Identification of a putative novel polycyclic aromatic hydrocarbon-biodegrading gene cluster in a marine Roseobacteraceae bacterium Sagittula sp. MA-2.

IF 3.7 2区 生物学 Q2 MICROBIOLOGY Microbiology spectrum Pub Date : 2024-11-27 DOI:10.1128/spectrum.01074-24
Mayuko Abe, Miharu Sakai, Robert A Kanaly, Jiro F Mori
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Abstract

The ability to biodegrade polycyclic aromatic hydrocarbons (PAHs) and the catabolic enzymes responsible for PAH biotransformation in marine bacteria belonging to the family Roseobacteraceae remain largely unexplored despite their wide distribution and highly diverse physiological traits. A bacterial isolate within Roseobacteraceae originating from coastal seawater, Sagittula sp. strain MA-2, that biotransformed phenanthrene and utilized it as a growth substrate was found to possess a putative PAH-degrading gene cluster on one of the eight circular plasmids in its genome. Subsequent comprehensive investigations utilizing bacterial genomes in public databases revealed that gene clusters potentially homologous to this newly found cluster are widely but heterogeneously distributed within Roseobacteraceae and a few non-Roseobacteraceae (Paracoccaceae and Rhizobiaceae) strains from saline environments. Catabolic functions of the enzymes encoded in strain MA-2 were predicted through the profiling of phenanthrene biotransformation products by liquid chromatography-electrospray ionization high-resolution mass spectrometry and substrate docking simulations using predicted three-dimensional structures of selected proteins, and phenanthrene biodegradation pathways were proposed. Strain MA-2 appeared to biodegrade phenanthrene via two separated, concurrent pathways, namely the salicylate and phthalate pathways. This study serves as the first investigation into the functional genes potentially responsible for PAH biodegradation conserved in Roseobacteraceae bacteria, expanding scientific understanding of the physiological repertoire evolved in this ubiquitous marine bacterial group.

Importance: The ocean is often characterized as the terminal destination for persistent polycyclic aromatic hydrocarbon (PAH) environmental pollutants; however, the ability to biodegrade PAHs and the corresponding enzymes conserved among marine bacteria are less understood compared to their terrestrial counterparts. A marine bacterial isolate, Sagittula sp. strain MA-2, belonging to the family Roseobacteraceae-a widely distributed and physiologically diverse marine bacterial group-was found to possess a functional gene cluster encoding enzymes potentially responsible for PAH biodegradation in its genome and exhibit the ability to biodegrade the three-ring PAH, phenanthrene. Intriguingly, gene clusters potentially homologous to this cluster were also distributed broadly across genomes from different Roseobacteraceae genera in public databases, which has not been previously investigated. The knowledge provided here expands our understanding of the physiology of Roseobacteraceae and may be applied to explore biotechnologically useful bacteria that contribute to the remediation of polluted marine environments or high-salinity wastewater.

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鉴定海洋玫瑰菌科细菌 Sagittula sp. MA-2 中的推定新型多环芳烃生物降解基因簇。
尽管玫瑰细菌科(Roseobacteraceae)的海洋细菌分布广泛,生理特征多种多样,但它们生物降解多环芳烃(PAHs)的能力以及负责多环芳烃生物转化的分解酶在很大程度上仍未得到研究。Roseobacteraceae 属下的一个细菌分离株 Sagittula sp. 菌株 MA-2 源自沿海海水,它能对菲进行生物转化并将其作为生长底物,研究发现,在其基因组的八个环形质粒中的一个质粒上具有一个假定的多环芳烃降解基因簇。随后,利用公共数据库中的细菌基因组进行的综合研究发现,与这一新发现基因簇可能同源的基因簇广泛分布于盐碱环境中的玫瑰细菌科(Roseobacteraceae)和少数非玫瑰细菌科(Paracoccaceae和Rhizobiaceae)菌株中,但分布不均。通过液相色谱-电喷雾离子化高分辨质谱分析菲的生物转化产物,并利用所选蛋白质的三维结构预测底物对接模拟,预测了菌株 MA-2 中编码的酶的分解功能,并提出了菲的生物降解途径。菌株 MA-2 似乎通过两种分离的、同时发生的途径(即水杨酸酯途径和邻苯二甲酸酯途径)降解菲。这项研究首次调查了玫瑰杆菌科细菌中可能负责多环芳烃(PAH)生物降解的功能基因,拓展了科学界对这一无处不在的海洋细菌群所演化的生理特性的认识:海洋通常被描述为持久性多环芳烃(PAH)环境污染物的最终目的地;然而,与陆地细菌相比,人们对海洋细菌生物降解多环芳烃的能力和相应酶的了解较少。研究发现,一种海洋细菌分离物 Sagittula sp.耐人寻味的是,与该基因簇可能同源的基因簇也广泛分布于公共数据库中不同玫瑰细菌属的基因组中,而这是以前从未研究过的。本文提供的知识拓展了我们对玫瑰细菌科生理机能的了解,可用于探索有助于修复受污染海洋环境或高盐度废水的有用生物技术细菌。
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来源期刊
Microbiology spectrum
Microbiology spectrum Biochemistry, Genetics and Molecular Biology-Genetics
CiteScore
3.20
自引率
5.40%
发文量
1800
期刊介绍: Microbiology Spectrum publishes commissioned review articles on topics in microbiology representing ten content areas: Archaea; Food Microbiology; Bacterial Genetics, Cell Biology, and Physiology; Clinical Microbiology; Environmental Microbiology and Ecology; Eukaryotic Microbes; Genomics, Computational, and Synthetic Microbiology; Immunology; Pathogenesis; and Virology. Reviews are interrelated, with each review linking to other related content. A large board of Microbiology Spectrum editors aids in the development of topics for potential reviews and in the identification of an editor, or editors, who shepherd each collection.
期刊最新文献
Spleen tyrosine kinase inhibitors disrupt human neutrophil swarming and antifungal functions. Virulence-associated variants in Cryptococcus neoformans sequence type 93 are less likely to be associated with population structure compared to independent rare mutations. Antibiotic resistance genotype, phenotype, and clinical outcomes in patients with Gram-negative infections at Rabin Medical Center in Israel. Identification of a putative novel polycyclic aromatic hydrocarbon-biodegrading gene cluster in a marine Roseobacteraceae bacterium Sagittula sp. MA-2. Spatiotemporal and genomic analysis of carbapenem resistance elements in Enterobacterales from hospital inpatients and natural water ecosystems of an Irish city.
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