Molecular basis and evolutionary origin of 1-nitronaphthalene catabolism in Sphingobium sp. strain JS3065
Molecular basis and evolutionary origin of 1-nitronaphthalene catabolism in Sphingobium sp. strain JS3065
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Sphingobium sp. 1-硝基萘分解代谢的分子基础和进化起源。
DOI：
10.1128/aem.01728-22
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发表时间：
2023
影响因子：
4.4
通讯作者：
Ning-Yi Zhou
中科院分区：
文献类型：
--
作者：
Tao Li;Jia Xu;Amy L. Brower;Zhi-Jing Xu;Ying Xu;Jim C. Spain;Ning-Yi Zhou
硝化多环芳烃（nitro-PAHs）通过自然来源和人类活动进入环境。到目前为止，微生物能够矿化硝基多环芳烃还没有报道。在这里，Sphingobiumsp.菌株JS 3065是通过选择性富集分离的，因为它能够在1-硝基萘作为唯一的碳、氮和能源上生长。对菌株JS 3065全基因组的分析表明，编码1-硝基萘催化剂（nin）的基因簇位于质粒上。基于遗传和生化证据，theningenes与Ralstoniasp中编码萘降解的类thenag基因具有共同的起源。菌株U2。1-硝基萘降解的初始步骤由三组分双加氧酶NinAaAbAcAd催化，导致形成1，2-二羟基萘，其也是萘降解途径中的早期中间体。将theninAaAbAcAdgenes导入菌株U2，使其能够在1-硝基萘上生长。NinAc的系统发育分析表明，祖先1-硝基萘双加氧酶是硝基芳烃双加氧酶进化的早期步骤。基于生物信息学分析和酶分析，随后的同化1，2-二羟基萘似乎遵循Ralstoniasp的萘降解途径。菌株U2。这是1-硝基萘分解代谢途径的首次报道，也是扩大Rieske型双加氧酶的底物范围使细菌能够在难降解的硝基芳烃上生长的又一个例子。重要的是，硝化多环芳烃（nitro-PAHs）在环境中已被广泛检测到，它们比相应的母体多环芳烃具有更高的毒性。虽然许多多环芳烃的生物降解已被广泛描述在遗传和生物化学水平，很少有人知道微生物降解硝基多环芳烃。本文报道了一株生长在1-硝基萘上的鞘氨醇菌的分离及其分解代谢途径的遗传基础。该途径从祖先的萘分解代谢途径演变而来，通过对初始双加氧酶的特异性进行非常小的修改。这里提供的数据不仅揭示了全球重要的硝化多环芳烃的微生物降解所涉及的生化过程，而且还提供了一个进化的范例，细菌如何进化一种新的分解代谢途径，对天然有机化合物的预先存在的途径进行最小的改变。
Nitrated polycyclic aromatic hydrocarbons (nitro-PAHs) enter the environment from natural sources and anthropogenic activities. To date, microorganisms able to mineralize nitro-PAHs have not been reported. Here,Sphingobiumsp. strain JS3065 was isolated by selective enrichment for its ability to grow on 1-nitronaphthalene as the sole carbon, nitrogen, and energy source. Analysis of the complete genome of strain JS3065 indicated that the gene cluster encoding 1-nitronaphthalene catabolism (nin) is located on a plasmid. Based on the genetic and biochemical evidence, theningenes share an origin with thenag-like genes encoding naphthalene degradation inRalstoniasp. strain U2. The initial step in degradation of 1-nitronaphthalene is catalyzed by a three-component dioxygenase, NinAaAbAcAd, resulting in formation of 1,2-dihydroxynaphthalene which is also an early intermediate in the naphthalene degradation pathway. Introduction of theninAaAbAcAdgenes into strain U2 enabled its growth on 1-nitronaphthalene. Phylogenic analysis of NinAc suggested that an ancestral 1-nitronaphthalene dioxygenase was an early step in the evolution of nitroarene dioxygenases. Based on bioinformatic analysis and enzyme assays, the subsequent assimilation of 1,2-dihydroxynaphthalene seems to follow the well-established pathway for naphthalene degradation byRalstoniasp. strain U2. This is the first report of catabolic pathway for 1-nitronaphthalene and is another example of how expanding the substrate range of Rieske type dioxygenase enables bacteria to grow on recalcitrant nitroaromatic compounds.IMPORTANCENitrated polycyclic aromatic hydrocarbons (nitro-PAHs) have been widely detected in the environment and they are more toxic than their corresponding parent PAHs. Although biodegradation of many PAHs has been extensively described at genetic and biochemical levels, little is known about the microbial degradation of nitro-PAHs. This work reports the isolation of aSphingobiumstrain growing on 1-nitronaphthalene and the genetic basis for the catabolic pathway. The pathway evolved from an ancestral naphthalene catabolic pathway by a remarkably small modification in the specificity of the initial dioxygenase. Data presented here not only shed light on the biochemical processes involved in the microbial degradation of globally important nitrated polycyclic aromatic hydrocarbons, but also provide an evolutionary paradigm for how bacteria evolve a novel catabolic pathway with minimal alteration of preexisting pathways for natural organic compounds.