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Nutrient Removal in Eutrophic Water Promotes Stability of Planktonic Bacterial and Protist Communities

Abstract

Nutrient (nitrogen and phosphorus) removal by using bioremediation technologies in eutrophic water alters bacterial and protist community structure and function, but how it changes the stability of community remains unclear. To fill this gap, in this study, bacterial and protist communities were investigated using 16S and 18S rRNA gene high-throughput sequencing during the nutrient removal by using ecological floating beds of Canna indica L. Our results showed that both bacterial and protist community compositions in the treatment group were similar to those in the control group at the beginning of the experiment (day 1 to day 11), but then bacterial and protist community compositions became more stable with the removal of nutrients in the treatment group than those in the control group (day 12 to day 18). We further explored the mechanisms for this increased stability and found that the contribution of the stochastic process to bacterial and protist community variations was higher in the control group than that in the treatment group. This suggests that the high nutrient concentration in the control group might increase the random colonization or extinction, and therefore resulted in the high temporal variability (i.e., unstable) of bacterial and protist communities. Our findings suggest that bioremediation for eutrophication can promote the stability of aquatic communities, and therefore potentially maintain aquatic ecosystem functions and services to humanity.

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Availability of Data and Material

All sequence data from this study have been deposited in the public NCBI Sequence Read Archive (SRA) database under the accession numbers PRJNA562503 (bacteria) and PRJNA542064 (protists).

References

  1. 1.

    Sinha E, Michalak A, Balaji V (2017) Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357:405–408

    CAS  Article  Google Scholar 

  2. 2.

    Kim MS, Kim KH, Hwang SJ, Lee TK (2021) Role of algal community stability in harmful algal blooms in river-connected lakes. Microb Ecol 82:309–318

    CAS  Article  Google Scholar 

  3. 3.

    Morelli B, Hawkins TR, Niblick B, Henderson AD, Golden HE, Compton JE et al (2018) Critical Review of eutrophication models for life cycle assessment. Environ Sci Technol 52:9562–9578

    CAS  Article  Google Scholar 

  4. 4.

    Birk S, Chapman D, Carvalho L, Spears BM, Andersen HE, Argillier C et al (2020) Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nat Ecol Evol 4:1060–1068

    Article  Google Scholar 

  5. 5.

    Liu L, Wang S, Chen J (2021) Anthropogenic activities change the relationship between microbial community taxonomic composition and functional attributes. Environ. Microbiol

  6. 6.

    Afzal M, Arslan M, Müller JA, Shabir G, Islam E, Tahseen R et al (2019) Floating treatment wetlands as a suitable option for large-scale wastewater treatment. Nat Sustain 2:863–871

    Article  Google Scholar 

  7. 7.

    Chanc LMG, van Brunt SC, Majsztrik JC, White SA (2019) Short- and long-term dynamics of nutrient removal in floating treatment wetlands. Water Res 159:153–163

    Article  Google Scholar 

  8. 8.

    Huang Z, Kong F, Li Y, Xu G, Yuan R, Wang S (2020) Advanced treatment of effluent from municipal wastewater treatment plant by strengthened ecological floating bed. Bioresource Technol 309:123358

    CAS  Article  Google Scholar 

  9. 9.

    Chao C, Wang L, Li Y, Yan Z, Liu H, Yu D et al (2021) Response of sediment and water microbial communities to submerged vegetations restoration in a shallow eutrophic lake. Sci Total Environ 801:149701

    CAS  Article  Google Scholar 

  10. 10.

    Liu L, Wang S, Chen J (2021) Transformations from specialists to generalists cause bacterial communities are more stable than micro-eukaryotic communities under anthropogenic activity disturbance. Sci Total Environ 790:148141

    CAS  Article  Google Scholar 

  11. 11.

    Sun Y, Wang S, Niu J (2018) Microbial community evolution of black and stinking rivers during in situ remediation through micro-nano bubble and submerged resin floating bed technology. Bioresour Technol 258:187–194

    CAS  Article  Google Scholar 

  12. 12.

    Li X, Zhang M, Liu F, Chen L, Li Y, Li Y et al (2018) Seasonality distribution of the abundance and activity of nitrification and denitrification microorganisms in sediments of surface flow constructed wetlands planted with Myriophyllum elatinoides during swine wastewater treatment. Bioresour Technol 248:89–97

    CAS  Article  Google Scholar 

  13. 13.

    Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hillebrand H et al (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521

    CAS  Article  Google Scholar 

  14. 14.

    Tian W, Zhang H, Zhao L, Zhang F, Huang H (2017) Phytoplankton diversity effects on community biomass and stability along nutrient gradients in a eutrophic lake. Int J Environ Res Public Health 14:95

    Article  Google Scholar 

  15. 15.

    Yang W, Zheng C, Zheng Z, Wei Y, Lu K, Zhu J (2018) Nutrient enrichment during shrimp cultivation alters bacterioplankton assemblies and destroys community stability. Ecotoxicol Environ Saf 156:366–374

    CAS  Article  Google Scholar 

  16. 16.

    Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129

    CAS  Article  Google Scholar 

  17. 17.

    Amalfitano S, Corno G, Eckert E, Fazi S, Ninio S, Callieri C et al (2017) Tracing particulate matter and associated microorganisms in freshwaters. Hydrobiologia 800:145–154

    CAS  Article  Google Scholar 

  18. 18.

    Liu L, Chen H, Liu M, Yang JR, Xiao P, Wilkinson DM et al (2019) Response of the eukaryotic plankton community to the cyanobacterial biomass cycle over 6 years in two subtropical reservoirs. ISME J 13:2196–2208

    Article  Google Scholar 

  19. 19.

    Logares R, Tesson SVM, Canbck B, Pontarp M, Hedlund K, Rengefors K (2018) Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes. Environ Microbiol 20:2231–2240

    Article  Google Scholar 

  20. 20.

    Liu L, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9:2068–2077

    Article  Google Scholar 

  21. 21.

    Royo AA, Ristau TE (2013) Stochastic and deterministic processes regulate spatio-temporal variation in seed bank diversity. J Veg Sci 24:724–734

    Article  Google Scholar 

  22. 22.

    Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391

    CAS  Article  Google Scholar 

  23. 23.

    Liu L, Wang S, Chen J (2020) Hysteretic response of microbial eukaryotic communities to gradually decreased nutrient concentrations in eutrophic water. Microb Ecol 79:815–822

    Article  Google Scholar 

  24. 24.

    Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC et al (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321

    CAS  Article  Google Scholar 

  25. 25.

    Liu L, Wang S, Ji J, Xie Y, Shi X, Chen J (2020) Characteristics of microbial eukaryotic community recovery in eutrophic water by using ecological floating beds. Sci Total Environ 711:134551

    CAS  Article  Google Scholar 

  26. 26.

    Greenberg A, Clesceri L, Eaton A (1992) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

    Google Scholar 

  27. 27.

    Liu L, Wang S, Chen J (2021) Anthropogenic activities destabilized riverine bacterial communities by increasing synchrony between taxa. Aquat Sci 83:60

    CAS  Article  Google Scholar 

  28. 28.

    Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    CAS  Article  Google Scholar 

  29. 29.

    Cheung MK, Au CH, Chu KH, Kwan HS, Wong CK (2010) Composition and genetic diversity of picoeukaryotes in subtropical coastal waters as revealed by 454 pyrosequencing. ISME J 4:1053–1059

    Article  Google Scholar 

  30. 30.

    Elwood H, Olsen G, Sogin M (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol 2:399–410

    CAS  PubMed  Google Scholar 

  31. 31.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    CAS  Article  Google Scholar 

  32. 32.

    Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643

    Article  Google Scholar 

  33. 33.

    Clarke KR, Gorley RN (2015) PRIMER v7: User Manual/Tutorial. PRIMER-E Ltd, Plymouth

  34. 34.

    Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:24

    Article  Google Scholar 

  35. 35.

    Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ et al (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079

    Article  Google Scholar 

  36. 36.

    Zhang Z, Deng Y, Feng K, Cai W, Li S, Yin H et al (2019) Deterministic assembly and diversity gradient altered the biofilm community performances of bioreactors. Environ Sci Technol 53:1315–1324

    CAS  Article  Google Scholar 

  37. 37.

    Ma Z, Liu H, Mi Z, Zhang Z, Wang Y, Xu W et al (2017) Climate warming reduces the temporal stability of plant community biomass production. Nat Commun 8:15378

    Article  Google Scholar 

  38. 38.

    Kline RB (2005) Principles and practice of structural equation modelling. Guilford Press, New York

    Google Scholar 

  39. 39.

    Pennekamp F, Pontarp M, Tabi A, Altermatt F, Alther R, Choffat Y et al (2018) Biodiversity increases and decreases ecosystem stability. Nature 563:109–112

    CAS  Article  Google Scholar 

  40. 40.

    Puentes-Téllez PE, Salles JF (2020) Dynamics of abundant and rare bacteria during degradation of lignocellulose from sugarcane biomass. Microb Ecol 79:312–325

    Article  Google Scholar 

  41. 41.

    Conradi T, Temperton VM, Kollmann J (2017) Resource availability determines the importance of niche-based versus stochastic community assembly in grasslands. Oikos 126:1134–1141

    Article  Google Scholar 

  42. 42.

    Shade A, Read JS, Welkie DG, Kratz TK, Wu CH, McMahon KD (2011) Resistance, resilience and recovery: aquatic bacterial dynamics after water column disturbance. Environ Microbiol 13:2752–2767

    CAS  Article  Google Scholar 

Download references

Funding

This work was funded by the National Natural Science Foundation of China (31971469), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23040302), the Qishan Scholar Program of Fuzhou University (GXRC-20061), and the Research Project of Development Center of Science and Education Park, Fuzhou University (JinJiang) (2019-JJFDKY-71).

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Contributions

LL, JY, and JC conceived the idea and designed the experiments. LL wrote the paper. SW and LL performed the experiments. LL and SW analyzed the data. LL, JY, and JC contributed the reagents/materials/analysis tools. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Lemian Liu or Jun Yang.

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All authors have no conflict of interest to declare.

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Liu, L., Wang, S., Yang, J. et al. Nutrient Removal in Eutrophic Water Promotes Stability of Planktonic Bacterial and Protist Communities. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01898-2

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Keywords

  • Microbial community
  • Eutrophication
  • Ecological floating beds
  • 16S and 18S rRNA genes
  • Community stability