Skip to main content
SpringerLink
Log in

Biological and chemical factors driving the temporal distribution of cyanobacteria and heterotrophic bacteria in a eutrophic lake (West Lake, China)

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Physico-chemical parameters, hydrological conditions, and microbial interactions can affect the growth and persistence of cyanobacteria, but the interacting effects among these bloom-forming factors are still poorly known. This hampers our capacity to predict the occurrence of cyanobacterial bloom accurately. Here, we studied the relationship between temperature, N and P cycles, and the microbial community abundance and diversity at 0.5 m under the surface of West Lake (China) from January 21 to November 20, 2015, in order to better understand the key factors regulating temporal changes in the cyanobacterial community. Using high throughput sequencing of the 16S rRNA gene V3-V4 region, we studied the diversity and abundance of bacteria. In parallel, we measured physico-chemical parameters and followed the abundance of key genes involved in N fixation, denitrification, and nutrient uptake. Multivariate analyses suggest that P concentration and water temperature are the key factors controlling the outbreak of summer cyanobacterial bloom. RT-qPCR analyses of the bacterial community and measurements of the copy number of denitrification-related gene (nirK, nosZ, nirS) show that denitrification potential and denitrifying bacteria relative abundance (Pseudomonas and Bacillus) increased in concert with diazotrophic cyanobacterial genera (Anabaena, Nostoc, Aphanizomenon flos-aquae) and the common bloom-forming non-diazotrophic cyanobacterium genus Microcystis. The present study brings new insights on the complex interplay between physico-chemical parameters, heterotrophic bacterial community composition, nitrogen cycle, and cyanobacteria dominance in a eutrophic lake.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12:1319–1333

    Article  CAS  PubMed  Google Scholar 

  • Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JL, Markager S, Riemann L (2014) Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 9:273–285

    Article  PubMed  PubMed Central  Google Scholar 

  • Berdjeb L, Pollet T, Chardon C, Jacquet S (2013) Spatio-temporal changes in the structure of archaeal communities in two deep freshwater lakes. FEMS Microbiol Ecol 86:215–230

    Article  CAS  PubMed  Google Scholar 

  • Beversdorf LJ, Miller TR, McMahon KD (2013) The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PLoS One 8:e56103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouwman AF, Boumans LJM, Batjes NH (2002) Emissions of N2O and NO from fertilized fields: summary of available measurement data. Global Biogeochem Cycle 16:1058–1071

    Google Scholar 

  • Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brookes JD, Carey CC (2011) Resilience to blooms. Science 333:46–47

    Article  Google Scholar 

  • Cai H, Jiang H, Krumholz LR, Yang Z (2014) Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS One 9:e102879

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai HY, Yan ZS, Wang AJ, Krumholz LR, Jiang HL (2013) Analysis of the attached microbial community on mucilaginous cyanobacterial aggregates in the eutrophic Lake Taihu reveals the importance of Planctomycetes. Microb Ecol 66:73–83

    Article  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dai R, Liu H, Qu J, Hou Y, Zhao X (2009) Effects of amino acids on microcystin production of the Microcystis aeruginosa. J Hazard Mater 161:730–736

    Article  CAS  PubMed  Google Scholar 

  • Duan HT, Ma RH, Xu XF, Kong FX, Zhang SX, Kong WJ, Hao JY, Shang LL (2009) Two-decade reconstruction of algal blooms in China’s Lake Taihu. Environ Sci Technol 43:3522–3528

    Article  CAS  PubMed  Google Scholar 

  • Duarte S, Fernandes I, Nogueira MJ, Cássio F, Pascoal C (2013) Temperature alters interspecific relationships among aquatic fungi. Fungal Ecol 6:187–191

    Article  Google Scholar 

  • Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci U S A 105:7774–7778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang ZT, Xie B, Yuan Q, Xu WQ, Lu J (2014) Microbial community study in newly established Qingcaosha Reservoir of Shanghai, China. Appl Microbiol Biotechnol 98:9849–9858

    Article  CAS  PubMed  Google Scholar 

  • Huber V, Wagner C, Gerten D, Adrian R (2012) To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers. Oecologia 169:245–256

    Article  PubMed  Google Scholar 

  • Hunter PD, Tyler AN, Gilvear DJ, Willby NJ (2009) Using remote sensing to aid the assessment of human health risks from blooms of potentially toxic cyanobacteria. Environ Sci Technol 43:2627–2633

    Article  CAS  PubMed  Google Scholar 

  • Jin ZF, Qin X, Chen LX, Jin MT, Li FL (2015) Using dual isotopes to evaluate sources and transformations of nitrate in the West Lake watershed, eastern China. J Contam Hydrol 177:64–75

    Article  PubMed  Google Scholar 

  • Leflaive J, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52:199–214

    Article  CAS  Google Scholar 

  • Lewis WM, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol 45:10300–10305

    Article  CAS  PubMed  Google Scholar 

  • O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334

    Article  Google Scholar 

  • Ogilvie BG, Rutter M, Nedwell DB (1997) Selection by temperature of nitrate-reducing bacteria from estuarine sediments: species composition and competition for nitrate. FEMS Microbiol Ecol 23:11–22

    Article  CAS  Google Scholar 

  • Otten TG, Xu H, Qin B, Zhu G, Paerl HW (2012) Spatiotemporal patterns and ecophysiology of toxigenic microcystis blooms in Lake Taihu, China: implications for water quality management. Environ Sci Technol 46:3480–3488

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater marine continuum. Adv Exp Med Biol 619:216–237

    Google Scholar 

  • Paerl HW (2009) Controlling eutrophication along the freshwater marine continuum: dual nutrient (N and P) reductions are essential. Estuar Coast 32:593–601

    Article  CAS  Google Scholar 

  • Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Xu H, Hall NS, Zhu G, Qin B, Wu Y, Rossignol KL, Dong L, McCarthy MJ, Joyner AR (2014) Controlling cyanobacterial blooms in hypertrophic Lake Taihu, China: will nitrogen reductions cause replacement of non-N2 fixing by N2 fixing taxa? PLoS One 9:113–123

    Article  Google Scholar 

  • Pomeroy LR, Wiebe WJ (2001) Temperature and substratesas interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204

    Article  Google Scholar 

  • Qian HF, Lu T, Peng XF, Han X, Fu ZW, Liu WP (2011) Enantioselective phytotoxicity of the herbicide imazethapyr on the response of the antioxidant system and starch metabolism in Arabidopsis thaliana. PLoS One 6:e19451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian HF, Pan XJ, Chen J, Zhou DM, Chen ZG, Zhang L, Fu ZW (2012) Analyses of gene expression and physiological changes in Microcystis aeruginosa reveal the phytotoxicities of three environmental pollutants. Ecotoxicology 21:847–859

    Article  CAS  PubMed  Google Scholar 

  • Qin HP, Su Q, Khu ST (2013) Assessment of environmental improvement measures using a novel integrated model: a case study of the Shenzhen River catchment, China. J Environ Manag 114:486–495

    Article  Google Scholar 

  • Rigosi A, Carey CC, Ibelings BW, Brookes JD (2014) The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol Oceanogr 59:99–114

    Article  Google Scholar 

  • Rigosi A, Hanson P, Hamilton DP, Hipsey M, Rusak JA, Bois J, Sparber K, Chorus I, Watkinson AJ, Qin B, Kim B, Brookes JD (2015) Determining the probability of cyanobacterial blooms: the application of Bayesian networks in multiple lake systems. Ecol Appl 25:186–199

    Article  PubMed  Google Scholar 

  • Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci U S A 105:11254–11258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler DW (1977) Evolution of phosphorus limitation in lakes: natural mechanisms compensate for deficiencies of nitrogen and carbon in eutrophied lakes. Science 195:260–262

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Cai Y, Li P, Yang H, Liu Z, Kong L, Yu Y, Kong F (2009) Molecular identification of the colony-associated cultivable bacteria of the cyanobacterium Microcystis aeruginosa and their effects on algal growth. J Freshw Ecol 24:211–218

    Article  CAS  Google Scholar 

  • Shi T, Ilikchyan I, Rabouille S, Zehr JP (2010) Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501. ISME J 4:621–632

    Article  CAS  PubMed  Google Scholar 

  • Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196

    Article  CAS  PubMed  Google Scholar 

  • Sun CC, Jin YJ, He HF, Wang W, He HW, Fu ZW, Qian HF (2015) Two novel herbicide candidates affect Arabidopsis thaliana growth by inhibiting nitrogen and phosphate absorption. Pestic Biochem Physiol 123:1–8

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Kong FX, Cao HS, Yu Y, Zhang M (2008) Recruitment of bloom-forming cyanobacteria and its driving factors. Afr J Biotechnol 7:4726–4731

    Google Scholar 

  • Tang CJ, Zheng P, Zhang L, Chen JW, Mahmood Q, Chen XG, Hu BL, Wang CH, Yu Y (2010) Enrichment features of anammox consortia from methanogenic granules loaded with high organic and methanol contents. Chemosphere 79:613–619

    Article  CAS  PubMed  Google Scholar 

  • Tison DL, Pope DH, Boylen CW (1980) Influence of seasonal temperature on the temperature optima of bacteria in sediments of Lake George. New-York Appl Environ Microbiol 39:675–677

    CAS  PubMed  Google Scholar 

  • Torrey MS, Lee GF (1975) Nitrogen fixation in Lake Mendota, Madison. Wisconsin Limnol Oceanogr 21:365–378

    Article  Google Scholar 

  • Wei W, Isobe K, Nishizawa T (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9:1954–1965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 49:1051–1059

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Yang Y, Zhao L, Li Y, Xie S, Liu Y (2015) Distribution of sediment bacterial and archaeal communities in plateau freshwater lakes. Appl Microbiol Biotechnol 99:3291–3302

    Article  CAS  PubMed  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Natural Science Foundation of China (21277127, 21577128), Zhejiang Provincial Natural Science Foundation of China (LR14B070001), and Program for Changjiang Scholars and Innovative Research Team in University (IRT13096).

Author information

Authors and Affiliations

  1. College of Environment, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Hao Song, Liwei Sun & Haifeng Qian

  2. Department of Food Science and Technology, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Jiahui Xu & Guangfu Liu

  3. Quebec-Ocean and Takuvik Joint International Research Unit, Université Laval, Québec, Canada

    Michel Lavoie

  4. College of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Xiaoji Fan & Zhengwei Fu

  5. Xinjiang Key Laboratory of Environmental Pollution and Bioremediation, Chinese Academy of Sciences, Urumqi, 830011, People’s Republic of China

    Haifeng Qian

Authors
  1. Hao Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiahui Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Lavoie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoji Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guangfu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liwei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhengwei Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haifeng Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haifeng Qian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any experiments involving human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, H., Xu, J., Lavoie, M. et al. Biological and chemical factors driving the temporal distribution of cyanobacteria and heterotrophic bacteria in a eutrophic lake (West Lake, China). Appl Microbiol Biotechnol 101, 1685–1696 (2017). https://doi.org/10.1007/s00253-016-7968-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7968-8

Keywords

Search

Navigation