Volume 42 Issue 8
Aug.  2023
Turn off MathJax
Article Contents
Xiaogang Chen, Qi Ye, Jinzhou Du, Neven Cukrov, Nuša Cukrov, Yan Zhang, Ling Li, Jing Zhang. Linking bacterial and archaeal community dynamics to related hydrological, geochemical and environmental characteristics between surface water and groundwater in a karstic estuary[J]. Acta Oceanologica Sinica, 2023, 42(8): 158-170. doi: 10.1007/s13131-023-2185-7
Citation: Xiaogang Chen, Qi Ye, Jinzhou Du, Neven Cukrov, Nuša Cukrov, Yan Zhang, Ling Li, Jing Zhang. Linking bacterial and archaeal community dynamics to related hydrological, geochemical and environmental characteristics between surface water and groundwater in a karstic estuary[J]. Acta Oceanologica Sinica, 2023, 42(8): 158-170. doi: 10.1007/s13131-023-2185-7

Linking bacterial and archaeal community dynamics to related hydrological, geochemical and environmental characteristics between surface water and groundwater in a karstic estuary

doi: 10.1007/s13131-023-2185-7
Funds:  The National Key R&D Program of China under contract No. 2022YFE0209300; the National Natural Science Foundation of China under contract No. 42006152; the Zhejiang Provincial Natural Science Foundation of China under contract No. LQ21D060005; the 111 Project under contract No. BP0820020.
More Information
  • Corresponding author: qye@sklec.ecnu.edu.cn
  • Received Date: 2022-10-27
  • Accepted Date: 2023-03-11
  • Available Online: 2023-06-08
  • Publish Date: 2023-08-31
  • Subterranean estuaries (STEs) are characterized by the mixing of terrestrial fresh groundwater and seawater in coastal aquifers. Although microorganisms are important components of coastal groundwater ecosystems and play critical roles in biogeochemical transformations in STEs, limited information is available about how their community dynamics interact with hydrological, geochemical and environmental characteristics in STEs. Here, we studied bacterial and archaeal diversities and distributions with 16S rRNA-based Illumina MiSeq sequencing technology between surface water and groundwater in a karstic STE. Principal-coordinate analysis found that the bacterial and archaeal communities in the areas where algal blooms occurred were significantly separated from those in other stations without algal bloom occurrence. Canonical correspondence analysis showed that nutrients and salinity can explain the patterns of bacterial and archaeal community dynamics. The results suggest that hydrological, geochemical and environmental characteristics between surface water and groundwater likely control the bacterial and archaeal diversities and distributions in STEs. Furthermore, we found that some key species can utilize terrestrial pollutants such as nitrate and ammonia in STEs, indicating that these species (e.g., Nitrosopumilus maritimus, Limnohabitans parvus and Simplicispira limi) may be excellent candidates for in situ degradation/remediation of coastal groundwater contaminations concerned with the nitrate and ammonia. Overall, this study reveals the coupling relationship between the microbial communities and hydrochemical environments in STEs, and provides a perspective of in situ degradation/remediation for coastal groundwater quality management.
  • loading
  • Adolf J E, Burns J, Walker J K, et al. 2019. Near shore distributions of phytoplankton and bacteria in relation to submarine groundwater discharge-fed fishponds, Kona coast, Hawai’i, USA. Estuarine, Coastal and Shelf Science, 219: 341–353,
    Adyasari D, Hassenrück C, Montiel D, et al. 2020. Microbial community composition across a coastal hydrological system affected by submarine groundwater discharge (SGD). PLoS ONE, 15(6): e0235235. doi: 10.1371/journal.pone.0235235
    Adyasari D, Hassenrück C, Oehler T, et al. 2019. Microbial community structure associated with submarine groundwater discharge in northern Java (Indonesia). Science of the Total Environment, 689: 590–601. doi: 10.1016/j.scitotenv.2019.06.193
    Altschul S F, Madden T L, Schäffer A A, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17): 3389–3402. doi: 10.1093/nar/25.17.3389
    Archana A, Francis C A, Boehm A B. 2021. The beach aquifer microbiome: research gaps and data needs. Frontiers in Environmental Science, 9: 653568. doi: 10.3389/fenvs.2021.653568
    Bishop R E, Humphreys W F, Cukrov N, et al. 2015. ‘Anchialine’ redefined as a subterranean estuary in a crevicular or cavernous geological setting. Journal of Crustacean Biology, 35(4): 511–514. doi: 10.1163/1937240X-00002335
    Boehm A B, Shellenbarger G G, Paytan A. 2004. Groundwater discharge: potential association with fecal indicator bacteria in the surf zone. Environmental Science & Technology, 38(13): 3558–3566. doi: 10.1021/es035385a
    Bonacci O, Jukić D, Ljubenkov I. 2006. Definition of catchment area in karst: case of the rivers Krčić and Krka, Croatia. Hydrological Sciences Journal, 51(4): 682–699. doi: 10.1623/hysj.51.4.682
    Cai Pinghe, Shi Xiangming, Hong Qingquan, et al. 2015. Using 224Ra/228Th disequilibrium to quantify benthic fluxes of dissolved inorganic carbon and nutrients into the Pearl River Estuary. Geochimica et Cosmochimica Acta, 170: 188–203. doi: 10.1016/j.gca.2015.08.015
    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: 10.1038/nmeth.f.303
    Cardenas M B, Rodolfo R S, Lapus M R, et al. 2020. Submarine groundwater and vent discharge in a volcanic area associated with coastal acidification. Geophysical Research Letters, 47(1): e2019GL085730. doi: 10.1029/2019GL085730
    Chaudhary D K, Kim J. 2016. Novosphingobium naphthae sp. nov., from oil-contaminated soil. International Journal of Systematic and Evolutionary Microbiology, 66(8): 3170–3176. doi: 10.1099/ijsem.0.001164
    Chen Xiaogang, Cukrov N, Santos I R, et al. 2020a. Karstic submarine groundwater discharge into the Mediterranean: radon-based nutrient fluxes in an anchialine cave and a basin-wide upscaling. Geochimica et Cosmochimica Acta, 268: 467–484. doi: 10.1016/j.gca.2019.08.019
    Chen Xiaogang, Du Jinzhou, Yu Xueqing, et al. 2021a. Porewater-derived dissolved inorganic carbon and nutrient fluxes in a saltmarsh of the Changjiang River Estuary. Acta Oceanologica Sinica, 40(8): 32–43. doi: 10.1007/s13131-021-1797-z
    Chen Xiaogang, Lao Yanling, Wang Jinlong, et al. 2018a. Submarine groundwater-borne nutrients in a tropical bay (Maowei Sea, China) and their impacts on the oyster aquaculture. Geochemistry, Geophysics, Geosystems, 19(3): 932–951,
    Chen Xiaogang, Santos I R, Call M, et al. 2021b. The mangrove CO2 pump: tidally driven pore-water exchange. Limnology and Oceanography, 66(4): 1563–1577. doi: 10.1002/lno.11704
    Chen Xiaogang, Santos I R, Hu Duofei, et al. 2022. Pore-water exchange flushes blue carbon from intertidal saltmarsh sediments into the sea. Limnology and Oceanography Letters, 7(4): 312–320. doi: 10.1002/lol2.10236
    Chen Xiaogang, Ye Qi, Du Jinzhou, et al. 2019. Bacterial and archaeal assemblages from two size fractions in submarine groundwater near an industrial zone. Water, 11(6): 1261. doi: 10.3390/w11061261
    Chen Xiaogang, Ye Qi, Sanders C J, et al. 2020b. Bacterial-derived nutrient and carbon source-sink behaviors in a sandy beach subterranean estuary. Marine Pollution Bulletin, 160: 111570. doi: 10.1016/j.marpolbul.2020.111570
    Chen Xiaogang, Zhang Fenfen, Lao Yanling, et al. 2018b. Submarine groundwater discharge-derived carbon fluxes in mangroves: an important component of blue carbon budgets?. Journal of Geophysical Research: Oceans, 123(9): 6962–6979,
    Chen Xiaogang, Zhu Peiyuan, Zhang Yan, et al. 2023. Plum rain enhances porewater greenhouse gas fluxes and weakens the acidification buffering potential in saltmarshes. Journal of Hydrology, 616: 128686. doi: 10.1016/j.jhydrol.2022.128686
    DeLong E F, Karl D M. 2005. Genomic perspectives in microbial oceanography. Nature, 437(7057): 336–342. doi: 10.1038/nature04157
    Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998. doi: 10.1038/nmeth.2604
    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: 10.1093/bioinformatics/btr381
    Guo Xiaoyi, Xu Bochao, Burnett W C, et al. 2020. Does submarine groundwater discharge contribute to summer hypoxia in the Changjiang (Yangtze) River Estuary?. Science of the Total environment, 719: 137450,
    Huang Laibin, Bae H S, Young C, et al. 2021. Campylobacterota dominate the microbial communities in a tropical karst subterranean estuary, with implications for cycling and export of nitrogen to coastal waters. Environmental Microbiology, 23(11): 6749–6763. doi: 10.1111/1462-2920.15746
    Hwang D W, Lee Y W, Kim G. 2005. Large submarine groundwater discharge and benthic eutrophication in Bangdu Bay on volcanic Jeju Island, Korea. Limnology and Oceanography, 50(5): 1393–1403. doi: 10.4319/lo.2005.50.5.1393
    Jiang Shan, Zhang Yixue, Jin Jie, et al. 2020. Organic carbon in a seepage face of a subterranean estuary: turnover and microbial interrelations. Science of the Total Environment, 725: 138220. doi: 10.1016/j.scitotenv.2020.138220
    Kasalický V, Jezbera J, Šimek K, et al. 2010. Limnohabitans planktonicus sp. nov. and Limnohabitans parvus sp. nov., planktonic Betaproteobacteria isolated from a freshwater reservoir, and emended description of the genus Limnohabitans. International Journal of Systematic and Evolutionary Microbiology, 60(12): 2710–2714. doi: 10.1099/ijs.0.018952-0
    Knee K L, Layton B A, Street J H, et al. 2008. Sources of nutrients and fecal indicator bacteria to nearshore waters on the north shore of Kaua’i (Hawai’i, USA). Estuaries and Coasts, 31(4): 607–622. doi: 10.1007/s12237-008-9055-6
    Kraft B, Jehmlich N, Larsen M, et al. 2022. Oxygen and nitrogen production by an ammonia-oxidizing archaeon. Science, 375(6576): 97–100. doi: 10.1126/science.abe6733
    Kwokal Ž, Cukrov N, Cuculić V. 2014. Natural causes of changes in marine environment: mercury speciation and distribution in anchialine caves. Estuarine, Coastal and Shelf Science, 151: 10–20,
    Lecher A L, Mackey K R M. 2018. Synthesizing the effects of submarine groundwater discharge on marine biota. Hydrology, 5(4): 60. doi: 10.3390/hydrology5040060
    Lee E, Shin D, Hyun S P, et al. 2017. Periodic change in coastal microbial community structure associated with submarine groundwater discharge and tidal fluctuation. Limnology and Oceanography, 62(2): 437–451. doi: 10.1002/lno.10433
    Li Aihua, Liu Hongcan, Hou Weiguo, et al. 2016. Pseudorhodobacter sinensis sp. nov. and Pseudorhodobacter aquaticus sp. nov., isolated from crater lakes. International Journal of Systematic and Evolutionary Microbiology, 66(8): 2819–2824. doi: 10.1099/ijsem.0.001061
    Liu Qian, Charette M A, Henderson P B, et al. 2014. Effect of submarine groundwater discharge on the coastal ocean inorganic carbon cycle. Limnology and Oceanography, 59(5): 1529–1554. doi: 10.4319/lo.2014.59.5.1529
    Liu Jianan, Hrustić E, Du Jinzhou, et al. 2019. Net submarine groundwater-derived dissolved inorganic nutrients and carbon input to the oligotrophic stratified karstic estuary of the Krka River (Adriatic Sea, Croatia). Journal of Geophysical Research: Oceans, 124(6): 4334–4349. doi: 10.1029/2018JC014814
    Lu Shipeng, Ryu S H, Chung B S, et al. 2007. Simplicispira limi sp. nov., isolated from activated sludge. International Journal of Systematic and Evolutionary Microbiology, 57(1): 31–34. doi: 10.1099/ijs.0.64566-0
    Martens-Habbena W, Qin W. 2022. Archaeal nitrification without oxygen. Science, 375(6576): 27–28. doi: 10.1126/science.abn0373
    Mayfield K K, Eisenhauer A, Ramos D P S, et al. 2021. Groundwater discharge impacts marine isotope budgets of Li, Mg, Ca, Sr, and Ba. Nature Communications, 12(1): 148. doi: 10.1038/s41467-020-20248-3
    Moore W S. 1999. The subterranean estuary: a reaction zone of ground water and sea water. Marine Chemistry, 65(1–2): 111–125,
    Park S, Kim S, Jung Y T, et al. 2016. Marivivens donghaensis gen. nov., sp. nov., isolated from seawater. International Journal of Systematic and Evolutionary Microbiology, 66(2): 666–672. doi: 10.1099/ijsem.0.000772
    Pires A C C, Cleary D F R, Almeida A, et al. 2012. Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Applied and Environmental Microbiology, 78(16): 5520–5528. doi: 10.1128/AEM.00386-12
    Pitt A, Schmidt J, Koll U, et al. 2019. Aquirufa antheringensis gen. nov., sp. nov. and Aquirufa nivalisilvae sp. nov., representing a new genus of widespread freshwater bacteria. International Journal of Systematic and Evolutionary Microbiology, 69(9): 2739–2749. doi: 10.1099/ijsem.0.003554
    Qin Wei, Heal K R, Ramdasi R, et al. 2017. Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota. International Journal of Systematic and Evolutionary Microbiology, 67(12): 5067–5079. doi: 10.1099/ijsem.0.002416
    Reading M J, Tait D R, Maher D T, et al. 2021. Submarine groundwater discharge drives nitrous oxide source/sink dynamics in a metropolitan estuary. Limnology and Oceanography, 66(5): 1665–1686. doi: 10.1002/lno.11710
    Rocha C, Robinson C E, Santos I R, et al. 2021. A place for subterranean estuaries in the coastal zone. Estuarine, Coastal and Shelf Science, 250: 107167,
    Ruiz-González C, Rodellas V, Garcia-Orellana J. 2021. The microbial dimension of submarine groundwater discharge: current challenges and future directions. FEMS Microbiology Reviews, 45(5): fuab010. doi: 10.1093/femsre/fuab010
    Ruiz-González C, Rodríguez-Pie L, Maister O, et al. 2022. High spatial heterogeneity and low connectivity of bacterial communities along a Mediterranean subterranean estuary. Molecular Ecology, 31(22): 5745–5764. doi: 10.1111/mec.16695
    Santoro A E, Boehm A B, Francis C A. 2006. Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer. Applied and Environmental Microbiology, 72(3): 2102–2109. doi: 10.1128/AEM.72.3.2102-2109.2006
    Santoro A E, Francis C A, De Sieyes N R, et al. 2008. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology, 10(4): 1068–1079. doi: 10.1111/j.1462-2920.2007.01547.x
    Santos I R, Chen Xiaogang, Lecher A L, et al. 2021. Submarine groundwater discharge impacts on coastal nutrient biogeochemistry. Nature Reviews Earth & Environment, 2(5): 307–323. doi: 10.1038/s43017-021-00152-0
    Schloss P D, Westcott S L, Ryabin T, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23): 7537–7541. doi: 10.1128/AEM.01541-09
    Stieglmeier M, Klingl A, Alves R J E, et al. 2014. Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. International Journal of Systematic and Evolutionary Microbiology, 64(8): 2738–2752. doi: 10.1099/ijs.0.063172-0
    Strickland J D H, Parsons T R. 1972. A Practical Handbook of Seawater Analysis. 2nd ed. Ottawa: Minister des Approvisionnements et Services, 119–123
    Tamura K, Stecher G, Peterson D, et al. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12): 2725–2729. doi: 10.1093/molbev/mst197
    ter Braak C J F. 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology, 67(5): 1167–1179. doi: 10.2307/1938672
    Torre D M, Coyne K J, Kroeger K D, et al. 2019. Phytoplankton community structure response to groundwater-borne nutrients in the Inland Bays, Delaware, USA. Marine Ecology Progress Series, 624: 51–63. doi: 10.3354/meps13012
    Walker C B, de la Torre J R, Klotz M G, et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences of the United States of America, 107(19): 8818–8823. doi: 10.1073/pnas.0913533107
    Wang Guizhi, Jing Wenping, Wang Shuling, et al. 2014. Coastal acidification induced by tidal-driven submarine groundwater discharge in a coastal coral reef system. Environmental Science & Technology, 48(22): 13069–13075. doi: 10.1021/es5026867
    Wang Qianqian, Li Hailong, Zhang Yan, et al. 2019. Evaluations of submarine groundwater discharge and associated heavy metal fluxes in Bohai Bay, China. Science of the Total Environment, 695: 133873. doi: 10.1016/j.scitotenv.2019.133873
    Wang Xuejing, Li Hailong, Zheng Chunmiao, et al. 2018. Submarine groundwater discharge as an important nutrient source influencing nutrient structure in coastal water of Daya Bay, China. Geochimica et Cosmochimica Acta, 225: 52–65. doi: 10.1016/j.gca.2018.01.029
    Wang Yongming, Pan Jie, Yang Jun, et al. 2020. Patterns and processes of free-living and particle-associated bacterioplankton and archaeaplankton communities in a subtropical river-bay system in South China. Limnology and Oceanography, 65(S1): S161–S179. doi: 10.1002/lno.11314
    Wang Xilong, Su Kaijun, Chen Xiaogang, et al. 2021. Submarine groundwater discharge-driven nutrient fluxes in a typical mangrove and aquaculture bay of the Beibu Gulf, China. Marine Pollution Bulletin, 168: 112500. doi: 10.1016/j.marpolbul.2021.112500
    Wu Jiapeng, Hong Yiguo, Wilson S J, et al. 2021. Microbial nitrogen loss by coupled nitrification to denitrification and anammox in a permeable subterranean estuary at Gloucester Point, Virginia. Marine Pollution Bulletin, 168: 112440. doi: 10.1016/j.marpolbul.2021.112440
    Xie Wei, Luo Haiwei, Murugapiran S K, et al. 2018. Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation. Environmental Microbiology, 20(2): 734–754. doi: 10.1111/1462-2920.14004
    Xiong Jinbo, Liu Yongqin, Lin Xiangui, et al. 2012. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environmental Microbiology, 14(9): 2457–2466. doi: 10.1111/j.1462-2920.2012.02799.x
    Yang Fan, Liu Sen, Jia Chao, et al. 2022. Identification of groundwater microbial communities and their connection to the hydrochemical environment in southern Laizhou Bay, China. Environmental Science and Pollution Research, 29(10): 14263–14278. doi: 10.1007/s11356-021-16812-z
    Yau Y Y Y, Xin Pei, Chen Xiaogang, et al. 2022. Alkalinity export to the ocean is a major carbon sequestration mechanism in a macrotidal saltmarsh. Limnology and Oceanography, 67(S2): S158–S170. doi: 10.1002/lno.12155
    Ye Qi, Liu Jianan, Du Jinzhou, et al. 2016. Bacterial diversity in submarine groundwater along the coasts of the Yellow Sea. Frontiers in Microbiology, 6: 1519. doi: 10.3389/fmicb.2015.01519
    Yu Xueqing, Liu Jianan, Chen Xiaogang, et al. 2022. Submarine groundwater-derived inorganic and organic nutrients vs. mariculture discharge and river contributions in a typical mariculture bay. Journal of Hydrology, 613: 128342. doi: 10.1016/j.jhydrol.2022.128342
    Zhang Shengdong, Zhao Shibin, Chen Ye, et al. 2021. Effects of submarine groundwater discharge on bacterial community structure in the coastal waters of South Yellow Sea. Acta Scientiae Circumstantiae (in Chinese), 41(12): 4942–4952. doi: 10.13671/j.hjkxxb.2021.0250
    Zhao Shibin, Xu Bochao, Yao Qinzhen, et al. 2021. Nutrient-rich submarine groundwater discharge fuels the largest green tide in the world. Science of the Total Environment, 770: 144845. doi: 10.1016/j.scitotenv.2020.144845
    Zhong Qiangqiang, Puigcorbé V, Chen Xiaogang, et al. 2022. Unexpectedly high dissolved 210Pb in coastal groundwaters: is submarine groundwater discharge important in coastal sea?. Chemical Geology, 614: 121165. doi: 10.1016/j.chemgeo.2022.121165
    Zhu Peiyuan, Chen Xiaogang, Zhang Yan, et al. 2022. Porewater-derived blue carbon outwelling and greenhouse gas emissions in a subtropical multi-species saltmarsh. Frontiers in Marine Science, 9: 884951. doi: 10.3389/fmars.2022.884951
    Žic V, Truesdale V W, Cukrov N. 2008. The distribution of iodide and iodate in anchialine cave waters—Evidence for sustained localised oxidation of iodide to iodate in marine water. Marine Chemistry, 112(3–4): 168–178,
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(8)  / Tables(3)

    Article Metrics

    Article views (209) PDF downloads(19) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint