Comparative Profiling and Discovery of Novel Glycosylated Mycosporine-Like Amino Acids in Two Strains of the Cyanobacterium Scytonema cf. crispum

Applied and Environmental Microbiology
2016.0

Abstract

<jats:title>ABSTRACT</jats:title> <jats:p> The mycosporine-like amino acids (MAAs) are a group of small molecules with a diverse ecological distribution among microorganisms. MAAs have a range of physiological functions, including protection against UV radiation, making them important from a biotechnological perspective. In the present study, we identified a putative MAA ( <jats:italic>mys</jats:italic> ) gene cluster in two New Zealand isolates of <jats:named-content content-type="genus-species">Scytonema</jats:named-content> cf. <jats:named-content content-type="genus-species">crispum</jats:named-content> (UCFS10 and UCFS15). Homology to “ <jats:named-content content-type="genus-species">Anabaena</jats:named-content> -type” <jats:italic>mys</jats:italic> clusters suggested that this cluster was likely to be involved in shinorine biosynthesis. Surprisingly, high-performance liquid chromatography analysis of <jats:italic>S</jats:italic> . cf. <jats:named-content content-type="genus-species">crispum</jats:named-content> cell extracts revealed a complex MAA profile, including shinorine, palythine-serine, and their hexose-bound variants. It was hypothesized that a short-chain dehydrogenase (UCFS15_00405) encoded by a gene adjacent to the <jats:italic>S</jats:italic> . cf. <jats:named-content content-type="genus-species">crispum</jats:named-content> <jats:italic>mys</jats:italic> cluster was responsible for the conversion of shinorine to palythine-serine. Heterologous expression of MysABCE and UCFS15_00405 in <jats:named-content content-type="genus-species">Escherichia coli</jats:named-content> resulted in the exclusive production of the parent compound shinorine. Taken together, these results suggest that shinorine biosynthesis in <jats:italic>S</jats:italic> . cf. <jats:named-content content-type="genus-species">crispum</jats:named-content> proceeds via an <jats:named-content content-type="genus-species">Anabaena</jats:named-content> -type mechanism and that the genes responsible for the production of other MAA analogues, including palythine-serine and glycosylated analogues, may be located elsewhere in the genome. <jats:p> <jats:bold>IMPORTANCE</jats:bold> Recently, New Zealand isolates of <jats:italic>S</jats:italic> . cf. <jats:named-content content-type="genus-species">crispum</jats:named-content> were linked to the production of paralytic shellfish toxins for the first time, but no other natural products from this species have been reported. Thus, the species was screened for important natural product biosynthesis. The mycosporine-like amino acids (MAAs) are among the strongest absorbers of UV radiation produced in nature. The identification of novel MAAs is important from a biotechnology perspective, as these molecules are able to be utilized as sunscreens. This study has identified two novel MAAs that have provided several new avenues of future research related to MAA genetics and biosynthesis. Further, we have revealed that the genetic basis of MAA biosynthesis may not be clustered on the genome. The identification of the genes responsible for MAA biosynthesis is vital for future genetic engineering.

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