Metagenomic analysis of petroleum biodegradation coupled to specific N-cycling process in oil-contaminated soil

• Published in: Applied soil ecology : a section of Agriculture, ecosystems & environment Vol. 193; p. 105144
• Main Authors: Kong, Lulu, Xu, Tiebing, Wang, Zepeng, Wen, Xueyou, Jiao, Zhen, Liu, Jingze
• Format: Journal Article
• Language: English
• Published: Elsevier B.V 01.01.2024
• Subjects: Crude oil contamination; DNRA; Metagenomics; N-cycling; Petroleum hydrocarbons biodegradation; Soil microbiome; TPHs; PCoA; NAS; Metagenomics; CK soil; NR; LDA; LP soil; RDA; ANOVA; NCBI; DNRA; KEGG; GOGAT; soil C/N ratio; GC–MS; AMO; TCA cycle; DIN; TOC; HP soil; GS; ANOSIM; MMO; SOM; LEfSe; NAD; Petroleum hydrocarbons biodegradation; NMO; N-cycling; Crude oil contamination; ORFs; Soil microbiome; PAHs; PHs; TN; NADH or NAD(P)H; TP
• ISSN: 0929-1393; 1873-0272
• DOI: 10.1016/j.apsoil.2023.105144

With the increased soil contamination by crude oil, understanding the effects on the metabolic potential of petroleum hydrocarbons (PHs) as well as its coupling to nitrogen-cycling (N-cycling) is crucial for improving the efficiency of in-situ bioremediation. Chemical measurements combined with metagenomic sequencing were used to investigate soils with different oiling intensity in coastal area. We suggested that oil contamination exerted strong impacts on soil properties with increased ammonium but decreased nitrite and nitrate concentrations. Taxonomic analysis revealed that oil contamination molded a unique microbial community structure with a bias towards the PHs-degrading specific populations with halophilic and oligotrophic characteristics. Alcanivorax, Marinobacter and some other potential PHs degraders were also nitrate reducing bacteria, and thus involved in both PHs biodegradation and N-cycling pathways. Microbial community structure was mainly explained by soil C/N ratio based on redundancy analysis (RDA) results. Further, functional metagenomics demonstrated that the genetic potential of PHs oxidation as well as dissimilatory nitrate reduction to ammonium (DNRA) and N-fixation was activated by oil contamination. Overall, metagenomic results in conjunction with co-occurrence network demonstrated that PHs oxidation probably coupled to DNRA, N-fixation and N-immobilization in the contaminated soil. PHs biodegradation was coupled to DNRA by the electrons transfer to nitrate/nitrite. Ammonium accumulated through N-fixation and DNRA processes could be utilized by PHs-degrading heterotrophs through N-immobilization, which was another way that connected to PHs biodegradation. [Display omitted] •Alcanivorax and Marinobacter were involved in both PHs biodegradation and N-cycling.•PHs biodegradation coupled to DNRA, N-fixation and N immobilization.•PHs oxidation was coupled to DNRA by providing electrons to nitrate/nitrite.•Ammonium accumulated by DNRA and N-fixation was utilized by PHs degraders.