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      Phylogenomic analyses reveal the diversity of laccase-coding genes in Fonsecaea genomes

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          Abstract

          The genus Fonsecaea comprises black yeast-like fungi of clinical relevance, including etiologic agents of chromoblastomycosis and cerebral phaeohyphomycosis. Presence of melanin and assimilation of monoaromatic hydrocarbons and alkylbenzenes have been proposed as virulence factors. Multicopper oxidase (MCO) is a family of enzymes including laccases, ferroxidases and ascorbate oxidases which are able to catalyze the oxidation of various aromatic organic compounds with the reduction of molecular oxygen to water. Additionally, laccases are required for the production of fungal melanins, a cell-wall black pigment recognized as a key polymer for pathogenicity and extremotolerance in black yeast-like fungi. Although the activity of laccase enzymes has previously been reported in many wood-rotting fungi, the diversity of laccase genes in Fonsecaea has not yet been assessed. In this study, we identified and characterized laccase-coding genes and determined their genomic location in five clinical and environmental Fonsecaea species. The identification of laccases sensu stricto will provide insights into carbon acquisition strategies as well as melanin production in Fonsecaea.

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          Most cited references35

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          Laccases: a never-ending story.

          Laccases (benzenediol:oxygen oxidoreductases, EC 1.10.3.2) are blue multicopper oxidases that catalyze the oxidation of an array of aromatic substrates concomitantly with the reduction of molecular oxygen to water. In fungi, laccases carry out a variety of physiological roles during their life cycle. These enzymes are being increasingly evaluated for a variety of biotechnological applications due to their broad substrate range. In this review, the most recent studies on laccase structural features and catalytic mechanisms along with analyses of their expression are reported and examined with the aim of contributing to the discussion on their structure-function relationships. Attention has also been paid to the properties of enzymes endowed with unique characteristics and to fungal laccase multigene families and their organization.
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            The contribution of melanin to microbial pathogenesis.

            Melanins are enigmatic pigments that are produced by a wide variety of microorganisms including several species of pathogenic bacteria, fungi and helminths. The study of melanin is difficult because these pigments defy complete biochemical and structural analysis. Nevertheless, the availability of new reagents in the form of monoclonal antibodies and melanin-binding peptides, combined with the application of various physical techniques, has provided insights into the process of melanization. Melanization is important in microbial pathogenesis because it has been associated with virulence in many microorganisms. Melanin appears to contribute to virulence by reducing the susceptibility of melanized microbes to host defence mechanisms. However, the interaction of melanized microbes and the host is complex and includes immune responses to melanin-related antigens. Production of melanin has also been linked to protection against environmental insults. Interference with melanization is a potential strategy for antimicrobial drug and pesticide development. The process of melanization poses fascinating problems in cell biology and provides a type of pathogenic strategy that is common to highly diverse pathogens.
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              Comparative genomics of biotechnologically important yeasts.

              Ascomycete yeasts are metabolically diverse, with great potential for biotechnology. Here, we report the comparative genome analysis of 29 taxonomically and biotechnologically important yeasts, including 16 newly sequenced. We identify a genetic code change, CUG-Ala, in Pachysolen tannophilus in the clade sister to the known CUG-Ser clade. Our well-resolved yeast phylogeny shows that some traits, such as methylotrophy, are restricted to single clades, whereas others, such as l-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode many pathways of interest. Genomics can predict some biochemical traits precisely, but the genomic basis of others, such as xylose utilization, remains unresolved. Our data also provide insight into early evolution of ascomycetes. We document the loss of H3K9me2/3 heterochromatin, the origin of ascomycete mating-type switching, and panascomycete synteny at the MAT locus. These data and analyses will facilitate the engineering of efficient biosynthetic and degradative pathways and gateways for genomic manipulation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                10 February 2017
                2017
                : 12
                : 2
                : e0171291
                Affiliations
                [1 ]CBS-KNAW Fungal Biodiversity Centre, Utrecht, Netherlands
                [2 ]Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands
                [3 ]Department of Basic Pathology, Federal University of Paraná State, Curitiba, PR, Brazil
                [4 ]Department of Dermatology, Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, China
                University of Minnesota, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: LFM PF VAV JBS SdH.

                • Data curation: LFM PF VAW JBS SdH.

                • Formal analysis: LFM PF VAW.

                • Funding acquisition: LFM PF VAW JBS SdH.

                • Investigation: LFM PF VAW JBS SdH.

                • Methodology: LFM PF JBS SdH.

                • Project administration: LFM PF JBS SdH.

                • Resources: LFM PF VAV JBS SdH.

                • Software: LFM PF VAW.

                • Supervision: VAV JBS SdH.

                • Validation: VAV JBS SdH.

                • Visualization: LFM PF.

                • Writing – original draft: LFM PF.

                • Writing – review & editing: LFM PF JBS SdH.

                Author information
                http://orcid.org/0000-0002-2529-0855
                Article
                PONE-D-16-46197
                10.1371/journal.pone.0171291
                5302831
                28187150
                7d35ce29-4e19-4711-a22a-c90f582bdde3
                © 2017 Moreno et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 November 2016
                : 19 January 2017
                Page count
                Figures: 5, Tables: 4, Pages: 17
                Funding
                Funded by: CAPES-Brazil
                Award ID: 1331-13-2
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 81401650
                Award Recipient :
                Funded by: Young Teacher Foundation of Sun Yat-sen University
                Award ID: 13ykpy32
                Award Recipient :
                LFM was funded by the Science without Borders fellowship (Process-number: 1331-13-2), CAPES-Brazil [capes.gov.br]. PF was partly funded by the National Science Foundation of China No. 81401650 and the Young Teacher Foundation of Sun Yat-sen University No. 13ykpy32. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Enzymology
                Enzymes
                Laccases
                Biology and Life Sciences
                Biochemistry
                Proteins
                Enzymes
                Laccases
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Fungal Pathogens
                Fonsecaea
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Fungal Pathogens
                Fonsecaea
                Biology and Life Sciences
                Mycology
                Fungal Pathogens
                Fonsecaea
                Biology and Life Sciences
                Organisms
                Fungi
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Fungal Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Fungal Pathogens
                Biology and Life Sciences
                Mycology
                Fungal Pathogens
                Biology and Life Sciences
                Genetics
                Fungal Genetics
                Fungal Genomics
                Biology and Life Sciences
                Mycology
                Fungal Genetics
                Fungal Genomics
                Biology and Life Sciences
                Genetics
                Genomics
                Fungal Genomics
                Biology and Life Sciences
                Genetics
                Fungal Genetics
                Biology and Life Sciences
                Mycology
                Fungal Genetics
                Biology and Life Sciences
                Organisms
                Fungi
                Molds (Fungi)
                Aspergillus
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Motif Analysis
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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