Abstract
Cyanobacterial blooms may stimulate epiphytic nitrification and denitrification in the water column. To validate this hypothesis, a 4-week floating mesocosms experiment that involved a cyanobacterial decay–growth–decay period was conducted at Lake Taihu. In addition to conventional methods for detecting the physical and chemical properties, quantitative real-time PCR was used to identify the nitrification and denitrification genes (archaeal and bacterial amoA, nirS and nirK). Treatment with cyanobacteria led to removal of about 3.62 mg N L−1 total nitrogen, 40% of which was organic nitrogen, indicating a nitrogen transformation and removal mechanism was present in the system. Variations in the biogeochemical properties suggested that remineralization and coupling nitrification and denitrification by epiphytic and pelagic microorganisms was the primary pathway through which organic nitrogen was removed. The results of this study revealed that algal blooms can accelerate nitrogen removal efficiency, which may be the primary reason that nitrogen is limited in summer in Lake Taihu.
Similar content being viewed by others
References
Akunna JC, Bizeau C, Moletta R (1993) Nitrate and nitrite reductions with anaerobic sludge using various carbon sources: glucose, glycerol, acetic acid, lactic acid and methanol. Water Res 27(8):1303–1312
An S, Joye SB (2001) Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnol Oceanogr 46(1):62–74
Andersen T, Jensen M, Sørensen J (1984) Diurnal variation of nitrogen cycling in coastal, marine sediments. Mar Biol 83(2):171–176
Braker G, Zhou J, Wu L, Devol AH, Tiedje JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in pacific northwest marine sediment communities. Appl Environ Microbiol 66(5):2096–2104
Brandes JA, Devol AH, Deutsch C (2007) New developments in the marine nitrogen cycle. Chem Rev 107(2):577–589
Brunberg A-K (1999) Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol Ecol 29(1):13–22
Cardinale BJ (2011) Cardinale reply. Nature 477(7366):E3–E4
Chen P, Zhou Q, Paing J, Le H, Picot B (2003) Nutrient removal by the integrated use of high rate algal ponds and macrophyte systems in China. Water Sci Technol 48(2):251–257
Chen X, Yang L, Xiao L, Miao A, Xi B (2012) Nitrogen removal by denitrification during cyanobacterial bloom in Lake Taihu. J Freshw Ecol 27(2):243–258
Choi O, Das A, Yu CP, Hu Z (2010) Nitrifying bacterial growth inhibition in the presence of algae and cyanobacteria. Biotechnol Bioeng 107(6):1004–1011
Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156(4):457–464
de Godos I, Blanco S, García-Encina PA, Becares E, Muñoz R (2009) Long-term operation of high rate algal ponds for the bioremediation of piggery wastewaters at high loading rates. Bioresour Technol 100(19):4332–4339
De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22(3):151–175
Eriksson PG (2001) Interaction effects of flow velocity and oxygen metabolism on nitrification and denitrification in biofilms on submersed macrophytes. Biogeochemistry 55(1):29–44
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci 102(41):14683–14688
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451(7176):293–296
Hamonts K, Clough TJ, Stewart A, Clinton PW, Richardson AE, Wakelin SA, O’Callaghan M, Condron LM (2013) Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol 83(3):568–584
Hansen L, Blackburn T (1992) Effect of algal bloom deposition on sediment respiration and fluxes. Mar Biol 112(1):147–152
Hou J, Song C, Cao X, Zhou Y (2013) Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu). Water Res 47(7):2285–2296
Jiang L, Yang L, Xiao L, Shi X, Gao G, Qin B (2007) Quantitative studies on phosphorus transference occuring between Microcystis aeruginosa and its attached bacterium (Pseudomonas sp.). Hydrobiologia 581(1):161–165
Kester RA, De Boer W, Laanbroek HJ (1997) Production of NO and N2 O by pure cultures of nitrifying and denitrifying bacteria during changes in aeration. Appl Environ Microbiol 63(10):3872–3877
Lai PC, Lam PK (1997) Major pathways for nitrogen removal in waste water stabilization ponds. Water Air Soil Pollut 94(1–2):125–136
Law CS, Rees AP, Owens NJP (1993) Nitrous oxide production by estuarine epiphyton. Limnol Oceanogr 38(2):435–441
Li H, Xing P, Chen M, Bian Y, Wu QL (2011) Short-term bacterial community composition dynamics in response to accumulation and breakdown of Microcystis blooms. Water Res 45(4):1702–1710
Loken LC, Small GE, Finlay JC, Sterner RW, Stanley EH (2016) Nitrogen cycling in a freshwater estuary. Biogeochemistry 127(2–3):1–18
Mccarthy MJ, Lavrentyev PJ, Yang L, Zhang L, Chen Y, Qin B, Gardner WS (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
McMillan SK, Piehler MF, Thompson SP, Paerl HW (2010) Denitrification of nitrogen released from senescing algal biomass in coastal agricultural headwater streams. J Environ Qual 39(1):274–281
Michotey V, Méjean V, Bonin P (2000) Comparison of methods for quantification of cytochrome cd(1)-denitrifying bacteria in environmental marine samples. Appl Environ Microbiol 66(4):1564–1571
Nguyen M-L, Westerhoff P, Baker L, Hu Q, Esparza-Soto M, Sommerfeld M (2005) Characteristics and reactivity of algae-produced dissolved organic carbon. J Environ Eng 131(11):1574–1582
Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma Z, Qi M (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45(14):4169–4182
Paraskaki I, Lazaridis M (2005) Quantification of landfill emissions to air: a case study of the Ano Liosia landfill site in the greater Athens area. Waste Manag Res 23(3):199–208
Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14(4):993–1008
Poulson SR, Sullivan AB (2010) Assessment of diel chemical and isotopic techniques to investigate biogeochemical cycles in the upper Klamath River, Oregon, USA. Chem Geol 269(1):3–11
Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66(12):5368–5382
Risgaard-Petersen N, Rysgaard S, Nielsen LP, Revsbech NP (1994) Diurnal variation of denitrification and nitrification in sediments colonized by benthic microphytes. Limnol Oceanogr 39(3):573–579
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63(12):4704–4712
Scheffer M, Jeppesen E (1998) Alternative stable states. In: The structuring role of submerged macrophytes in lakes. Springer, pp 397–406
Shang J, Zhang L, Shi C, Fan C (2013) Influence of Chironomid Larvae on oxygen and nitrogen fluxes across the sediment-water interface (Lake Taihu, China). J Environ Sci 25(5):978–985
Smyth AR, Thompson SP, Siporin KN, Gardner WS, Mccarthy MJ, Piehler MF (2013) Assessing nitrogen dynamics throughout the estuarine landscape. Estuar Coasts 36(1):44–55
Strauss EA, Mitchell NL, Lamberti GA (2002) Factors regulating nitrification in aquatic sediments: effects of organic carbon, nitrogen availability, and pH. Can J Fish Aquat Sci 59(3):554–563
Takács I, Vanrolleghem P (2006) Elemental balances in activated sludge modelling. In: Proceedings of IWA World Water Congress, pp 10–14
Thouvenot M, Billen G, Garnier J (2007) Modelling nutrient exchange at the sediment–water interface of river systems. J Hydrol 341(1):55–78
Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnde AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 179–244
Tuomainen JM, Hietanen S, Kuparinen J, Martikainen PJ, Servomaa K (2003) Baltic Sea cyanobacterial bloom contains denitrification and nitrification genes, but has negligible denitrification activity. FEMS Microbiol Ecol 45(2):83–96
Wang Y, Li Z, Zhou L, Feng L, Fan N, Shen J (2013) Effects of macrophyte-associated nitrogen cycling bacteria on denitrification in the sediments of the eutrophic Gonghu Bay, Taihu Lake. Hydrobiologia 700(1):329–341
Xu H, Paerl HW, Qin B, Zhu G, Guang G (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55(1):420–432
Xu H, Paerl HW, Qin B, Zhu G, Hall NS, Wu Y (2015) Determining critical nutrient thresholds needed to control harmful cyanobacterial blooms in eutrophic Lake Taihu, China. Environ Sci Technol 49(2):1051–1059
Zhong J, Fan C, Liu G, Lei Z, Shang J, Gu X (2010) Seasonal variation of potential denitrification rates of surface sediment from Meiliang Bay, Taihu Lake, China. J Environ Sci 22(7):961–967
Zhu M, Zhu G, Zhao L, Yao X, Zhang Y, Gao G, Qin B (2013) Influence of algal bloom degradation on nutrient release at the sediment–water interface in Lake Taihu, China. Environ Sci Pollut Res Int 20(3):1803–1811
Zumft WG (1992) The denitrifying prokaryotes. Prokaryotes 1:554–582
Acknowledgements
We are grateful to the Taihu Laboratory for Lake Ecosystem Research (TLLER) for providing the experimental fields and other technical helps. This research was financially supported by National Natural Science Foundation of China (Contracts 41373076).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jennifer Leah Tank.
Rights and permissions
About this article
Cite this article
Chen, X., Jiang, H., Sun, X. et al. Nitrification and denitrification by algae-attached and free-living microorganisms during a cyanobacterial bloom in Lake Taihu, a shallow Eutrophic Lake in China. Biogeochemistry 131, 135–146 (2016). https://doi.org/10.1007/s10533-016-0271-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-016-0271-z