi.org/10.1111/j.1462-2920.2007.01539.x
Stubner S. 2002. Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen™ detection. Journal of Microbiological Methods, 50(2): 155–164, doi: https://doi.org/10.1016/S0167-7012(02)00024-6
Suyama T, Shigematsu T, Suzuki T, et al. 2002. Photosynthetic apparatus in Roseateles depolymerans 61A is transcriptionally induced by carbon limitation. Applied and Environmental Microbiology, 68(4): 1665–1673, doi: https://doi.org/10.1128/AEM.68.4.1665-1673.2002
Synytsya A, Čopíková J, Kim W J, et al. 2015. Cell wall polysaccharides of marine algae. In: Kim S K, ed. Springer Handbook of Marine Biotechnology. Berlin: Springer, 543–590
Tang Kai, Lin Yingfan, Han Yu, et al. 2017. Characterization of potential polysaccharide utilization systems in the marine Bacteroidetes gramella flava JLT2011 using a multi-omics approach. Frontiers in Microbiology, 8: 220
Teeling H, Amann R. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science; 336(6081): 608–611, doi: https://doi.org/10.1126/science.1218344
ter Braak C J F, Smilauer P. 2002. Canoco reference manual and canodraw for windows user’s guide: software for canonical community ordination (version 4.5). Ithaca NY, USA: Microcomputer Power
Thrash J C, Seitz K W, Baker B J, et al. 2017. Metabolic roles of uncultivated bacterioplankton lineages in the northern Gulf of Mexico “dead zone”. mBio, 8(5): e01017–17
Turner R E, Rabalais N N, Justic D. 2008. Gulf of Mexico hypoxia: alternate states and a legacy. Environmental Science & Technology, 42(7): 2323–2327
Vaulot D, Marie D, Olson R J, et al. 1995. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science, 268(5216): 1480–1482, doi: https://doi.org/10.1126/science.268.5216.1480
Wang Lei, Zhong Chao, Liu Xin, et al. 2013. The comparative study on the diurnal variations of phytoplankton community between the northeastern South China Sea and the East China Sea in summer. Haiyang Xuebao (in Chinese), 35(6): 170–177
Wickham H, Chang W. 2009. ggplot2: an implementation of the grammar of graphics. R package version 0.7. https://www.researchgate.net/publication/245585126_ggplot2_An_Implementation_of_the_Grammar_of_Graphics [2018-6-30]
Wright J J, Konwar K M, Hallam S J. 2012. Microbial ecology of expanding oxygen minimum zones. Nature Reviews Microbiology, 10(6): 381–394, doi: https://doi.org/10.1038/nrmicro2778
Wright J J, Mewis K, Hanson N W, et al. 2014. Genomic properties of marine group a bacteria indicate a role in the marine sulfur cycle. The ISME Journal, 8(2): 455–468, doi: https://doi.org/10.1038/ismej.2013.152
Wu Dongmei, Dai Qiuping, Liu Xuezhu, et al. 2019. Comparison of bacterial community structure and potential functions in hypoxic and non-hypoxic zones of the Changjiang Estuary. PLoS One, 14(6): e0217431, doi: https://doi.org/10.1371/journal.pone.0217431
Yan Shi, Fuchs B M, Lenk S, et al. 2009. Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Systematic and Applied Microbiology, 32(2): 124–139, doi: https://doi.org/10.1016/j.syapm.2008.12.001
Yan Weijin, Yang Libiao, Wang Fang, et al. 2012. Riverine N2O concentrations, exports to estuary and emissions to atmosphere from the Changjiang River in response to increasing nitrogen loads. Global Biogeochemical Cycles, 26(4): GB4006
Yang Dezhou, Yin Baoshu, Liu Zhiliang, et al. 2012. Numerical study on the pattern and origins of Kuroshio branches in the bottom water of southern East China Sea in summer. Journal of Geophysical Research, 117(C2): C02014
Ye Qi, Wu Ying, Zhu Zhuoyi, et al. 2016. Bacterial diversity in the surface sediments of the hypoxic zone near the Changjiang Estuary and in the East China Sea. MicrobiologyOpen, 5(2): 323–339, doi: https://doi.org/10.1002/mbo3.330
Zhang J, Zhang Z F, Liu S M, et al. 1999. Human impacts on the large world rivers: would the Changjiang (Yangtze River) be an illustration?. Global Biogeochemical Cycles, 13(4): 1099–1105, doi: https://doi.org/10.1029/1999GB900044
Zheng Qiang, Wang Yu, Xie Rui, et al. 2017. Dynamics of heterotrophic bacterial assemblages within Synechococcus cultures. Applied and Environmental Microbiology, 84(3): e01517–17
Zhu Zhuoyi, Zhang Jing, Wu Ying, et al. 2011. Hypoxia off the Changjiang (Yangtze River) Estuary: oxygen depletion and organic matter decomposition. Marine Chemistry, 125(1–4): 108–116
Acknowledgements
We are grateful to all the staff who assisted in the field sampling. Particularly, we thank Xiaoyu Zhu from the Ocean University of China, Wu Qu from the Zhejiang Ocean University and Xiaomin Xia from the South China Sea Institute of Oceanology for their valuable comments and suggestions to improve the manuscript, and Elixigen (www.elixigen.com) for its linguistic assistance of this manuscript.
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Foundation item: The National Key R&D Program of China under contract No. 2019YFD0901305; the Science and Technology Program of Zhoushan under contract No. 2019C21011; the National Natural Science Foundation of China under contract Nos 31270160 and J1310037; the Natural Science Foundation of Zhejiang Province, China under contract No. LY12C03003; the Zhejiang Public Welfare Technology Application Research Project under contract No. 2016C33084; the Research Project of Ecological Environment Protection and Restoration of Yangtze River in Zhoushan under contract No. SZGXZS2020068.
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Huang, Y., Yuan, L., Fan, Y. et al. Diurnal changes in bacterial communities in oxic surface and hypoxic middle seawater layers of the Changjiang River Estuary. Acta Oceanol. Sin. 40, 92–106 (2021). https://doi.org/10.1007/s13131-021-1778-2
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DOI: https://doi.org/10.1007/s13131-021-1778-2