Huang Yue, Li Liguan, Yin Xiaole, Zhang Tong
Environmental Microbiome Engineering and Biotechnology Lab, Department of Civil Engineering, The University of Hong Kong, Pokfulam Road, Hong Kong, China.
Environ Microbiome. 2023 Apr 30;18(1):39. doi: 10.1186/s40793-023-00497-7.
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.
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.
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.
多环芳烃（PAH）污染因其对生态系统和人类健康的影响，已成为一个全球性的环境问题。生物降解在自然环境中PAH的去除过程中起着重要作用。迄今为止，已报道了许多PAH降解菌株和降解基因。然而，仍然缺乏一个全面的PAH降解基因数据库，这阻碍了在大数据时代对PAH降解菌的深入了解。此外，PAH分解代谢基因型与表型之间的关系仍不明确。
在此，我们建立了一个细菌PAH降解基因数据库，并通过基因组-功能关系方法探索了PAH生物降解能力。对经实验验证的PAH降解菌中的功能基因进行研究表明，编码水化酶-醛缩酶的基因可作为初步鉴定潜在降解菌的生物标志物。此外，在公共基因组数据库中对PAH降解基因进行了以基因组为中心的解读，结果表明它们在变形菌门和放线菌门中普遍存在。同时，全球系统发育分布总体上与基于培养的证据一致。值得注意的是，一些隶属于此前未知有任何PAH降解菌的属（生丝微菌属、霍夫勒菌属、亨利氏菌属、糖单孢菌属、裂丝菌属、嗜热栖菌属和嗜异源菌属）的菌株也携带完整的PAH分解代谢基因簇，这意味着它们具有PAH生物降解的潜力。此外，应用随机森林分析在完整基因组数据库中预测PAH降解特性，发现了28个新预测的PAH降解菌，其中9个菌株编码完整的PAH分解代谢途径。
我们的研究结果建立了一个全面的PAH降解基因数据库和一种基因组-功能关系方法，揭示了几个潜在的新型PAH降解菌谱系。重要的是，这种以基因组为中心和以功能为导向的方法可以克服传统基于培养的生物降解研究的瓶颈，并大幅扩展我们目前对环境污染物潜在降解菌的认识。
