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Excess copper promotes catabolic activity of gram-positive bacteria and resistance of gram-negative bacteria but inhibits fungal community in soil

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Abstract

The extensive use of copper fungicides has resulted in significant non-target effects on soil microbial communities. However, the documented effects are often variable and contradictory, depending on the methods used to assess them. In this study, we examined the effects of copper accumulation in surface soils on microbial catabolic activity, active biomass and composition, and sensitive bacterial species. The community-level catabolic profiles (CLCPs) showed that both normal (50 mg CuSO4 kg−1 soil) and high dosages (tenfold rate) of CuSO4 significantly increased the catabolic diversity of gram-positive bacteria, while the high dosage increased the overall catabolic activity of gram-negative bacteria. The phospholipid fatty acid (PLFA) analysis showed that the high dosage reduced the biomass of gram-positive bacteria by 27% but did not affect that of gram-negative bacteria. In comparison, the normal and high dosages decreased the fungal biomass by 34% and 58%, respectively. Furthermore, 16S rRNA-denaturing gradient gel electrophoresis (DGGE) fingerprint revealed that more than two-thirds of identified bands belonged to gram-negative bacteria. Some Cu-resistant gram-negative bacterial genera, such as Actinobacterium, Pseudomonas, and Proteobacterium, were detected in the soil to which the high dosage of CuSO4 had been applied. In conclusion, an excess application of CuSO4 increased the catabolic diversity of gram-positive bacteria and induced resistance in gram-negative bacteria, whereas the active fungal community displayed a dosage-dependent response to CuSO4 and can thus be used as a sensitive indicator of copper contamination.

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Acknowledgements

We thank Jianfang Feng from State Key Laboratory of Pollution Control and Resource Reuse in the School of Environment of Nanjing University for her assistance with the GC-MS analysis. We are very grateful to Mr. Robert Luan and Dr. Muhammad Fahad Sardar for their helpful comments in composing the manuscript.

Funding

This work was financially supported by the National Natural Science Foundation of China (NSFC) (31870495, 31372140, 40371071), the Program for Changjiang Scholars and Innovative Research Team in University (IRT_14R27), and the Fundamental Research Funds for the Central Universities (No. 020814380002).

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YHY and ZH acquired funds, designed, and supervised the research. MKY, YHL1, YHL2, ZLW, AYF, and YCL performed the experimental work and analyzed the data. MKY, YCL, and YHY wrote the manuscript. All discussed the results and edited/commented on the manuscript.

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Correspondence to Zhi Hong, Yongchun Li or Yonghua Yang.

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The authors declare no competing interests.

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Responsible Editor: Robert Duran

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Yang, M., Liu, Y., Liao, Y. et al. Excess copper promotes catabolic activity of gram-positive bacteria and resistance of gram-negative bacteria but inhibits fungal community in soil. Environ Sci Pollut Res 29, 22602–22612 (2022). https://doi.org/10.1007/s11356-021-17510-6

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  • DOI: https://doi.org/10.1007/s11356-021-17510-6

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