Dataset Information

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 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.

SUBMITTER: Huang Y

PROVIDER: S-EPMC10150532 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Publications

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

Huang Yue Y Li Liguan L Yin Xiaole X Zhang Tong T

Environmental microbiome 20230430 1

<h4>Background</h4>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 bet ...[more]

PMID: 37122013

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Project description:Arsenic and polycyclic aromatic hydrocarbons (PAH) are environmental pollutants to which people around the world are exposed through water, food and air. In mouse and in vitro studies of human cells, both of these chemicals have been shown to modulate the immune system. In some experimental studies, a synergistic disruption of immune function was observed by a combined exposure to arsenic and PAH. However, a joint effect of arsenic and PAH on immune function has not been studied in humans. We have conducted an epidemiological investigation to examine effects of chronic arsenic and PAH exposures on immune function. We assessed T-cell proliferation (TCP) and cytokine production of anti-CD3/anti-CD28 stimulated lymphocytes in human peripheral blood mononuclear cells (HPBMC) among 197 healthy men enrolled to the Health Effects of Arsenic Longitudinal (HEALS) cohort in Bangladesh. By design, approximately half were active smokers and the rest were never smokers. Our analyses demonstrated that IL-1b, IL-2, IL-4 and IL-6 were significantly stimulated as a function of urinary arsenic levels in models adjusted for age, body mass index (BMI), smoking status and PAH-DNA adducts. After correcting for false detection rate (FDR), only IL-1b remained statistically significant. We found a U-shaped dose response relationship between urinary arsenic and IL-1b. On the other hand, PAH-DNA adducts were associated with an inhibition of TCP and appeared as an inverted U-shape curve. Dose response curves were non-monotonic for PAH-DNA adduct exposures and suggested that cytokine secretion of IFNg, IL-1b, IL-2, IL-10 and IL17A followed a complex pattern. In the majority of donors, there was a trend towards a decrease in cytokine associated with PAH-DNA adducts. We did not observe any interaction between urinary arsenic and PAH-DNA adducts on immune parameters. Our results indicate that long-term exposures to arsenic and PAH have independent, non-monotonic associations with TCP and cytokine production.

Project description:Bacteria play an important role in the removal of polycyclic aromatic hydrocarbons (PAHs) from polluted environments. In marine environments, Cycloclasticus is one of the most prevalent PAH-degrading bacterial genera. However, little is known regarding the degradation mechanisms for multiple PAHs by CycloclasticusCycloclasticus sp. strain P1 was isolated from deep-sea sediments and is known to degrade naphthalene, phenanthrene, pyrene, and other aromatic hydrocarbons. Here, six ring-hydroxylating dioxygenases (RHDs) were identified in the complete genome of Cycloclasticus sp. P1 and were confirmed to be involved in PAH degradation by enzymatic assays. Further, five gene clusters in its genome were identified to be responsible for PAH degradation. Degradation pathways for naphthalene, phenanthrene, and pyrene were elucidated in Cycloclasticus sp. P1 based on genomic and transcriptomic analysis and characterization of an interconnected metabolic network. The metabolic pathway overlaps in many steps in the degradation of pyrene, phenanthrene, and naphthalene, which were validated by the detection of metabolic intermediates in cultures. This study describes a pyrene degradation pathway for Cycloclasticus. Moreover, the study represents the integration of a PAH metabolic network that comprises pyrene, phenanthrene, and naphthalene degradation pathways. Taken together, these results provide a comprehensive investigation of PAH metabolism in CycloclasticusIMPORTANCE PAHs are ubiquitous in the environment and are carcinogenic compounds and tend to accumulate in food chains due to their low bioavailability and poor biodegradability. Cycloclasticus is an obligate marine PAH degrader and is widespread in marine environments, while the PAH degradation pathways remain unclear. In this report, the degradation pathways for naphthalene, phenanthrene, and pyrene were revealed, and an integrated PAH metabolic network covering pyrene, phenanthrene, and naphthalene was constructed in Cycloclasticus This overlapping network provides streamlined processing of PAHs to intermediates and ultimately to complete mineralization. Furthermore, these results provide an additional context for the prevalence of Cycloclasticus in oil-polluted marine environments and pelagic settings. In conclusion, these analyses provide a useful framework for understanding the cellular processes involved in PAH metabolism in an ecologically important marine bacterium.

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Dataset Information

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

Background

Results

Conclusions

Publications

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

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