Suspended solids induce increasing microbial ammonium recycling along the river-estuary continuum of the Yangtze River
Jingya Xue
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
College of Resources and Environment, University of Chinese Academy of Science, Beijing, China
Search for more papers by this authorZhonghua Zhao
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Search for more papers by this authorXiaolong Yao
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Search for more papers by this authorWeiting Liu
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
College of Resources and Environment, University of Chinese Academy of Science, Beijing, China
Search for more papers by this authorCorresponding Author
Lu Zhang
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Correspondence
Lu Zhang, State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China.
Email: [email protected]
Search for more papers by this authorJingya Xue
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
College of Resources and Environment, University of Chinese Academy of Science, Beijing, China
Search for more papers by this authorZhonghua Zhao
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Search for more papers by this authorXiaolong Yao
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Search for more papers by this authorWeiting Liu
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
College of Resources and Environment, University of Chinese Academy of Science, Beijing, China
Search for more papers by this authorCorresponding Author
Lu Zhang
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China
Correspondence
Lu Zhang, State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China.
Email: [email protected]
Search for more papers by this authorAbstract
Many large rivers worldwide are enriched with high levels of suspended solids (SS), which are known to be hotspots of many nitrogen (N) transformation processes (e.g., denitrification, nitrification). However, the influence of SS on microbial ammonium (NH4+) recycling remains unclear. Water column NH4+ regeneration rates (REGs) and potential uptake rates (Upots) as well as community biological NH4+ demand (CBAD) was measured in the river-estuary continuum of the third longest river in the world—Yangtze River, which has dramatic SS gradients. We found that REGs, Upots, and CBAD all increased downriver, with higher REGs, Upots, and CBAD in the estuary than in the river sections. The regeneration and uptake of NH4+ were nearly balanced in the river sections, while the positive CBAD in the estuary indicated obvious NH4+ demand of microbes. Concentrations of SS, which also control the content of chemical oxygen demand and particulate N, were the main factor influencing NH4+ recycling rates and CBAD. SS-induced regenerated NH4+ in the river-estuary continuum of Yangtze River was estimated to be 11.02 × 108 kg N yr−1 and accounted for about 14% of total N inputs, suggesting that regenerated NH4+ is an important N source for microbes and may influence nutrient dynamics in lower coasts. To our knowledge, this is the first study to report NH4+ recycling in Yangtze River with an emphasis on its influencing factors and contribution to N budgets.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author (Professor Lu Zhang, [email protected]).
Supporting Information
Filename | Description |
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hyp14345-sup-0001-SupInfo.docxWord 2007 document , 411.7 KB | Figure S1. Relationship between REGs and Upots in the river-estuary continuum of Yangtze River. Figure S2. Correlation analyses between SS and COD, TN, PN in the river-estuary continuum of Yangtze River. Figure S3. Correlation analyses of PN and Chl-a in the river-estuary continuum of Yangtze River. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Bilotta, G. S., & Brazier, R. E. (2008). Understanding the influence of suspended solids on water quality and aquatic biota. Water Research, 42(12), 2849–2861.
- Blackburn, T. H. (1979). Method for measuring rates of turnover in anoxic marine sediments, using a dilution technique. Applied and Environmental Microbiology, 37(4), 760–765.
- Bruesewitz, D. A., Gardner, W. S., Mooney, R. F., & Buskey, E. (2015). Seasonal water column cycling along a semi-arid sub-tropical river–estuary continuum: Responses to episodic events and drought conditions. Ecosystems, 18(5), 792–812.
- Chen, F., Hou, L., Liu, M., Zheng, Y., Yin, G., Lin, X., Li, X., Zong, H., Deng, F., Gao, J., & Jiang, X. (2016). Net anthropogenic nitrogen inputs (NANI) into the Yangtze River basin and the relationship with riverine nitrogen export. Journal of Geophysical Research – Biogeosciences, 121(2), 451–465.
- Collos, Y., Vaquer, A., Johnston, A. M., Pons, V., Bibent, B., & Richard, S. (2001). Carbon fixation, ammonium uptake and regeneration in an equatorial lake: Biological versus physical control. Journal of Plankton Research, 23(3), 263–270.
- Connelly, T. L., Baer, S. E., Cooper, J. T., Bronk, D. A., & Wawrik, B. (2014). Urea uptake and carbon fixation by marine pelagic bacteria and archaea during the Arctic summer and winter seasons. Applied and Environmental Microbiology, 80(19), 6013–6022.
- Dai, Z., Du, J., Zhang, X., Su, N., & Li, J. (2011). Variation of riverine material loads and environmental consequences on the Changjiang (Yangtze) estuary in recent decades (1955-2008). Environmental Science & Technology, 45, 223–227.
- Di, Z., Zhang, H., & Shan, B. (2015). Using sedimentary phosphorus/nitrogen as indicators of shallow lake eutrophication: Concentrations or accumulation fluxes. Environment and Earth Science, 74, 3935–3944.
- Diaz, R. J., & Rosenberg, R. (2008). Spreading dead zones and consequences for marine ecosystems. Science, 321(5891), 926–929.
- Gardner, W. S., Cavaletto, J. F., Bootsma, H. A., & Lavrentyev, P. J. (1998). Nitrogen cycling rates and light effects in tropical Lake Maracaibo, Venezuela. Limnology and Oceanography, 43(8), 1814–1825.
- Gardner, W. S., Lavrentyev, P. J., Cavaletto, J. F., McCarthy, M. J., Eadie, B. J., Johengen, T. H., & Cotner, J. B. (2004). Distribution and dynamics of nitrogen and microbial plankton in southern Lake Michigan during spring transition 1999–2000. Journal of Geophysical Research, 109, C03007.
- Gardner, W. S., Newell, S. E., McCarthy, M. J., Hoffman, D. K., Lu, K., Lavrentyev, P. J., Hellweger, F. L., Wilhelm, S. W., Liu, Z., Bruesewitz, D. A., & Paerl, H. W. (2017). Community biological ammonium demand: A conceptual model for cyanobacteria blooms in eutrophic lakes. Environmental Science & Technology, 51(14), 7785–7793.
- Glibert, P. M., Lipschultz, F., McCarthy, M. J., & Altabet, M. A. (1982). Isotope dilution models of uptake and remineralization ammonium by marine plankton. Limnology and Oceanography, 27(4), 639–650.
- Gudasz, C., Sobek, S., Bastviken, D., Koehler, B., & Tranvik, L. J. (2015). Temperature sensitivity of organic carbon mineralization in contrasting lake sediments. Journal of Geophysical Research – Biogeosciences, 120, 1215–1225.
- Hampel, J. J., McCarthy, M. J., Gardner, W. S., Zhang, L., Xu, H., Zhu, G., & Newell, S. E. (2018). Nitrification and ammonium dynamics in Taihu Lake, China: Seasonal competition for ammonium between nitrifiers and cyanobacteria. Biogeosciences, 15, 733–748.
- Hampel, J. J., McCarthy, M. J., Neudeck, M., Bullerjahn, G. S., McKay, R. M. L., & Newell, S. E. (2019). Ammonium recycling supports toxic Planktothrix blooms in Sandusky Bay, Lake Erie: Evidence from stable isotope and metatranscriptome data. Harmful Algae, 81, 42–52.
- Jiang, X., Zhang, L., Gao, G., Yao, X., Zhao, Z., & Shen, Q. (2019). High rates of ammonium recycling in northwestern Lake Taihu and adjacent rivers: An important pathway of nutrient supply in a water column. Environmental Pollution, 252, 1325–1334.
- Jiang, Z., Liu, J., Chen, J., Chen, Q., Yan, X., Xuan, J., & Zeng, J. (2014). Responses of summer phytoplankton community to drastic environmental changes in the Changjiang (Yangtze River) estuary during the past 50 years. Water Research, 54, 1–11.
- Jin, X., & Tu, Q. (1990). The stand methods for observation and analysis in Lake eutrophication. Chinese Environmental Science Press.
- Li, S., Liu, C., Li, J., Liu, X., Chetelat, B., Wang, B., & Wang, F. (2010). Assessment of the sources of nitrate in the Changjiang River, China using a nitrogen and oxygen isotopic approach. Environmental Science & Technology, 44, 1573–1578.
- Liang, C., & Xian, W. (2018). Changjiang nutrient distribution and transportation and their impacts on the estuary. Continental Shelf Research, 165, 137–145.
- Lin, X., Hou, L., Liu, M., Li, X., Yin, G., Zheng, Y., & Deng, F. (2016). Gross nitrogen mineralization in surface sediments of the Yangtze estuary. PLoS One, 11(3), e0151930.
- Liu, T., Xia, X., Liu, S., Mou, X., & Qiu, Y. (2013). Acceleration of denitrification in turbid rivers due to denitrification occurring on suspended sediment in oxic waters. Environmental Science & Technology, 47(9), 4053–4061.
- Liu, X., Beusen, A. H. W., Van Beek, L. P. H., Mogollon, J. M., Ran, X., & Bouwman, A. F. (2018). Exploring spatiotemporal changes of the Yangtze River (Changjiang) nitrogen and phosphorus sources, retention and export to the East China Sea and Yellow Sea. Water Research, 142, 246–255.
- McCarthy, M. J., Gardner, W. S., Lavrentyev, P. J., Moats, K. M., Jochem, F. J., & Klarer, D. M. (2007). Effects of hydrological flow regime on sediment-water interface and water column nitrogen dynamics in a great lakes coastal wetland (old Woman Creek, Lake Erie). Journal of Great Lakes Research, 33, 219–231.
- Mccarthy, M. J., Lavrentyev Peter, J., Yang, L., Zhang, L., Chen, Y., Qin, B., & Gardner, W. S. (2007). Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic Lake (Lake Taihu, China). Hydrobiologia, 581(1), 195–207.
- Muller, B., Berg, M., Yao, Z. P., Zhang, X. F., Wang, D., & Pfluger, A. (2008). How polluted is the Yangtze river? Water quality downstream from the three gorges dam. Science of the Total Environment, 402(2–3), 232–247.
- Mulvenna, P. F., & Graham, S. (1992). A modified manual method for the determination of urea in seawater using diacetylmonoxime reagent. Estuarine, Coastal and Shelf Science, 34, 429–438.
- Odman, F., Ruth, T., & Ponter, C. (1999). Validation of a field filtration technique for characterization of suspended particulate matter from freshwater. Part I. Major elements. Applied Geochemisrty, 14, 301–317.
- Paerl, H. W., Xu, H., McCarthy, M. J., Zhu, G., Qin, B., Li, Y., & Gardner, W. S. (2011). Controlling harmful cyanobacterial blooms in a hyper-eutrophic Lake (Lake Taihu, China): The need for a dual nutrient (N & P) management strategy. Water Research, 45(5), 1973–1983.
- Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H. W., & Carmichael, W. W. (2010). A drinking water crisis in Lake Taihu, China: Linkage to climatic variability and lake management. Environmental Management, 45(1), 105–112.
- Sipler, R. E., Baer, S. E., Connelly, T. L., Frischer, M. E., Roberts, Q. N., Yager, P. L., & Bronk, D. A. (2017). Chemical and photophysiological impact of terrestrially-derived dissolved organic matter on nitrate uptake in the coastal western Arctic. Limnology and Oceanography, 62(5), 1881–1894.
- Tang, D., Di, B., Wei, G., Ni, I. H., Oh, I. S., & Wang, S. (2006). Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia, 568(1), 245–253.
- Turner, A., & Millward, G. E. (2002). Suspended particles: Their role in estuarine biogeochemical cycles. Estuarine, Coastal and Shelf Science, 55, 857–883.
- Wang, H., Yang, Z., Wang, Y., Saito, Y., & Liu, J. P. (2008). Reconstruction of sediment flux from the Changjiang (Yangtze River) to the sea since the 1860s. Journal of Hydrology, 349, 318–332.
- Wong, G. T. F., Gomg, G.-C., Liu, K.-K., & Pai, S.-C. (1998). Excess nitrate in the East China Sea. Estuarine, Coastal and Shelf Science, 46, 411–418.
- Wu, Z., Liu, Y., Liang, Z., Wu, S., & Guo, H. (2017). Internal cycling, not external loading, decides the nutrient limitation in eutrophic lake: A dynamic model with temporal Bayesian hierarchical inference. Water Research, 116, 231–240.
- Xia, X., Liu, T., Yang, Z., Zhang, X., & Yu, Z. (2013). Dissolved organic nitrogen transformation in river water: Effects of suspended sediment and organic nitrogen concentration. Journal of Hydrology, 484, 96–104.
- Xia, X., Yang, Z., & Zhang, X. (2009). Effect of suspended-sediment concentration on nitrification in river water: Importance of suspended sediment-water interface. Environmental Science & Technology, 43, 3681–3687.
- Xue, J., Liu, W., Jiang, X., Zhao, Z., Zhang, L., Cai, Y., & Wang, X. (2019). Ammonium recycling and its influencing factors along the littoral zone of the middle reaches of Yangtze River. Resources and Environment in the Yangtze Basin, 28(11), 2735–2742.
- Yan, W., Mayorga, E., Li, X., Seitzinger, S. P., & Bouwman, A. F. (2010). Increasing anthropogenic nitrogen inputs and riverine DIN exports from the Changjiang River basin under changing human pressures. Global Biogeochemical Cycles, 24, GB0A06.
- Yang, S. L., Zhang, J., & Xu, X. J. (2007). Influence of the three gorges dam on downstream delivery of sediment and its environmental implications, Yangtze River. Geophysical Research Letters, 34, L10401.
- Yao, X., Zhang, L., Zhang, Y., Xu, H., & Jiang, X. (2016). Denitrification occurring on suspended sediment in a large, shallow, subtropical Lake (Poyang lake, China). Environmental Pollution, 219, 501–511.
- Yi, Y., Yang, Z., & Zhang, S. (2011). Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environmental Pollution, 159(10), 2575–2585.
- Yin, G., Hou, L., Liu, M., Liu, Z., & Gardner, W. S. (2014). A novel membrane inlet mass spectrometer method to measure for isotope-enrichment experiments in aquatic ecosystems. Environmental Science & Technology, 48(16), 9555–9562.
- Zhang, W., Gu, J., Li, Y., Lin, L., Wang, P., Wang, C., Qian, B., Wang, H., Niu, L., Wang, L., Zhang, H., Gao, Y., Zhu, M., & Fang, S. (2019). New insights into sediment transport in interconnected river-lake systems through tracing microorganisms. Environmental Science & Technology, 53(8), 4099–4108.
- Zheng, Z.-Z., Wan, X., Xu, M. N., Hsiao, S. S.-Y., Zhang, Y., Zheng, L.-W., Wu, Y., Zou, W., & Kao, S.-J. (2017). Effects of temperature and particles on nitrification in a eutrophic coastal bay in southern China. Journal of Geophysical Research – Biogeosciences, 122(9), 2325–2337.
- Zhou, M., Shen, Z., & Yu, R. (2008). Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) river. Continental Shelf Research, 28, 1483–1489.
- Zhou, Y., Xu, X., Han, R., Li, L., Feng, Y., Yeerken, S., Song, K., & Wang, Q. (2019). Suspended particles potentially enhance nitrous oxide (N2O) emissions in the oxic estuarine waters of eutrophic lakes: Field and experimental evidence. Environmental Pollution, 252, 1225–1234.