Skip to main content

Advertisement

Log in

Nonpoint Source Pollution (NPSP) Induces Structural and Functional Variation in the Fungal Community of Sediments in the Jialing River, China

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Nonpoint source pollution (NPSP) from human production and life activities causes severe destruction in river basin environments. In this study, three types of sediment samples (A, NPSP tributary samples; B, non-NPSP mainstream samples; C, NPSP mainstream samples) were collected at the estuary of the NPSP tributaries of the Jialing River. High-throughput sequencing of the fungal-specific internal transcribed spacer (ITS) gene region was used to identify fungal taxa. The impact of NPSP on the aquatic environment of the Jialing River was revealed by analysing the community structure, community diversity, and functions of sediment fungi. The results showed that the dominant phylum of sediment fungi was Rozellomycota, followed by Ascomycota and Basidiomycota (relative abundance > 5%). NPSP caused a significant increase in the relative abundances of Exosporium, Phialosimplex, Candida, Inocybe, Tausonia, and Slooffia, and caused a significant decrease in the relative abundances of Cercospora, Cladosporium, Dokmaia, Setophaeosphaeria, Paraphoma, Neosetophoma, Periconia, Plectosphaerella, Claviceps, Botrytis, and Papiliotrema. These fungal communities therefore have a certain indicator role. In addition, NPSP caused significant changes in the physicochemical properties of Jialing River sediments, such as pH and available nitrogen (AN), which significantly increased the species richness of fungi and caused significant changes in the fungal community β-diversity (P < 0.05). pH, total phosphorus (TP), and AN were the main environmental factors affecting fungal communities in sediments of Jialing River. The functions of sediment fungi mainly involved three types of nutrient metabolism (symbiotrophic, pathotrophic, and saprotrophic) and 75 metabolic circulation pathways. NPSP significantly improved the pentose phosphate pathway, pentose phosphate pathway, and fatty acid beta-oxidation V metabolic circulation pathway functions (P < 0.05) and inhibited the chitin degradation to ethanol, super pathway of heme biosynthesis from glycine, and adenine and adenosine salvage III metabolic circulation pathway functions (P < 0.05). Hence, NPSP causes changes in the community structure and functions of sediment fungi in Jialing River and has adversely affected for the stability of the Jialing River Basin ecosystem.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The data involved in this article have been included in the “Results” section and the supplementary information.

Code Availability

Not applicable.

References

  1. Abia ALK, Alisoltani A, Keshri J, Ubomba-Jaswa E (2018) Metagenomic analysis of the bacterial communities and their functional profiles in water and sediments of the Apies River, South Africa, as a function of land use. Sci Total Environ 616–617:326–334. https://doi.org/10.1016/j.scitotenv.2017.10.322

    Article  CAS  PubMed  Google Scholar 

  2. Al-Gabr HM, Zheng TL, Yu X (2014) Occurrence and quantification of fungi and detection of mycotoxigenic fungi in drinking water in Xiamen City. China Sci Total Environ 466:1103–1111. https://doi.org/10.1016/j.scitotenv.2012.12.060

    Article  CAS  PubMed  Google Scholar 

  3. Andrade VS, Gutierrez MF, Regaldo L, Paira AR, Repetti MR, Gagneten AM (2021) Influence of rainfall and seasonal crop practices on nutrient and pesticide runoff from soybean dominated agricultural areas in Pampean streams. Argentina Sci Total Environ 788:147676–147676. https://doi.org/10.1016/j.scitotenv.2021.147676

    Article  CAS  PubMed  Google Scholar 

  4. Arauzo M, Valladolid M, García G, Andries DM (2022) N and P behaviour in alluvial aquifers and in the soil solution of their catchment areas: how land use and the physical environment contribute to diffuse pollution. Sci Total Environ 804:150056. https://doi.org/10.1016/J.SCITOTENV.2021.150056

    Article  CAS  PubMed  Google Scholar 

  5. Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan J, Coelho LP, Harend H, Huerta-Cepas J, Medema MH, Maltz MR, Mundra S, Olsson PA, Pent M, Põlme S, Sunagawa S, Ryberg M, Tedersoo L, Bork P (2018) Structure and function of the global topsoil microbiome. Nature 560:233–237. https://doi.org/10.1038/s41586-018-0386-6

    Article  CAS  PubMed  Google Scholar 

  6. Baudy P, Zubrod JP, Konschak M, Kolbenschlag S, Pollitt A, Baschien C, Schulz R, Bundschuh M (2021) Fungal-fungal and fungal-bacterial interactions in aquatic decomposer communities: bacteria promote fungal diversity. Ecology 102(10):e03471. https://doi.org/10.1002/ecy.3471

    Article  PubMed  Google Scholar 

  7. Chen KH, Longley R, Bonito G, Liao HL (2021) A two-step PCR protocol enabling flexible primer choice and high sequencing yield for Illumina MiSeq meta-barcoding. Agronomy-basel 11(7):1274. https://doi.org/10.3390/agronomy11071274

    Article  CAS  Google Scholar 

  8. Chen J, Heikkinen J, Hobbie EA, Rinne-Garmston KT, Penttilä R, Mäkipää R (2019) Strategies of carbon and nitrogen acquisition by saprotrophic and ectomycorrhizal fungi in Finnish boreal Picea abies-dominated forests. Fungal Biol 123(6):456–464. https://doi.org/10.1016/j.funbio.2019.03.005

    Article  CAS  PubMed  Google Scholar 

  9. Chen L, Wang GB, Zhong YC, Shen ZY (2016) Evaluating the impacts of soil data on hydrological and nonpoint source pollution prediction. Sci Total Environ 563:19–28. https://doi.org/10.1016/j.scitotenv.2016.04.107

    Article  CAS  PubMed  Google Scholar 

  10. Costa MEL, Carvalho DJ, Koide S (2021) Assessment of pollutants from diffuse pollution through the correlation between rainfall and runoff characteristics using EMC and first flush analysis. Water 13(18):2552–2552. https://doi.org/10.3390/w13182552

    Article  CAS  Google Scholar 

  11. Eschen R, Allan E, Hartmann M, Schneider S, Prospero S (2020) Drivers of richness and community composition of fungal endophytes of tree seeds. FEMS Microbiolo Ecol 96(9):166–175. https://doi.org/10.1093/femsec/fiaa166

    Article  CAS  Google Scholar 

  12. Fang T., Li Y.C., Yao Z.X., Li Y.F., Wang X.M., Wang Y., Yu Y.F., 2021. Effects of planting broadleaf trees and Moso bamboo on soil carbon mineralization and microbial community structure. China. J. Appl. Ecol. 32(01): 82–92. https://doi.org/10.13287/j.1001-9332.202101.033.

  13. Fang Z.D., Su J.J., Zhao H.T., Hu L., Li X.Y., 2021. Output characteristics of nitrogen and phosphorus from nonpoint source pollution of typical land use in a micro-watershed in Hilly red soil region. Environ. Sci. 42(11): 5394–5404. https://doi.org/10.13227/j.hjkx.202103163.

  14. Foster S, Chilton J (2021) Policy experience with groundwater protection from diffuse pollution-a review. Curr Opin Environ Sci Heal 23:100288. https://doi.org/10.1016/j.coesh.2021.100288

    Article  Google Scholar 

  15. Genevieve L, Pierre-Luc C, Roxanne GT, Amelie M, Danny B, Vincent M, Hugo G (2019) Estimation of fungal diversity and identification of major abiotic drivers influencing fungal richness and communities in Northern Temperate and Boreal Quebec Forests. Forests 10(12):1096. https://doi.org/10.3390/f10121096

    Article  Google Scholar 

  16. Geng RZ, Liang XJ, Yin PH, Wang M, Zhou LL (2019) A review: multi-objective collaborative optimization of best management practices for non-point sources pollution control. Acta Ecol Sinica 39(8):2667–2675. https://doi.org/10.5846/stxb201804140860

    Article  Google Scholar 

  17. Guo ML, Jiang Y, Xie JX, Cao QF, Zhang Q, Mabruk A, Chen CJ (2022) Bamboo charcoal addition enhanced the nitrogen removal of anammox granular sludge with COD: performance, physicochemical characteristics and microbial community. J ENVIRON SCI 115:554–564. https://doi.org/10.1016/j.jes.2021.07.010

    Article  CAS  Google Scholar 

  18. Han X.M., Gong Z.L., Yang X.M., Li Y.Y., Chen Z.J., Zhu H.H., Wang F.M., 2021. Community diversity and function prediction of bacterioplankton in the main stream of Laoguan River before and after flood season. Environ. Sci. 42(02): 831–841. https://doi.org/10.13227/j.hjkx.202007082.

  19. Heikkinen K, Saari M, Heino J, Ronkanen AK, Kortelainen P, Joensuu S, Vilmi A, Karjalainen SM, Hellsten S, Visuri M, Marttila H (2021) Iron in boreal river catchments: biogeochemical, ecological and management implications. Sci Total Environ 805:150256. https://doi.org/10.1016/J.SCITOTENV.2021.150256

    Article  PubMed  Google Scholar 

  20. Huhe CX, Hou F, Wu YP, Cheng YX (2017) Bacterial and fungal community structures in loess plateau grasslands with different grazing intensities. Front Microbiolo 8:606. https://doi.org/10.3389/fmicb.2017.00606

    Article  CAS  Google Scholar 

  21. Jiao S, Yang YF, Xu YQ, Zhang J, Lu YH (2020) Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME J 14(1):202–216. https://doi.org/10.1038/s41396-019-0522-9

    Article  PubMed  Google Scholar 

  22. Kim J, Park B, Choi J, Park M, Lee JM, Kim K, Kim Y (2021) Optimum detailed standards to control non-point source pollution priority panagement areas: centered on highland agriculture watershed. Sustainability 13(17):9842–9842. https://doi.org/10.3390/SU13179842

    Article  CAS  Google Scholar 

  23. Li CC, Quan Q, Gan YD, Dong JY, Fang JH, Wang LF, Liu J (2020) Effects of heavy metals on microbial communities in sediments and establishment of bioindicators based on microbial taxa and function for environmental monitoring and management. Sci Total Environ 749:141555. https://doi.org/10.1016/j.scitotenv.2020.141555

    Article  CAS  PubMed  Google Scholar 

  24. Li JY, Chen QF, Li Q, Zhao CS, Feng Y (2021) Influence of plants and environmental variables on the diversity of soil microbial communities in the Yellow River Delta Wetland. China Chemosphere 274:129967. https://doi.org/10.1016/j.chemosphere.2021.129967

    Article  CAS  PubMed  Google Scholar 

  25. Li N, Chen X, Zhao H, Tang J, Jiang G, Li Z, Li X, Chen S, Zou S, Dong K, Xu Q (2020) Spatial distribution and functional profile of the bacterial community in response to eutrophication in the subtropical Beibu Gulf. China Mar Pollut Bull 161:111742. https://doi.org/10.1016/j.marpolbul.2020.111742

    Article  CAS  PubMed  Google Scholar 

  26. Li QX, Feng J, Wu JJ, Jia W, Zhang Q, Chen Q, Zhang DD, Cheng XL (2019) Spatial variation in soil microbial community structure and its relation to plant distribution and local environments following afforestation in central China. Soil Till Res 193:8–16. https://doi.org/10.1016/j.still.2019.05.015

    Article  Google Scholar 

  27. Li Y.J., Wang H., Zhao J.N., Huang P.C.H., Yang D.L., 2015. Effects of tillage methods on soil physicochemical properties and biological characteristics in farmland: a review. Chinese J. Appl. Ecol. 26(3): 939–948. https://doi.org/10.13287/j.1001-9332.20150106.018.

  28. Lin YB, Ye YM, Hu YM, Shi HK (2019) The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotox environ Safe 180:557–564. https://doi.org/10.1016/j.ecoenv.2019.05.057

    Article  CAS  Google Scholar 

  29. Liu JL, Le TH, Zhu HN, Yao YA, Zhu HL, Cao Y, Zhao Z (2020) Afforestation of cropland fundamentally alters the soil fungal community. Plant Soil 457(1–2):279–292. https://doi.org/10.1007/s11104-020-04739-2

    Article  CAS  Google Scholar 

  30. Liu XM, Wang D, Wang L, Tang JC (2022) Dissolved biochar eliminates the effect of Cu (II) on the transfer of antibiotic resistance genes between bacteria. J Hazard Mater 424:127251. https://doi.org/10.1016/J.JHAZMAT.2021.127251

    Article  CAS  PubMed  Google Scholar 

  31. Liu Y, Zhang JX, Zhang XL, Xie SG (2014) Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Appl Microbiol Biot 98(12):5697–5707. https://doi.org/10.1007/s00253-014-5651-5

    Article  CAS  Google Scholar 

  32. Purahong W, Kruger D, Buscot F, Wubet T (2016) Correlations between the composition of modular fungal communities and litter decomposition-associated ecosystem functions. Fungal Ecol 22:106–114. https://doi.org/10.1016/j.funeco.2016.04.009

    Article  Google Scholar 

  33. Schmidt R, Mitchell J, Scow K (2019) Cover cropping and no-till increase diversity and symbiotroph: saprotroph ratios of soil fungal communities. Soil Biol Biochem 129:99–109. https://doi.org/10.1016/j.soilbio.2018.11.010

    Article  CAS  Google Scholar 

  34. Zhou J.B., Jin Z.J., Xiao Y.Y.,Leng M., Wang X.T., Pan F.J., 2021. Investigation of soil fungal communities and functionalities within karst paddy field. Environ. Sci. 42(08): 4005–4014. https://doi.org/10.13227/j.hjkx.202011164.

  35. Sheik CS, Mitchell TW, Rizvi FZ, Rehman Y, Faisal M, Hasnain S, McInerney MJ, Krumholz LR (2012) Exposure of soil microbial communities to chromium andarsenic alters their diversity and structure. PLOS ONE 7(6):e40059. https://doi.org/10.1371/journal.pone.0040059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Song F.M., Guo D.D., Chen Y.G., Yang Q.L., Wang W.M., 2020. Influence of industrial organic pollution on fungal community in the sediment of small water body. Microbiol. China 47(10): 3216−3225. https://doi.org/10.13344/j.microbiol.china.200170.

  37. Sun SY, Zhang JF, Cai CJ, Cai ZY, Li XG, Wang RJ (2020) Coupling of non-point source pollution and soil characteristics covered by Phyllostachys edulis stands in hilly water source area. J Environ Manage 268:110657. https://doi.org/10.1016/j.jenvman.2020.110657

    Article  CAS  PubMed  Google Scholar 

  38. Mushi D, Kebede G, Linke RB, Lakew A, Hayes DS, Graf W, Farnleitner AH (2021) Microbial faecal pollution of river water in a watershed of tropical Ethiopian highlands is driven by diffuse pollution sources. J Water Health 19(4):575–591. https://doi.org/10.2166/wh.2021.269

    Article  PubMed  Google Scholar 

  39. Wang HL, He P, Shen CY, Wu ZN (2019) Effect of irrigation amount and fertilization on agriculture non-point source pollution in the paddy field. Environ Sci Pollut R 26(10):10363–10373. https://doi.org/10.1007/s11356-019-04375-z

    Article  Google Scholar 

  40. Wang JW, Chen Y, Cai PG, Gao Q, Zhong HH, Sun WL, Chen Q (2022) Impacts of municipal wastewater treatment plant discharge on microbial community structure and function of the receiving river in Northwest Tibetan Plateau. J Hazard Mater 423:127170. https://doi.org/10.1016/j.jhazmat.2021.127170

    Article  CAS  PubMed  Google Scholar 

  41. Wang M, Shi S, Lin F, Jiang P (2014) Response of the soil fungal community to multi-factor environmental changes in a temperate forest. Appl Soil Ecol 81:45–56. https://doi.org/10.1016/j.apsoil.2014.04.008

    Article  Google Scholar 

  42. Wang Q.H., Ren Y.F., Meng L., Li H., Fu H.M., Wang H.F., 2013. Simultaneous determination of total nitrogen and organic carbon in soil with an elemental analyzer. Chinese Journal of analysis Laboratory. 32: 41–45. https://doi.org/10.13595/j.cnki.issn1000-0720.2013.0265.

  43. Wang R, Xu SJ, Jiang CC, Zhang Y, Bai N, Zhuang GQ, Bai ZH, Zhuang XL (2019) Impacts of human activities on the composition and abundance of sulfate-reducing and sulfur-oxidizing microorganisms in polluted river sediments. Front Microbio 10:231. https://doi.org/10.3389/fmicb.2019.00231

    Article  CAS  Google Scholar 

  44. Wang YH, Li SF, Lang XD, Huang XB, Su JR (2022) Effects of microtopography on soil fungal community diversity, composition, and assembly in a subtropical monsoon evergreen broadleaf forest of Southwest China. CATENA 211:106025. https://doi.org/10.1016/j.catena.2022.106025

    Article  Google Scholar 

  45. Wu L, Misselbrook TH, Feng LP, Wu LH (2020) Assessment of nitrogen uptake and biological nitrogen fixation responses of soybean to nitrogen fertiliser with SPACSYS. Sustainability 12(15):5921. https://doi.org/10.3390/su12155921

    Article  CAS  Google Scholar 

  46. Wu JY, Hua ZL, Gu L (2021) Planktonic microbial responses to perfluorinated compound (PFC) pollution: integrating PFC distributions with community coalescence and metabolism. Sci Total Environ 788:147743. https://doi.org/10.1016/j.scitotenv.2021.147743

    Article  CAS  PubMed  Google Scholar 

  47. Wu YH, Rene ER, Zhou MH, Tiwari A (2020) Non-point source pollution control and aquatic ecosystem protection-an introduction. Bioresource Technol 316:123956. https://doi.org/10.1016/j.biortech.2020.123956

    Article  CAS  Google Scholar 

  48. Xiang SZ, Li YQ, Wang WY, Zhang B, Shi WY, Zhang J, Huang FY, Liu F, Guan XY (2021) Antibiotics adaptation costs alter carbon sequestration strategies of microorganisms in karst river. Environ Pollut 288:117819. https://doi.org/10.1016/j.envpol.2021.117819

    Article  CAS  PubMed  Google Scholar 

  49. Xi M, Kong FL, Lv XG, Jiang M, Li Y (2015) Spatial variation of dissolved organic carbon in soils of riparian wetlands and responses to Hydro-geomorphologic changes in Sanjiang Plain. China Chin Geogra Sci 25(2):174–183. https://doi.org/10.1007/s11769-015-0744-3

    Article  Google Scholar 

  50. Xu F., Zhang T., Huai B.D., Sui W.Z., Yang X., 2021. Effects of land use changes on soil fungal community structure and function in the riparian wetland along the downstream of Songhua River. Environ. Sci. 42(5): 2531–2540. https://doi.org/10.13227/J.HJKX.202008307.

  51. Xu Z, Woodhouse JN, Te SH, Gin KYH, He YL, Xu C, Chen L (2018) Seasonal variation in the bacterial community composition of a large estuarine reservoir and response to cyanobacterial proliferation. Chemosphere 202:576–585. https://doi.org/10.1016/j.chemosphere.2018.03.037

    Article  CAS  PubMed  Google Scholar 

  52. Yang M.Y., Pan X.Y., Liu H.L., Yu L., Chen H., Wang J.W., 2020. Urban non-point pollution characteristics in China: a meta-analysis. Ecol. Environ. Sci. 29(08): 1634–1644. https://doi.org/10.16258/j.cnki.1674-5906.2020.08.015.

  53. Yano KA, Geronimo FK, Reyes NJ, Kim LH (2021) Characterization and comparison of microplastic occurrence in point and non-point pollution sources. Sci Total Environ 797(25):148939. https://doi.org/10.1016/j.scitotenv.2021.148939

    Article  CAS  PubMed  Google Scholar 

  54. Zhang T, Ni JP, Xie DT (2015) Severe situation of rural nonpoint source pollution and efficient utilization of agricultural wastes in the Three Gorges Reservoir Area. Environ Sci Pollut R 22(21):16453–16462. https://doi.org/10.1007/s11356-015-5429-z

    Article  Google Scholar 

  55. Zheng B.H., Wang X.Y., Li Y.J., Chen Y, Li B.L., Li Y.Y., Chen Z.J., 2021. Community structure, function, and influencing factors of planktonic fungi in the Danjiangkou reservoir. Environ. Sci. 42(1): 234–241. https://doi.org/10.13227/j.hjkx.202006192.

  56. Zhao CS, Pan X, Yang ST, Xiang H, Zhao J, Gan XJ, Ding SY, Yu Q (2021) Effects and prediction of nonpoint source pollution on the structure of aquatic food webs. Ecohydrology 14(1):e2257. https://doi.org/10.1002/eco.2257

    Article  Google Scholar 

  57. Zhao ZL, Li HJ, Sun Y, Zhan AB, Lan WL, Woo SP, Shau-Hwai AT, Fan JF (2022) Bacteria versus fungi for predicting anthropogenic pollution in subtropical coastal sediments: assembly process and environmental response. Ecol Indic 134:108484. https://doi.org/10.1016/j.ecolind.2021.108484

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank for the American Journal Expert agent (AJE) to help with the manuscript revision.

Funding

This study was financially supported by the Science Research Program of China West Normal University (Project No. 19E061), the Tianfu Scholar Program of Sichuan Province (Project No. 2020–17), the Environmental Protection Research Program of the Yangtze River (Project No. CJZDZYJ47), and the National Science Foundation of China (NSFC) (Project No. 41907132).

Author information

Authors and Affiliations

Authors

Contributions

Fei Xu: writing–original draft preparation; Lanping Zhu: reviewing, checking, and editing; Yuqin Xue: investigation; Kunhe Liu: software, data curation; Fubin Zhang: software, data curation; Tuo Zhang: conceptualization, supervision, funding acquisition.

Corresponding author

Correspondence to Tuo Zhang.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Ethics Approval

Not applicable.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 393 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, F., Zhu, L., Wang, J. et al. Nonpoint Source Pollution (NPSP) Induces Structural and Functional Variation in the Fungal Community of Sediments in the Jialing River, China. Microb Ecol 85, 1308–1322 (2023). https://doi.org/10.1007/s00248-022-02009-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-022-02009-5

Keywords

Navigation