Volume 42 Issue 8
Aug.  2023
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Yueming Wu, Yongjun Wei, Juan Severino Pino Ibánhez, Danqing Sun, Kaiqi Lu, Qianqian Wang, Jian Li, Shan Jiang. Microbiota of a seepage face at the mouth of a subterranean estuary: diversity, distribution and substrate dependence[J]. Acta Oceanologica Sinica, 2023, 42(8): 147-157. doi: 10.1007/s13131-023-2257-8
Citation: Yueming Wu, Yongjun Wei, Juan Severino Pino Ibánhez, Danqing Sun, Kaiqi Lu, Qianqian Wang, Jian Li, Shan Jiang. Microbiota of a seepage face at the mouth of a subterranean estuary: diversity, distribution and substrate dependence[J]. Acta Oceanologica Sinica, 2023, 42(8): 147-157. doi: 10.1007/s13131-023-2257-8

Microbiota of a seepage face at the mouth of a subterranean estuary: diversity, distribution and substrate dependence

doi: 10.1007/s13131-023-2257-8
Funds:  The National Natural Science Foundation of China under contract No. 41706081.
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  • Corresponding author: E-mail: sjiang@sklec.ecnu.edu.cn
  • Received Date: 2023-07-04
  • Accepted Date: 2023-09-18
  • Publish Date: 2023-08-31
  • Subterranean estuaries, i.e., the mixing zone between terrestrial groundwater and recirculated seawater, host a wide range of microbiota. Here, field campaigns were conducted at the mouth of the subterranean estuary at the Sanggou Bay (Shandong Province, China) over four consecutive seasons at a seepage face (0−20 cm depth). The diversity of benthic microbiome was characterized via 16S rRNA gene sequencing and metagenomics, combined with physic-chemical parameters, e.g., organic carbon, total nitrogen and sulfate contents in sediments. During spring, the dominant species were assigned to the phylum Proteobacteria. Important opportunistic species was assigned to Acidobacteria, Actinobacteria and Bacteroidetes. The key components were identified to be species of the genera Pseudoalteromonas, Colwellia and Sphingobium, indicating the involvement of sediment microbiota in the degradation of sedimentary organic carbon, particularly that of pelagic origin, e.g., phytoplankton detritus and bivalve pseudo-feces. During spring, the microbial community was statistically similar along the depth profiles and among the three sampled stations. Similar spatial distributions were obtained in the remaining seasons. By contrast, the dominant species assemblages varied significantly among seasons, with key genera being Thioprofundum and Nitrosopumilus during summer and autumn and Thioprofundum and Ilumatobacter during winter. Network analysis revealed a seasonal shift in benthic nitrogen and sulfur metabolism associated with these variations in microbial community composition. Overall, our findings suggested that macro elements derived from pelagic inputs, particularly detrital phytoplankton, shaped the microbial community compositions at the seepage face, resulting in significant seasonal variations, while the influence of terrestrial materials transported by groundwater on the sediment microbiota at the seepage face found to be minor.
  • These authors contributed equally to this work.
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  • 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
    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
    Banerjee S, Schlaeppi K, van der Heijden M G A. 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology, 16(9): 567–576. doi: 10.1038/s41579-018-0024-1
    Boehm A B, Yamahara K M, Sassoubre L M. 2014. Diversity and transport of microorganisms in intertidal sands of the California coast. Applied and Environmental Microbiology, 80(13): 3943–3951
    Bohórquez J, McGenity T J, Papaspyrou S, et al. 2017. Different types of diatom-derived extracellular polymeric substances drive changes in heterotrophic bacterial communities from intertidal sediments. Frontiers in microbiology, 8: 245
    Calvo-Martin E, Álvarez-Salgado X A, Rocha C, et al. 2021. Reactive solute transport through two contrasting subterranean estuary exit sites in the Ría de Vigo (NW Iberian Peninsula). Frontiers in Marine Science, 8: 626813. doi: 10.3389/fmars.2021.626813
    Calvo-Martin E, Teira E, Álvarez-Salgado X A, et al. 2022. On the hidden diversity and niche specialization of the microbial realm of subterranean estuaries. Environmental Microbiology, 24(12): 5859–5881. doi: 10.1111/1462-2920.16160
    Chen Xiaogang, Ye Qi, Sanders C J, et al. 2020. 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
    Cho H M, Kim G, Kwon E Y, et al. 2018. Radium tracing nutrient inputs through submarine groundwater discharge in the global ocean. Scientific Reports, 8(1): 2439. doi: 10.1038/s41598-018-20806-2
    Choi D H, Hwang C Y, Cho B C. 2009. Pelagibius litoralis gen. nov., sp. nov., a marine bacterium in the family Rhodospirillaceae isolated from coastal seawater. International Journal of Systematic and Evolutionary Microbiology, 59(4): 818–823. doi: 10.1099/ijs.0.002774-0
    Clark C D, De Bruyn W J, Aiona P D. 2016. Temporal variation in optical properties of chromophoric dissolved organic matter (CDOM) in Southern California coastal waters with nearshore kelp and seagrass. Limnology and Oceanography, 61(1): 32–46. doi: 10.1002/lno.10198
    Cole J R, Wang Qiong, Fish J A, et al. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42(D1): D633–D642. doi: 10.1093/nar/gkt1244
    Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19): 2460–2461. doi: 10.1093/bioinformatics/btq461
    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. 2016. SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. https://www.biorxiv.org/content/10.1101/074161v1[2016-09-12/2023-05-28]
    Edgar R C, Flyvbjerg H. 2015. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics, 31(21): 3476–3482. doi: 10.1093/bioinformatics/btv401
    Fernandes S O, Gonsalves M J, Nazareth D R, et al. 2022. Seasonal variability in environmental parameters influence bacterial communities in mangrove sediments along an estuarine gradient. Estuarine, Coastal and Shelf Science, 270: 107791
    Hong Yiguo, Wu Jiapeng, Wilson S, et al. 2019. Vertical stratification of sediment microbial communities along geochemical gradients of a subterranean estuary located at the Gloucester Beach of Virginia, United States. Frontiers in Microbiology, 9: 3343. doi: 10.3389/fmicb.2018.03343
    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: 10.1126/sciadv.1601897
    Jiang Shan, Jin Jie, Wei Yongjun, et al. 2023. Sandy seepage faces as bioactive nitrate reactors: Biogeochemistry, microbial ecology and metagenomics. Geoscience Frontiers, 14(3): 101529. doi: 10.1016/j.gsf.2022.101529
    Jiang Shan, Jin Jie, Wu Ying, et al. 2021a. Response of Nitrate Processing to Bio-labile Dissolved Organic Matter Supply Under Variable Oxygen Conditions in a Sandy Beach Seepage Face. Frontiers in Marine Science, 8: 642143. doi: 10.3389/fmars.2021.642143
    Jiang Shan, Kavanagh M, Ibánhez J S P, et al. 2021b. Denitrification-nitrification process in permeable coastal sediments: An investigation on the effect of salinity and nitrate availability using flow-through reactors. Acta Oceanologica Sinica, 40(9): 1–12. doi: 10.1007/s13131-021-1811-5
    Jiang Shan, Lu Haoliang, Zhang Qiong, et al. 2016. Effect of enhanced reactive nitrogen availability on plant-sediment mediated degradation of polycyclic aromatic hydrocarbons in contaminated mangrove sediment. Marine Pollution Bulletin, 103(1–2): 151–158
    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
    Jiao Shuo, Liu Zhenshan, Lin Yanbing, et al. 2016. Bacterial communities in oil contaminated soils: biogeography and co-occurrence patterns. Soil Biology and Biochemistry, 98: 64–73. doi: 10.1016/j.soilbio.2016.04.005
    Klier J, Dellwig O, Leipe T, et al. 2018. Benthic bacterial community composition in the oligohaline-marine transition of surface sediments in the Baltic Sea based on rRNA analysis. Frontiers in Microbiology, 9: 236
    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
    Liang Jiawei, Mai Wenning, Tang Jinfeng, et al. 2019. Highly effective treatment of petrochemical wastewater by a super-sized industrial scale plant with expanded granular sludge bed bioreactor and aerobic activated sludge. Chemical Engineering Journal, 360: 15–23. doi: 10.1016/j.cej.2018.11.167
    Liang Jiawei, Mai Wenning, Wang Jia, et al. 2021. Performance and microbial communities of a novel integrated industrial-scale pulp and paper wastewater treatment plant. Journal of Cleaner Production, 278: 123896. doi: 10.1016/j.jclepro.2020.123896
    Linkhorst A, Dittmar T, Waska H. 2017. Molecular fractionation of dissolved organic matter in a shallow subterranean estuary: the role of the iron curtain. Environmental Science & Technology, 51(3): 1312–1320
    Liu Xiaohan, Liu Yuyang, Chai Zhaoyang, et al. 2023. A combined approach detected novel species diversity and distribution of dinoflagellate cysts in the Yellow Sea, China. Marine Pollution Bulletin, 187: 114567. doi: 10.1016/j.marpolbul.2022.114567
    Liu Hongjun, Zeng Wei, Meng Qingan, et al. 2022. Phosphorus removal performance, intracellular metabolites and clade-level community structure of Tetrasphaera-dominated polyphosphate accumulating organisms at different temperatures. Science of the Total Environment, 842: 156913. doi: 10.1016/j.scitotenv.2022.156913
    Moore W S. 2010. The effect of submarine groundwater discharge on the ocean. Annual Review of Marine Science, 2: 59–88. doi: 10.1146/annurev-marine-120308-081019
    Reckhardt A, Beck M, Seidel M, et al. 2015. Carbon, nutrient and trace metal cycling in sandy sediments: a comparison of high-energy beaches and backbarrier tidal flats. Estuarine, Coastal and Shelf Science, 159: 1–14
    Robinson C, Gibbes B, Carey H, et al. 2007. Salt-freshwater dynamics in a subterranean estuary over a spring-neap tidal cycle. Journal of Geophysical Research: Oceans, 112(C9): C09007
    Rocha C, Jiang Shan, Ibánhez J S P, et al. 2022. The effects of subterranean estuary dynamics on nutrient resource ratio availability to microphytobenthos in a coastal lagoon. Science of the Total Environment, 851: 157522. doi: 10.1016/j.scitotenv.2022.157522
    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, 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
    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
    Sia E S A, Zhu Zhuoyi, Zhang Jing, et al. 2019. Biogeographical distribution of microbial communities along the Rajang River-South China Sea continuum. Biogeosciences, 16(21): 4243–4260. doi: 10.5194/bg-16-4243-2019
    Wang Liping, Zheng Binghui, Nan Bingxu, et al. 2014. Diversity of bacterial community and detection of nirS-and nirK-encoding denitrifying bacteria in sandy intertidal sediments along Laizhou Bay of Bohai Sea, China. Marine Pollution Bulletin, 88(1−2): 215–223. doi: 10.1016/j.marpolbul.2014.09.002
    Waska H, Simon H, Ahmerkamp S, et al. 2021. Molecular traits of dissolved organic matter in the subterranean estuary of a high-energy beach: indications of sources and sinks. Frontiers in Marine Science, 8: 607083. doi: 10.3389/fmars.2021.607083
    Wei Yongjun, Jiang Shan, Tian Lingmin, et al. 2022. Benthic microbial biogeography along the continental shelf shaped by substrates from the Changjiang River plume. Acta Oceanologica Sinica, 41(1): 118–131. doi: 10.1007/s13131-021-1861-8
    Wei Yongjun, Wu Yuqian, Zhang Lei, et al. 2020. Genome recovery and metatranscriptomic confirmation of functional acetate-oxidizing bacteria from enriched anaerobic biogas digesters. Environmental Pollution, 265: 114843. doi: 10.1016/j.envpol.2020.114843
    Weston N B, Joye S B. 2005. Temperature-driven decoupling of key phases of organic matter degradation in marine sediments. Proceedings of the National Academy of Sciences of the United States of America, 102(47): 17036–17040
    Wu Ying, Zhu Kun, Zhang Jing, et al. 2019. Distribution and degradation of terrestrial organic matter in the sediments of peat-draining rivers, Sarawak, Malaysian Borneo. Biogeosciences, 16(22): 4517–4533. doi: 10.5194/bg-16-4517-2019
    Yu Lu, Bai Junhong, Huang Laibin, et al. 2022. Carbon-rich substrates altered microbial communities with indication of carbon metabolism functional shifting in a degraded salt marsh of the Yellow River Delta, China. Journal of Cleaner Production, 331: 129898. doi: 10.1016/j.jclepro.2021.129898
    Yuan Mingli, Zhang Cuixia, Jiang Zengjie, et al. 2014. Seasonal variations in phytoplankton community structure in the Sanggou, Ailian, and Lidao Bays. Journal of Ocean University of China, 13(6): 1012–1024. doi: 10.1007/s11802-014-2305-2
    Zeng Dingyong, Huang Daji, Qiao Xudong, et al. 2015. Effect of suspended kelp culture on water exchange as estimated by in situ current measurement in Sanggou Bay, China. Journal of Marine Systems, 149: 14–24. doi: 10.1016/j.jmarsys.2015.04.002
    Zhang Yixue, Wu Ying, Zhang Jing, et al. 2021. Seasonal dynamics of surface dissolved organic matter in the South China Sea and the Straits of Malacca: Implications for biogeochemical province delineation of marginal seas. Journal of Geophysical Research: Biogeosciences, 126(10): e2021JG006535. doi: 10.1029/2021JG006535
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