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Different nutrient levels, rather than seasonal changes, significantly affected the spatiotemporal dynamic changes of ammonia-oxidizing microorganisms in Lake Taihu

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Abstract

Ammonia-oxidizing microorganisms (AOM) play crucial roles in the degradation of ammonia nitrogen in freshwater lakes. Hence, it is necessary to reveal the spatiotemporal dynamic changes of AOM in freshwater lakes. Here, we conducted a study on the spatial and temporal dynamic changes of AOM in different lake regions under gradient nutrient levels in Lake Taihu, and found that the abundance of AOM had significant spatial changes, while the seasonal changes had relatively little effect on the abundance of AOM. We also found that ammonia-oxidizing archaea (AOA) were adapted to freshwater habitats with low nutrient levels, while ammonia-oxidizing bacteria (AOB) and anaerobic ammonia-oxidizing bacteria (AAOB) had higher abundance in high nutrient level lake regions. Moreover, the amoA gene abundance of AOB was much higher than that of AOA, indicating that AOB was the dominant aerobic ammonia oxidizer in the water of Lake Taihu. In addition, temperature, pH and dissolved oxygen all had a positive effect on AOM, especially AOB; while C- and N-related physicochemical factors had a significant positive effect on AAOB, but exhibited a significant negative correlation with AOA. The community structure of AOM also had obvious spatial changes and Group I.1a, Nitrosomonas and Candidatus Brocadia fulgida were the dominant cluster of AOA, AOB and AAOB, respectively.

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References

  • Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    CAS  Google Scholar 

  • Bollmann A, Schmidt I, Saunders AM, Nicolaisen MH (2005) Influence of starvation on potential ammonia-oxidizing activity and amoA mRNA levels of Nitrosospira briensis. Appl Environ Microbiol 71:1276–1282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cai Y, Gong Z, Qin B (2012) Benthic macroinvertebrate community structure in Lake Taihu, China: effects of trophic status, wind-induced disturbance and habitat complexity. J Great Lakes Res 38:39–48

    Google Scholar 

  • Colwell RK, Elsensohn JE (2014) EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography 37:609–613

    Google Scholar 

  • Dai J, Gao G, Chen D, Tang X, Shao K, Cai X (2013) Effects of trophic status and temperature on communities of sedimentary ammonia oxidizers in Lake Taihu. Geomicrobiol J 30:886–896

    CAS  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, Von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dietl A, Ferousi C, Maalcke WJ, Menzel A, De Vries S, Keltjens JT, Jetten MS, Kartal B, Barends TR (2015) The inner workings of the hydrazine synthase multiprotein complex. Nature 527:394–397

    CAS  PubMed  Google Scholar 

  • 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 USA 102:14683–14688

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francis CA, Beman JM, Kuypers MM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1:19–27

    CAS  PubMed  Google Scholar 

  • Gori F, Tringe SG, Kartal B, Marchiori E, Jetten MS (2011) The metagenomic basis of anammox metabolism in Candidatus “Brocadia fulgida.” Biochem Soc Trans 39:1799–1804

    CAS  PubMed  Google Scholar 

  • Guo L (2007) Ecology. Doing battle with the green monster of Taihu Lake. Science 317:1166

    CAS  PubMed  Google Scholar 

  • Guo X, Liu X, Wu L, Pan J, Yang H (2016) The algicidal activity of Aeromonas sp. strain GLY-2107 against bloom-forming Microcystis aeruginosa is regulated by N-acyl homoserine lactone-mediated quorum sensing. Environ Microbiol 18:3867–3883

    CAS  PubMed  Google Scholar 

  • Habteselassie MY, Li X, Norton JM (2013) Ammonia-oxidizer communities in an agricultural soil treated with contrasting nitrogen sources. Front Microbiol 4:326

    PubMed  PubMed Central  Google Scholar 

  • Han P, Klumper U, Wong A, Li M, Lin JG, Quan Z, Denecke M, Gu JD (2017) Assessment of molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in different environmental samples using PCR primers based on 16S rRNA and functional genes. Appl Microbiol Biotechnol 101:7689

    CAS  PubMed  Google Scholar 

  • Holmes DE, Dang Y, Smith JA (2019) Nitrogen cycling during wastewater treatment. Adv Appl Microbiol 106:113–192

    CAS  PubMed  Google Scholar 

  • 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 47:2285–2296

    CAS  PubMed  Google Scholar 

  • Huang R, Zhao D, Zeng J, Luo J, Shen F, Cao X, Jiang C, Huang F, Feng J, Zhou C, Sun Z, Yu Z, Wu QL (2016) Abundance and community composition of ammonia oxidizers in rhizosphere sediment of two submerged macrophytes. J Freshw Ecol 31:407–419

    CAS  Google Scholar 

  • Humbert S, Zopfi J, Tarnawski S-E (2012) Abundance of anammox bacteria in different wetland soils. Environ Microbiol Rep 4:484–490

    CAS  Google Scholar 

  • Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Sinninghe Damste JS, Kim GJ, Madsen EL, Rhee SK (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl Environ Microbiol 77:8635–8647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ke X, Lu Y (2012) Adaptation of ammonia-oxidizing microorganisms to environment shift of paddy field soil. FEMS Microbiol Ecol 80:87–97

    CAS  PubMed  Google Scholar 

  • Keshri J, Pradeep Ram AS, Sime-Ngando T (2018) Distinctive patterns in the taxonomical resolution of bacterioplankton in the sediment and pore waters of contrasted freshwater lakes. Microb Ecol 75:662–673

    CAS  PubMed  Google Scholar 

  • Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6:320–326

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276

    CAS  PubMed  Google Scholar 

  • Lehtovirta-Morley LE (2018) Ammonia oxidation: Ecology, physiology, biochemistry and why they must all come together. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fny058

    Article  PubMed  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    CAS  PubMed  Google Scholar 

  • Ling W, Hongyi Q, Mengyuan Z, Cheng H, Guangwei Z, Wenhui Z (2017) Distribution characteristics and controlling factors of nitrifying microorganisms in freshwater and sediment of eutrophic zones in Lake Taihu in autumn. J Lake Sci 29:1312–1323

    Google Scholar 

  • Oshiki M, Shimokawa M, Fujii N, Satoh H, Okabe S (2011) Physiological characteristics of the anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sinica.” Microbiology 157:1706–1713

    CAS  PubMed  Google Scholar 

  • Oshiki M, Satoh H, Okabe S (2016) Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol 18:2784–2796

    CAS  PubMed  Google Scholar 

  • Ostle N, Whiteley AS, Bailey MJ, Sleep D, Ineson P, Manefield M (2003) Active microbial RNA turnover in a grassland soil estimated using a 13CO2 spike. Soil Biol Biochem 35:877–885

    CAS  Google Scholar 

  • Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76:7575–7587

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:4704

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Xia C, Xu M, Guo J, Sun G, Wang A (2014) Community structure and distribution of planktonic ammonia-oxidizing archaea and bacteria in the Dongjiang River, China. Res Microbiol 165:657–670

    CAS  PubMed  Google Scholar 

  • Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    CAS  PubMed  Google Scholar 

  • Van Kessel MA, Speth DR, Albertsen M, Nielsen PH, Op Den Camp HJ, Kartal B, Jetten MS, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559

    PubMed  PubMed Central  Google Scholar 

  • Wan Y, Bai Y, He J, Zhang Y, Li R, Ruan X (2017) Temporal and spatial variations of aquatic environmental characteristics and sediment bacterial community in five regions of Lake Taihu. Aquat Ecol 51:343–358

    CAS  Google Scholar 

  • Wang S, Zhu G, Zhuang L, Li Y, Liu L, Lavik G, Berg M, Liu S, Long XE, Guo J, Jetten MSM, Kuypers MMM, Li F, Schwark L, Yin C (2019) Anaerobic ammonium oxidation is a major N-sink in aquifer systems around the world. ISME J 14:151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X, Xi W, Ye W, Yang H (2007) Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol Ecol 61:85–96

    CAS  PubMed  Google Scholar 

  • Wu X, Kong F, Chen Y, Qian X, Zhang L, Yu Y, Zhang M, Xing P (2010a) Horizontal distribution and transport processes of bloom-forming Microcystis in a large shallow lake (Taihu, China). Limnologica 40:8–15

    CAS  Google Scholar 

  • Wu Y, Xiang Y, Wang J, Zhong J, He J, Wu QL (2010b) Heterogeneity of archaeal and bacterial ammonia oxidizing communities in Lake Taihu, China. Environ Microbiol Rep 2:569–576

    CAS  PubMed  Google Scholar 

  • Wu L, Han C, Qin H, Zhu G, Zhong W (2018) Responses of active ammonia oxidizers to eutrophication and oxygen statuses in taihu freshwater sediments. Geomicrobiol J 35:829

    CAS  Google Scholar 

  • Zhang Y, Zhang B, Wang X, Li J, Feng S, Zhao Q, Liu M, Qin B (2007) A study of absorption characteristics of chromophoric dissolved organic matter and particles in Lake Taihu, China. Hydrobiologia 592:105–120

    CAS  Google Scholar 

  • Zhao DY, Luo J, Zeng J, Wang M, Yan WM, Huang R, Wu QL (2014) Effects of submerged macrophytes on the abundance and community composition of ammonia-oxidizing prokaryotes in a eutrophic lake. Environ Sci Pollut Res Int 21:389–398

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 21477077).

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  1. State Key Laboratory of Microbial Metabolism, and School of Life Science & Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, People’s Republic of China

    Tong-tong Liu & Hong Yang

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  1. Tong-tong Liu
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  2. Hong Yang
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TL and HY designed experiments. TL performed the experiments. TL and HY analyzed the data. TL wrote the manuscript.

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Correspondence to Hong Yang.

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Liu, Tt., Yang, H. Different nutrient levels, rather than seasonal changes, significantly affected the spatiotemporal dynamic changes of ammonia-oxidizing microorganisms in Lake Taihu. World J Microbiol Biotechnol 37, 91 (2021). https://doi.org/10.1007/s11274-021-03053-y

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