Extracellular and Intracellular Polyphenol Oxidases Cause Opposite Effects on Sensitivity of Streptomyces to Phenolics: A Case of Double-Edged Sword

Abstract

Many but not all species of Streptomyces species harbour a bicistronic melC operon, in which melC2 encodes an extracellular tyrosinase (a polyphenol oxidase) and melC1 encodes a helper protein. On the other hand, a melC-homologous operon (melD) is present in all sequenced Streptomyces chromosomes and could be isolated by PCR from six other species tested. Bioinformatic analysis showed that melC and melD have divergently evolved toward different functions. MelD2, unlike tyrosinase (MelC2), is not secreted, and has a narrower substrate spectrum. Deletion of melD caused an increased sensitivity to several phenolics that are substrates of MelD2. Intracellularly, MelD2 presumably oxidizes the phenolics, thus bypassing spontaneous copper-dependent oxidation that generates DNA-damaging reactive oxygen species. Surprisingly, melC+ strains were more sensitive rather than less sensitive to phenolics than melC − strains. This appeared to be due to conversion of the phenolics by MelC2 to more hydrophobic and membrane-permeable quinones. We propose that the conserved melD operon is involved in defense against phenolics produced by plants, and the sporadically present melC operon probably plays an aggressive role in converting the phenolics to the more permeable quinones, thus fending off less tolerant competing microbes (lacking melD) in the phenolic-rich rhizosphere.

Actinobacteria isolated from termite guts as a source of novel oxidative enzymes

“…A recent study by Yang and Chen (2009) suggested that in the presence of plant phenolics, extracellular tyrosinase (MelC, which this study assayed for) may play a protective role by converting the phenols to toxic quinones which, in turn, would kill competing bacteria. The presence of a homologous bicistronic operon in streptomycetes, melD, was proposed to protect the tyrosinaseproducing strain against the potential toxic effect of the quinones (Yang and Chen 2009). The MelD type tyrosinases are not secreted and are in no way involved in melanin or melanoid pigment production.…”

Copper mining in Streptomyces: enzymes, natural products and development

“…As the completed genome sequences for various Streptomyces species become available, a bicistronic operon homologous to melC has been found in all the sequenced chromosomes, and has subsequently been named melD. 82 The melD operon also contains melD1 which is homologous to the melC2 gene encoding for the chaperone protein (Fig. 4).…”

Characterization of an Insoluble and Soluble Form of Melanin Produced by Streptomyces cavourensis SV 21, a Sea Cucumber Associated Bacterium

“…In many bacteria, including Streptomyces spp., melanin serves as a natural marker for taxonomic identification up to the genus level [1][2][3]. Specifically, the production of melanin in Streptomyces was assigned to an adaptive response to elevated environmental stress conditions such as light, temperature, oxidative stress, as well as an elevated concentration of heavy metals [4][5][6]. In addition, melanin produced by Streptomyces spp.…”