Melanisation of Aspergillus terreus-Is Butyrolactone I Involved in the Regulation of Both DOPA and DHN Types of Pigments in Submerged Culture?

Elina Palonen,Tajalli Keshavarz,Sheetal Raina,Annika Brandt,Juhani Soini,Jussi Meriluoto

doi:10.3390/microorganisms5020022

Elina Palonen, Tajalli Keshavarz + Show 4 more

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https://doi.org/10.3390/microorganisms5020022

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Abstract

Pigments and melanins of fungal spores have been investigated for decades, revealing important roles in the survival of the fungus in hostile environments. The key genes and the encoded enzymes for pigment and melanin biosynthesis have recently been found in Ascomycota, including Aspergillus spp. In Aspergillus terreus, the pigmentation has remained mysterious with only one class of melanin biogenesis being found. In this study, we examined an intriguing, partially annotated gene cluster of A. terreus strain NIH2624, utilizing previously sequenced transcriptome and improved gene expression data of strain MUCL 38669, under the influence of a suggested quorum sensing inducing metabolite, butyrolactone I. The core polyketide synthase (PKS) gene of the cluster was predicted to be significantly longer on the basis of the obtained transcriptional data, and the surrounding cluster was positively regulated by butyrolactone I at the late growth phase of submerged culture, presumably during sporulation. Phylogenetic analysis of the extended PKS revealed remarkable similarity with a group of known pigments of Fusarium spp., indicating a similar function for this PKS. We present a hypothesis of this PKS cluster to biosynthesise a 1,8-dihydroxynaphthalene (DHN)-type of pigment during sporulation with the influence of butyrolactone I under submerged culture.

Highlights

The filamentous fungi of Aspergillus species are known to cause several diseases and to contain pathogenic features with objects ranging from plants to humans
The biosynthesis pathways of fungal pigment and melanin polymers have been divided into two classes, DHN (1,8-dihydroxynaphthalene) or DOPA (3,4-dihydroxyphenylalanine) pathways
We describe a potential, non-reducing polyketide synthase (NR-PKS) with a non-canonical domain structure within Aspergilli, and the surrounding gene cluster, which were revealed through an in-depth analysis of the recently sequenced transcriptome of A. terreus strain MUCL 38669 [22]

Summary

Introduction

The filamentous fungi of Aspergillus species are known to cause several diseases and to contain pathogenic features with objects ranging from plants to humans. The biosynthesis pathways of fungal pigment and melanin polymers have been divided into two classes, DHN (1,8-dihydroxynaphthalene) or DOPA (3,4-dihydroxyphenylalanine) pathways The classification of these types is, diverged into two methods, either based on the identification of the pathway intermediates, or on the observed effects of applying specific intermediate enzyme inhibitors. The DHN classification is either based on the identification of naphthopyrone precursors or on the effect of inhibitors—tricyclazole or phthalide—targeted to hydroxynaphthalene reductase with classical short-chain dehydrogenase/reductase (SDR) and Rossmann fold domains The biogenesis of this type of melanin usually begins with polyketide synthesis, followed by tailoring steps and polymerisation. Both DHN-type of conidial pigments and DOPA-type of melanins have been discovered in few Aspergillus species, the DHN-type of pigments are presumed to be more common [6,11,12,13,14]

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