Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach

Abstract Background Polycyclic aromatic hydrocarbon (PAH) contamination has been a worldwide environmental issue because of its impact on ecosystems and human health. Biodegradation plays an important role in PAH removal in natural environments. To date, many PAH-degrading strains and degradation ge...

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Main Authors: Yue Huang, Liguan Li, Xiaole Yin, Tong Zhang
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Environmental Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40793-023-00497-7
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author Yue Huang
Liguan Li
Xiaole Yin
Tong Zhang
author_facet Yue Huang
Liguan Li
Xiaole Yin
Tong Zhang
author_sort Yue Huang
collection DOAJ
description Abstract Background Polycyclic aromatic hydrocarbon (PAH) contamination has been a worldwide environmental issue because of its impact on ecosystems and human health. Biodegradation plays an important role in PAH removal in natural environments. To date, many PAH-degrading strains and degradation genes have been reported. However, a comprehensive PAH-degrading gene database is still lacking, hindering a deep understanding of PAH degraders in the era of big data. Furthermore, the relationships between the PAH-catabolic genotype and phenotype remain unclear. Results Here, we established a bacterial PAH-degrading gene database and explored PAH biodegradation capability via a genome-function relationship approach. The investigation of functional genes in the experimentally verified PAH degraders indicated that genes encoding hydratase-aldolase could serve as a biomarker for preliminarily identifying potential degraders. Additionally, a genome-centric interpretation of PAH-degrading genes was performed in the public genome database, demonstrating that they were ubiquitous in Proteobacteria and Actinobacteria. Meanwhile, the global phylogenetic distribution was generally consistent with the culture-based evidence. Notably, a few strains affiliated with the genera without any previously known PAH degraders (Hyphomonas, Hoeflea, Henriciella, Saccharomonospora, Sciscionella, Tepidiphilus, and Xenophilus) also bore a complete PAH-catabolic gene cluster, implying their potential of PAH biodegradation. Moreover, a random forest analysis was applied to predict the PAH-degrading trait in the complete genome database, revealing 28 newly predicted PAH degraders, of which nine strains encoded a complete PAH-catabolic pathway. Conclusions Our results established a comprehensive PAH-degrading gene database and a genome-function relationship approach, which revealed several potential novel PAH-degrader lineages. Importantly, this genome-centric and function-oriented approach can overcome the bottleneck of conventional cultivation-based biodegradation research and substantially expand our current knowledge on the potential degraders of environmental pollutants.
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spelling doaj.art-4147d42228094e409092e31b3dde82eb2023-05-07T11:24:51ZengBMCEnvironmental Microbiome2524-63722023-04-0118111310.1186/s40793-023-00497-7Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approachYue Huang0Liguan Li1Xiaole Yin2Tong Zhang3Environmental Microbiome Engineering and Biotechnology Lab, Department of Civil Engineering, The University of Hong KongEnvironmental Microbiome Engineering and Biotechnology Lab, Department of Civil Engineering, The University of Hong KongEnvironmental Microbiome Engineering and Biotechnology Lab, Department of Civil Engineering, The University of Hong KongEnvironmental Microbiome Engineering and Biotechnology Lab, Department of Civil Engineering, The University of Hong KongAbstract Background Polycyclic aromatic hydrocarbon (PAH) contamination has been a worldwide environmental issue because of its impact on ecosystems and human health. Biodegradation plays an important role in PAH removal in natural environments. To date, many PAH-degrading strains and degradation genes have been reported. However, a comprehensive PAH-degrading gene database is still lacking, hindering a deep understanding of PAH degraders in the era of big data. Furthermore, the relationships between the PAH-catabolic genotype and phenotype remain unclear. Results Here, we established a bacterial PAH-degrading gene database and explored PAH biodegradation capability via a genome-function relationship approach. The investigation of functional genes in the experimentally verified PAH degraders indicated that genes encoding hydratase-aldolase could serve as a biomarker for preliminarily identifying potential degraders. Additionally, a genome-centric interpretation of PAH-degrading genes was performed in the public genome database, demonstrating that they were ubiquitous in Proteobacteria and Actinobacteria. Meanwhile, the global phylogenetic distribution was generally consistent with the culture-based evidence. Notably, a few strains affiliated with the genera without any previously known PAH degraders (Hyphomonas, Hoeflea, Henriciella, Saccharomonospora, Sciscionella, Tepidiphilus, and Xenophilus) also bore a complete PAH-catabolic gene cluster, implying their potential of PAH biodegradation. Moreover, a random forest analysis was applied to predict the PAH-degrading trait in the complete genome database, revealing 28 newly predicted PAH degraders, of which nine strains encoded a complete PAH-catabolic pathway. Conclusions Our results established a comprehensive PAH-degrading gene database and a genome-function relationship approach, which revealed several potential novel PAH-degrader lineages. Importantly, this genome-centric and function-oriented approach can overcome the bottleneck of conventional cultivation-based biodegradation research and substantially expand our current knowledge on the potential degraders of environmental pollutants.https://doi.org/10.1186/s40793-023-00497-7PAHBiodegradationDatabase miningFunctional geneGenome-centric analysisGenotype–phenotype relationship
spellingShingle Yue Huang
Liguan Li
Xiaole Yin
Tong Zhang
Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
Environmental Microbiome
PAH
Biodegradation
Database mining
Functional gene
Genome-centric analysis
Genotype–phenotype relationship
title Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
title_full Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
title_fullStr Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
title_full_unstemmed Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
title_short Polycyclic aromatic hydrocarbon (PAH) biodegradation capacity revealed by a genome-function relationship approach
title_sort polycyclic aromatic hydrocarbon pah biodegradation capacity revealed by a genome function relationship approach
topic PAH
Biodegradation
Database mining
Functional gene
Genome-centric analysis
Genotype–phenotype relationship
url https://doi.org/10.1186/s40793-023-00497-7
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AT xiaoleyin polycyclicaromatichydrocarbonpahbiodegradationcapacityrevealedbyagenomefunctionrelationshipapproach
AT tongzhang polycyclicaromatichydrocarbonpahbiodegradationcapacityrevealedbyagenomefunctionrelationshipapproach