Isolation of a Novel Microcystin-Degrading Bacterium and the Evolutionary Origin of mlr Gene Cluster

The mlr-dependent biodegradation plays an essential role in the natural attenuation of microcystins (MCs) in eutrophic freshwater ecosystems. However, their evolutionary origin is still unclear due to the lack of mlr gene cluster sequences. In this study, a Sphingopyxis sp. strain X20 with high MC-degrading ability was isolated, and the mlrA gene activity was verified by heterologous expression. The whole sequence of the mlr gene cluster in strain X20 was obtained through PCR and thermal asymmetric interlaced (TAIL)-PCR, and then used for evolutionary origin analyses together with the sequences available in GenBank. Phylogenetic analyses of mlr gene clusters suggested that the four mlr genes had the same origin and evolutionary history. Genomic island analyses showed that there is a genomic island on the genome of sphingomonads that is capable of degrading MCs, on which the mlr gene cluster anchors. The concentrated distribution of the mlr gene cluster in sphingomonads implied that these genes have likely been present in the sphingomonads gene pool for a considerable time. Therefore, the mlr gene cluster may have initially entered into the genome of sphingomonads together with the genomic island by a horizontal gene transfer event, and then become inherited by some sphingomonads. The species other than sphingomonads have likely acquired mlr genes from sphingomonads by recently horizontal gene transfer due to the sporadic distribution of MC-degrading species and the mlr genes in them. Our results shed new light on the evolutionary origin of the mlr cluster and thus facilitate the interpretation of characteristic distribution of the mlr gene in bacteria and the understanding of whole mlr pathway.