Abstract
Currently, studies worldwide have comprehensively recognized the importance of Sphingomonadaceae bacteria and the mlrCABD gene cluster in microcystin (MC) degradation. However, knowledge about their degradation of nodularin (NOD) is still unclear. In this study, the degradation mechanism of NOD by Sphingopyxis sp. m6, an efficient MC degrader isolated from Lake Taihu, was investigated in several aspects, including degradation ability, degradation products, and potential application. The strain degraded NOD of 0.50 mg/L with a zero-order rate constant of 0.1656 mg/L/d and a half-life of 36 h. The average degradation rate of NOD was significantly influenced by the temperature, pH, and initial toxin concentrations. Moreover, four different biodegradation products, linear NOD, tetrapeptide H-Glu-Mdhb-MeAsp-Arg-OH, tripeptide H-Mdhb-MeAsp-Arg-OH, and dipeptide H-MeAsp-Arg-OH, were identified, of which the latter two are the first reported. Furthermore, the four mlr genes were upregulated during NOD degradation. The microcystinase MlrA encoded by the mlrA gene hydrolyzes the Arg-Adda bond to generate linear NOD as the first step of NOD biodegradation. Notably, recombinant MlrA showed higher degradation activity and stronger environmental adaptability than the wild strain, suggesting future applications in NOD pollution remediation. This research proposes a relatively complete NOD microbial degradation pathway, which lays a foundation for exploring the mechanisms of NOD degradation by MC-degrading bacteria.
Highlights
Cyanotoxins such as nodularin (NOD) and microcystin (MC) released by cyanobacterial cells pose a severe threat to the environment and human health, as evidenced by the destruction of aquatic food webs [1,2], mortality of marine mammals and birds [3], massive fish kills [4], and human diseases and even death [5]
We recently found that Sphingopyxis sp. m6, an indigenous strain isolated from Taihu
Monitored by high performance liquid chromatography (HPLC) decreased over time and was almost zero at 72 h, which meant that the NOD concentration was reduced below the detection threshold for HPLC (Figure 1a–c)
Summary
Cyanotoxins such as nodularin (NOD) and microcystin (MC) released by cyanobacterial cells pose a severe threat to the environment and human health, as evidenced by the destruction of aquatic food webs [1,2], mortality of marine mammals and birds [3], massive fish kills [4], and human diseases and even death [5]. The homologous mlr gene cluster was detected in other isolated Sphingomonadaceae bacteria, such as Sphingopyxis sp. The mlr gene cluster encodes three hydrolysis enzymes and one oligopeptide transporter protein. The first enzyme encoded by the mlrA gene is responsible for opening the highly stable cyclic structure of MC by cleaving the Arg-Adda bond. The resulting linear product is degraded to a tetrapeptide by the second enzyme encoded by the mlrB gene. The enzyme MlrC encoded by the mlrC gene hydrolyzes the tetrapeptide to Adda as the final nontoxic product and exerts cleavage activity on the linear product to degrade it directly to Adda. The transporter protein encoded by the mlrD gene is supposed to transport MC and its degradation products into bacterial cells [23,24]
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