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Genomic Analysis and Assessment of Melanin Synthesis in Amorphotheca Resinae KUC3009

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Genomic Analysis and Assessment of Melanin Synthesis in Amorphotheca Resinae KUC3009 Journal of Fungi Article Genomic Analysis and Assessment of Melanin Synthesis in Amorphotheca resinae KUC3009 Jeong-Joo Oh 1 , Young Jun Kim 2 , Jee Young Kim 1, Sun Lul Kwon 1, Changsu Lee 3, Myeong-Eun Lee 4, Jung Woo Kim 5 and Gyu-Hyeok Kim 1,* 1 Division of Environmental Science & Ecological Engineering, College of Life Sciences & Biotechnology, Korea University, 145, Anam-ro, Seongbuk-gu, Seoul 02841, Korea; [email protected] (J.-J.O.); [email protected] (J.Y.K.); [email protected] (S.L.K.) 2 Life Science and Biotechnology Department, Underwood Division, Underwood International College, Yonsei University, Seoul 03722, Korea; [email protected] 3 Microbiology and Functionality Research Group, World Institute of Kimchi, Gwangju 61755, Korea; [email protected] 4 Department of Biotechnology, College of Life Sciences & Biotechnology, Korea University, 145, Anam-ro, Seongbuk-gu, Seoul 02841, Korea; [email protected] 5 Department of Biomedical Engineering, Sungkyunkwan University, Suwon, 2066 Seobu-ro, Jangan-gu, Suwon 16419, Korea; [email protected] * Correspondence: [email protected]; Tel.: +82-2-3290-3014 Abstract: This study reports the draft genome of Amorphotheca resinae KUC30009, a fungal isolate with promising industrial-scale melanin production potential. The mechanisms for melanin or melanin- related pigment formation of this strain were examined through bioinformatic and biochemical strate- gies. The 30.11 Mb genome of A. resinae contains 9638 predicted genes. Genomic-based discovery analyses identified 14 biosynthetic gene clusters (BGCs) associated with secondary metabolite pro- duction. Moreover, genes encoding a specific type 1 polyketide synthase and 4-hydroxynaphthalene Citation: Oh, J.-J.; Kim, Y.J.; Kim, J.Y.; reductase were identified and predicted to produce intermediate metabolites of dihydroxy naphtha- Kwon, S.L.; Lee, C.; Lee, M.-E.; Kim, J.W.; Kim, G.-H. Genomic Analysis lene (DHN)-melanin biosynthesis pathway, but not to DHN-melanin. These findings were further and Assessment of Melanin Synthesis supported by the detection of increased flaviolin concentrations in mycelia and almost unchanged in Amorphotheca resinae KUC3009. J. morphologies of the culture grown with tricyclazole. Apart from this, the formation of melanin Fungi 2021, 7, 289. https://doi.org/ in the culture filtrate appeared to depend on the laccase-like activity of multi-copper oxidases. Si- 10.3390/jof7040289 multaneously, concentrations of nitrogen-containing sources decreased when the melanin formed in the media. Interestingly, melanin formation in the culture fluid was proportional to laccase-like Academic Editor: Laurent Dufossé activity. Based on these findings, we proposed novel strategies for the enhancement of melanin production in culture filtrates. Therefore, our study established a theoretical and methodological basis Received: 22 March 2021 for synthesizing pigments from fungal isolates using genomic- and biochemical-based approaches. Accepted: 9 April 2021 Published: 12 April 2021 Keywords: Amorphotheca resinae; fungal melanin; bioinformatics; melanin pigments Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Contrary to their synthetic counterparts, the demand for natural pigments has been steadily increasing in recent years in response to global market shifts and consumer prefer- ences [1,2]. Filamentous fungi have been gaining recognition as a potential microbial source of natural pigments; however, the industrial applications of these microorganisms are not Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. as widespread as those involving algae or bacteria [3]. Fungi can potentially produce a This article is an open access article wide range of pigments, such as carotenoids, Monascus pigments, and melanins [4–8], and distributed under the terms and can utilize a wide range of substrates, thus making the medium composition design and conditions of the Creative Commons fermentation process more flexible [9]. Attribution (CC BY) license (https:// However, fungal pigments are secondary metabolites, and most of their synthesis creativecommons.org/licenses/by/ pathways and optimal production conditions remain largely unknown [10], which limits 4.0/). their optimization and widespread adoption in industrial applications. Fortunately, with J. Fungi 2021, 7, 289. https://doi.org/10.3390/jof7040289 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 289 2 of 13 the accumulation of high-throughput sequencing data, bioinformatics tools can be used to identify putative genes or gene clusters involved in metabolite production. Afterward, comprehensive prediction of the provisional biosynthetic pathways of pigments would be possible based on the identified putative genes or gene clusters [11]. Therefore, genomic studies could provide fundamental insights into the pathways associated with secondary metabolite synthesis in fungi, thus paving the way for their adoption in industrial-scale pro- cesses. We previously reported the promising capacity of the fungus Amorphotheca resinae KUC3009 to produce melanin at an industrial scale due to its antioxidant activity and high metal ion adsorption capability [8,12]. However, general information on the mechanisms of melanin or melanin-related pigment biosynthesis in A. resinae is not yet available. There- fore, understanding the mechanisms involved in melanin biosynthesis using bioinformatic tools would provide critical insights to optimize scalable pigment production using fungi. Our study sequenced and assembled the whole genome of A. resinae KUC3009. After gene annotation, the putative genes and gene clusters involved in pigment formation were comprehensively investigated. Afterward, the involvement of putative genes or gene clusters was further corroborated with biochemical and molecular approaches. Based on these results, we proposed potential strategies for the optimization of scalable melanin production. Therefore, our study establishes a robust foundation for the production of secondary metabolites using A. resinae, as well as fundamental guidelines for future studies to improve upon. 2. Materials and Methods 2.1. Fungal Culture and DNA/RNA Extraction from Mycelia A. resinae KUC3009 obtained from the Korea University Culture (KUC) collection was sub-cultured on sterilized cellophane membrane disks placed on potato dextrose agar for seven days at 25 ◦C. The mycelia on the cellophane membrane were then harvested, and their genomic DNA was extracted using a DNeasy plant mini kit (Qiagen, Valencia, CA, USA) according to the manufacturer’s instructions [13]. The quantity and quality of the extracted DNA were analyzed via the PicoGreen® method and gel electrophoresis. Total RNA was also extracted from the same cultures using the RNeasy plant mini kit (Qiagen, CA, USA) according to the manufacturer’s instructions. The quantity and quality of the extracted RNA were assessed using an Agilent 2100 bioanalyzer (Agilent Technologies, Santa Clara, CA, USA) coupled with a DNA 1000 chip. 2.2. Library Construction and Whole-Genome Sequencing Library construction and genome sequencing were carried out by Macrogen Co. Ltd. (Seoul, Korea). A DNA library with fragment sizes of approximately 20 kb was prepared with the SMRTbell template prep kit 1.0 (Pacific Biosciences, Menlo Park, CA, USA) and se- quenced using the PacBio Sequel platform. Additionally, short reads were also constructed and sequenced with an Illumina HiSeq 4000 sequencer (San Diego, CA, USA). De novo assembly of PacBio sequence reads was performed using the hierarchical genome assembly process (HGAP) v4.0. After assembly, HiSeq reads were implemented to ensure a more accurate genome sequence using Pilon v1.21 [14]. An RNA-Seq library was also prepared and sequenced with an Illumina HiSeq 4000 system for high-quality genome annotation. 2.3. Genome Analysis, Annotation, and Phylogenetic Analyses The completeness of the draft genome assembly was evaluated with BUSCO v3.0.2 using 1315 core genes of the Ascomycota dataset [15]. Genomic similarity comparisons between A. resinae and other strains were performed using orthoANI [16]. After the draft genome was analyzed, the gene locations were predicted using Maker (v2.31.8) [17]. tRNA and rRNA genes were predicted using tRNAscan (v1.4) and barrnap (v0.7, https: //github.com/tseemann/barrnap, accessed on 1 November 2018), respectively [18]. The functions of the predicted genes were annotated using Protein BLAST+ (v2.6.0), after which the annotated genes were classified according to KOG analysis [19]. Gene clusters related J. Fungi 2021, 7, 289 3 of 13 to secondary metabolism were analyzed using antiSMASH Fungi v6.0 and secondary metabolite regions were identified using a “relaxed” strictness [20]. Lastly, Signal P5.0 was used to predict the presence of the signal peptide in translated products from the putative genes [21]. The internal transcribed spacer (ITS) region was selected for phylogenetic analysis of the selected fungus. The ITS region was amplified using the ITS1F (50-CTT GGT CAT TTA GAG GAA GTA A-30) and LR3 (50-CCG TGT TTC AAG ACG GG-30) primers. Polymerase chain reaction (PCR) was performed on a Bio-Rad MyCycler (Hercules, CA, USA) with the following protocol: initial denaturation at 95 ◦C for 5 min; 34 cycles at 95 ◦C (30 s), 55 ◦C (30 s), and 72 ◦C (30 s); final 5-min extension at 72 ◦C. DNA sequencing was carried out by Macrogen (Seoul, Korea) using the Sanger
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