Determination of soil phenanthrene degradation through a fungal–bacterial consortium

Author:

Luo Chunling12ORCID,Guan Guoqing12,Dai Yeliang12,Cai Xixi3,Huang Qihui4,Li Jibing12ORCID,Zhang Gan12

Affiliation:

1. State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, China

2. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China

3. Guangdong Key Laboratory of Ornamental Plant Germplasm Innovation and Utilization, Environmental Horticulture Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China

4. Guangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou, China

Abstract

ABSTRACT Fungal–bacterial consortia enhance organic pollutant removal, but the underlying mechanisms are unclear. We used stable isotope probing (SIP) to explore the mechanism of bioaugmentation involved in polycyclic aromatic hydrocarbon (PAH) biodegradation in petroleum-contaminated soil by introducing the indigenous fungal strain A spergillus sp. LJD-29 and the bacterial strain P seudomonas XH-1. While each strain alone increased phenanthrene (PHE) degradation, the simultaneous addition of both strains showed no significant enhancement compared to treatment with XH-1 alone. Nonetheless, the assimilation effect of microorganisms on PHE was significantly enhanced. SIP revealed a role of XH-1 in PHE degradation, while the absence of LJD-29 in 13 C-DNA indicated a supporting role. The correlations between fungal abundance, degradation efficiency, and soil extracellular enzyme activity indicated that LJD-29, while not directly involved in PHE assimilation, played a crucial role in the breakdown of PHE through extracellular enzymes, facilitating the assimilation of metabolites by bacteria. This observation was substantiated by the results of metabolite analysis. Furthermore, the combination of fungus and bacterium significantly influenced the diversity of PHE degraders. Taken together, this study highlighted the synergistic effects of fungi and bacteria in PAH degradation, revealed a new fungal–bacterial bioaugmentation mechanism and diversity of PAH-degrading microorganisms, and provided insights for in situ bioremediation of PAH-contaminated soil. IMPORTANCE This study was performed to explore the mechanism of bioaugmentation by a fungal–bacterial consortium for phenanthrene (PHE) degradation in petroleum-contaminated soil. Using the indigenous fungal strain Aspergillus sp. LJD-29 and bacterial strain Pseudomonas XH-1, we performed stable isotope probing (SIP) to trace active PHE-degrading microorganisms. While inoculation of either organism alone significantly enhanced PHE degradation, the simultaneous addition of both strains revealed complex interactions. The efficiency plateaued, highlighting the nuanced microbial interactions. SIP identified XH-1 as the primary contributor to in situ PHE degradation, in contrast to the limited role of LJD-29. Correlations between fungal abundance, degradation efficiency, and extracellular enzyme activity underscored the pivotal role of LJD-29 in enzymatically facilitating PHE breakdown and enriching bacterial assimilation. Metabolite analysis validated this synergy, unveiling distinct biodegradation mechanisms. Furthermore, this fungal–bacterial alliance significantly impacted PHE-degrading microorganism diversity. These findings advance our understanding of fungal–bacterial bioaugmentation and microorganism diversity in polycyclic aromatic hydrocarbon (PAH) degradation as well as providing insights for theoretical guidance in the in situ bioremediation of PAH-contaminated soil.

Funder

MOST | National Natural Science Foundation of China

Guangdong Foundation for Program of Science and Technology Research

GDSTC | Natural Science Foundation of Guangdong Province

Youth Innovation Promotion Association of the Chinese Academy of Sciences

Publisher

American Society for Microbiology

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