AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Mycology Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Article | Open Access

Synthesis and role of melanin for tolerating in vitro rumen digestion in Duddingtonia flagrans, a nematode-trapping fungus

Deivid França Freitasa ( ), Olney Vieira-Da-Mottab,†, Luciana Da Silva Mathiasb, Roberto Weider De Assis Francoc, Raphael Dos Santos Gomesd,, Ricardo Augusto Mendonça Vieirad, Letícia Oliveira Da Rochaa, Fabio Lopes Olivaresa, Clóvis De Paula Santosa,† ( )
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
Laboratório de Sanidade Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
Laboratório de Ciências Físicas, Centro de Ciências Tecnológicas, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil
Laboratório de Zootecnia, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil

†Both authors contributed equally to the article.

The present affiliation for Raphael Dos Santos Gomes is Instituto Federal de Educação, Ciência e Tecnologia do Acre - Campus Xapuri, Rua Coronel Brandão, n. 1622, Centro, Xapuri, AC. CEP: 69.930-000

Show Author Information

Abstract

We describe the synthesis and a function of melanin in Duddingtonia flagrans, a nematode-trapping fungus. We tested various culture media treated with L-DOPA, glucose and tricyclazole on fungal growth and melanin distribution using infrared spectroscopy (IS), electron paramagnetic resonance (EPR) and transmission electron microscopy (TEM). In vitro rumen digestion was used to test the environmental stress and then to evaluate the capacity of this fungus to trap nematode larvae. The growth and melanization of the fungus after 21 days of incubation at 30℃ were best in Sabouraud dextrose medium. IS indicated the presence of melanin in D. flagrans, with similar bands for commercial melanin used as a control, and assigned the values obtained by EPR (g of 2.0051 ± 0.0001) to the production of melanin by the fungus. TEM indicated that melanin was produced in melanosomes but was not totally inhibited by tricyclazole. Within the limits of experimental error, the predatory activity of fungus treated with tricyclazole was drastically affected after 27 h of in vitro anaerobic stress with rumen inoculum. The deposition of melanin particles on the fungal cell wall contributed to the maintenance of D. flagrans predatory abilities after in vitro anaerobic ruminal stress.

Keywords

L-DOPAmelaninDuddingtonia flagransnematode-trapping fungitricyclazole

References

 

Allam NG, El-Zaher EHF. 2014. Protective role of Aspergillus fumigatus melanin against ultraviolet (UV) irradiation and Bjerkandera adusta melanin as a candidate vaccine against systemic candidiasis. Afr J Biotechnol. 24:6566–6577.
Google Scholar
 

Almeida-Paes R, Frases S, Monteiro PCF, Gutierrez-Galhardo MC, Zancopé-Oliveira RM, Nosanchuk JD. 2009. Growth conditions influence melanization of Brazilian clinical Sporothrix schenckii isolates. Microbes Infect. 5:554–562.
Crossref Google Scholar
 

Alviano DS, Franzen AJ, Travassos LR, Holandino C, Rozental S, Ejzemberg R, Alviano CS, Rodrigues ML. 2004. Melanin from Fonsecaea pedrosoi induces production of human antifungal antibodies and enhances the antimicrobial efficacy of phagocytes. Infect Immun. 2:229–237.
Crossref Google Scholar
 

Andersson KM, Meerupati T, Levander F, Friman E, Ahrén D, Tunlid A. 2013. Characterization of the proteome of the nematode-trapping cells of the fungus Monacrosporium haptotylum. Appl Environ Microbiol. 16:4993–5004.
Crossref Google Scholar
 

Andrade MC, Hiura E, Fonseca LA, Magri C, Ferraz CCS, Sena FP, Giradi FM. 2016. Utilization of the Fungus Duddingtonia flagrans in Control of Nematode Larvae Development in Equine Stool. Curr Microbiol. 3:829–835.
Crossref Google Scholar
 

Assis RCL, Luns FD, Araújo JV, Braga FR, Assis RL, Marcelino JL, Andrade MAS. 2013. Comparison between the action of nematode predatory fungi Duddingtonia flagrans and Monacrosporium thaumasium in the biological control of bovine gastrointestinal nematodiasis in tropical southeastern Brazil. Vet Parasitol. 1:134–140.
Crossref Google Scholar
 

Bell AA, Wheeler MH. 1986. Biosynthesis and functions of fungal melanins. Ann Rev Phytopathol. 1:411–451.
Crossref Google Scholar
 

Braga FR, Araújo JV. 2014. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology. 1:71–82.
Crossref Google Scholar
 

Butler MJ, Gardiner RB, Day AW. 2009. Melanin synthesis by Sclerotinia sclerotiorum. Mycologia. 101:296–304.
Crossref Google Scholar
 

Buzatti A, Santos CP, Fernandes MAM, Yoshitani UY, Sprenger LK, Dos Santos CD, Molento MB. 2015. Duddingtonia flagrans in the control of gastrointestinal nematodes of horses. Exp Parasitol. 159:1–4.
Crossref Google Scholar
 

Casadevall A, Nakouzi A, Crippa PR, Eisner M. 2012. Fungal melanins differ in planar stacking distances. PLos One. 2:1–6.
Crossref Google Scholar
 

Cesareo E, Korkina L, D’errico G, Vitiello G, Aguzzi MS, Passarelli F, Pedersen JZ, Facchiano A. 2012. An endogenous electron spin resonance (ESR) signal discriminates nevi from melanomas in human specimens: a step forward in its diagnostic application. PLos One. 11:e48849.
Crossref Google Scholar
 

Dadachova E, Bryan RA, Howell RC, Schweitzer AD, Aisen P, Nosanchuk JD, Casadevall A. 2008. The radioprotective properties of fungal melanin are a function of its chemical composition, stable radical presence and spatial arrangement. Pigment Cell Melanoma Res. 2:192–199.
Crossref Google Scholar
 

Eisenman HC, Casadevall A. 2012. Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol. 3:931–940.
Crossref Google Scholar
 

Eisenman HC, Nosanchuk JD, Webber JBW, Emerson RJ, Camesano TA, Casadevall A. 2005. Microstructure of cell wall-associated melanin in the human pathogenic fungus Cryptococcus neoformans. Biochemistry. 10:3683–3693.
Crossref Google Scholar
 

Fernandez WC, Koide RT. 2013. The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecol. 6:479–486.
Crossref Google Scholar
 

Franzen AJ, Cunha ML, Batista EJO, Seabra SH, De Souza W, Rozental S. 2006. Effects of tricyclazole (5-methyl-1,2,4-triazol[3,4] benzothiazole), a specific DHN-melanin inhibitor, on the morphology of Fonsecaea pedrosoi conidia and sclerotic cells. ‎Microsc Res Tech. 9:729–737.
Crossref Google Scholar
 

Franzen AJ, Cunha MML, Miranda K, Hentschel J, Plattner H, Silva MB, Salgado CG, Souza W, Rozental S. 2008. Ultrastructural characterization of melanosomes of the human pathogenic fungus Fonsecaea pedrosoi. J Struct Biol. 1:75–84.
Crossref Google Scholar
 

Frases S, Chaskes S, Dadachova E, Casadevall A. 2006. Induction by Klebsiella aerogenes of a melanin-like pigment in Cryptococcus neoformans. Appl Environ Microbiol. 2:1542–1550.
Crossref Google Scholar
 
Goering HK, Van Soest PJ. 1970. Forage fiber analysis. Agricultural handbook No. 379. Washington (D.C.): U.S.D.A.
 

Gordon HM, Whitlock HV. 1939. A new technique for counting nematode eggs in sheep faeces. J. Counc Sci Ind Res. 12:50–52.
Google Scholar
 

Halaouli S, Asther M, Sigoillot JC, Hamdi M, Lomascolo A. 2006. Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. J Appl Microbiol. 2:219–232.
Crossref Google Scholar
 

Hall MB, Mertens D,R. 2008. In vitro fermentation vessel type and method alter fiber digestibility estimates. J Dairy Sci. 91:301–307.
Crossref Google Scholar
 

Howard RJ, Valent B. 1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Ann Rev Microbiol. 1:491–512.
Crossref Google Scholar
 

Jacobson ES, Ikeda R. 2005. Effect of melanization upon porosity of the cryptococcal cell wall. Med Mycol. 4:327–333.
Crossref Google Scholar
 

Kumar M, Chand R, Dubey RS, Shah K. 2015. Effect of Tricyclazole on morphology, virulence and enzymatic alterations in pathogenic fungi Bipolaris sorokiniana for management of spot blotch disease in barley. World J Microbiol Biotechnol. 1:23–35.
Crossref Google Scholar
 

Larsen M. 2006. Biological control of nematode parasites in sheep. J Anim Sci. 84:133–139.
Crossref Google Scholar
 

Lazarovits G, Stoessl A. 1988. Tricyclazole induces melanin shunt products and inhibits altersolanol A accumulation by Alternaria solani. Pest Biochem Physiol. 1:36–45.
Crossref Google Scholar
 

Mandal P, Roy TS, Das TK, Banerjee U, Xess I, Nosanchuk JD. 2007. Differences in the cell wall architecture of melanin lacking and melanin producing Cryptococcus neoformans clinical isolates from India: an electron microscopic study. Braz J Microbiol. 4:662–666.
Crossref Google Scholar
 

Mares D, Romagnoli C, Andreotti E, Manfrini M, Vicentini CB. 2004. Synthesis and antifungal action of new tricyclazole analogues. J Agric Food Chem. 7:2003–2009.
Crossref Google Scholar
 

Meerupati T, Andersson KM, Friman E, Kumar D, Tunlid A, Ahrén D. 2013. Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet. 11:e1003909.
Crossref Google Scholar
 

Meredith P, Sarna T. 2006. The physical and chemical properties of eumelanin. Pigment Cell Res. 6:572–594.
Crossref Google Scholar
 

MHG F-C, Dos Santos FB, Nosanchuk JD, Zancope-Oliveira RM, Almeida-Paes R. 2014. l-Dihydroxyphenylalanine induces melanin production by members of the genus Trichosporon. FEMS Yeast Res. 6:988–991.
Crossref Google Scholar
 

Miot B, Miot HA, Guimaraes SM, Alencar MME. 2009. Fisiopatologia do melasma. An Bras Dermatol. 6:623–635.
Crossref Google Scholar
 

Ojeda-Robertos NF, Torres-Acosta JF, Ayala-Burgos AJ, Sandoval-Castro CA, Valero-Coss RO, Mendoza-De-Gives P. 2009. Digestibility of Duddingtonia flagrans chlamydospores in ruminants: in vitro and in vivo studies. BMC Vet Res. 5:1–7.
Crossref Google Scholar
 

Orlow SJ. 1995. Melanosomes are specialized members of the lysosomal lineage of organelles. J Invest Dermatol. 1:3–7.
Crossref Google Scholar
 

Otręba M, Zdybel M, Pilawa B, Beberok A, Wrześniok D, Rok J, Buszman E. 2015. EPR spectroscopy of chlorpromazine-induced free radical formation in normal human melanocytes. Eur Biophys J. 5:359–365.
Crossref Google Scholar
 

Plonka PM, Grabacka M. 2006. Melanin synthesis in microorganisms-biotechnological and medical aspects. Acta Biochim Pol. 3:429–443.
Crossref Google Scholar
 

Prelovšek PM, Bulog B. 2003. Biogenesis of melanosomes in Kupffer cells of Proteus anguinus (Urodela, Amphibia). Pigment Cell Res. 4:345–350.
Crossref Google Scholar
 

Raposo G, Marks MS. 2007. Melanosomes-dark organelles enlighten endosomal membrane transport. Nat Rev Mol Cell Biol. 10:786–797.
Crossref Google Scholar
 

Raposo G, Tenza D, Murphy DM, Berson JF, Marks MS. 2001. Distinct Protein Sorting and Localization to Premelanosomes, Melanosomes, and Lysosomes in Pigmented Melanocytic Cells. J Cell Biol. 4:809–824.
Crossref Google Scholar
 

Rižner TL, Wheeler MH. 2003. Melanin biosynthesis in the fungus Curvularia lunata (teleomorph: cochliobolus lunatus). Can J Microbiol. 2:110–119.
Crossref Google Scholar
 

Roberts FHS, Sullivan PJ. 1950. Methods for egg counts and larval cultures for Strongyles infecting the gastro-intestinal tract of cattle. Aust J Agric Res. 1:99–102.
Crossref Google Scholar
 

Romero-Martinez R, Wheeler M, Guerrero-Plata A, Rico G, Torres-Guerrero H. 2000. Biosynthesis and Functions of Melanin in Sporothrix schenckii. Infect Immun. 6:3696–3703.
Crossref Google Scholar
 

Rosa LH, Vieira MDLA, Santiago IF, Rosa CA. 2010. Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol. 1:178–189.
Crossref Google Scholar
 

Rosas AL, Nosanchuk JD, Feldmesser M, Cox GM, Mcdade HC, Casadevall A. 2000. Synthesis of polymerized melanin by Cryptococcus neoformans in infected rodents. ‎Infect Immun. 68:2845–2853.
Crossref Google Scholar
 

Rubner A. 1996. Revision of predacious Hyphomycetes in the Dactylella-Monacrosporium complex. Stud Mycol. 39:1–134.
Google Scholar
 

Seiji M, Shimao K, Fitzpatrick TB, Simpson RT, Birbeck MSC. 1963. Chemical composition and terminology of specialized organelles (melanosomes and melanin granules) in mammalian melanocytes. Nature. 197:1082–1084.
Crossref Google Scholar
 

Silva ME, JVD A, Braga FR, Freitas FEDS, Rodrigues DS. 2013. Control of infective larvae of gastrointestinal nematodes in heifers using different isolates of nematophagous fungi. Rev Bras Parasitol Vet. 1:78–83.
Crossref Google Scholar
 

Slominski A, Tobin DJ, Shibahara S, Wortsman J. 2004. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev. 4:1155–1228.
Crossref Google Scholar
 

Solano F. 2014. Melanins: skin pigments and much more types, structural models, biological functions, and formation routes. New J Sci. 2014:1–28.
Crossref Google Scholar
 

Tian S, Garcia-Rivera J, Yan B, Casadevall A, Stark RE. 2003. Unlocking the molecular structure of fungal melanin using 13C biosynthetic labeling and solid-state NMR. Biochemistry. 27:8105–8109.
Crossref Google Scholar
 

Treseder KK, Lennon JT. 2015. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev. 2:243–262.
Crossref Google Scholar
 

Zalar P, Novak M, De Hoog GS, Gunde-Cimerman N. 2011. Dishwashers-a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol. 10:997–1007.
Crossref Google Scholar
 

Zhang CQ, Zhu GN, Ma ZH, Zhou MG. 2006. Isolation, Characterization and Preliminary Genetic Analysis of Laboratory Tricyclazole-resistant Mutants of the Rice Blast Fungus, Magnaporthe grisea. J Phytopathol. 154:392–397.
Crossref Google Scholar
 

Zhdanova NN, Zakharchenko VA, Vember VV, Nakonechnaya LT. 2000. Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol Res. 12:1421–1426.
Crossref Google Scholar
 

Zhong J, Frases S, Wang H, Casadevall A, Stark RE. 2008. Following Fungal Melanin Biosynthesis with Solid-State NMR: biopolymer Molecular Structures and Possible Connections to Cell-Wall Polysaccharides. Biochemistry. 16:4701–4710.
Crossref Google Scholar
Mycology
Volume 10 Issue 4,
December 2019
Pages 229-242
DOI: 10.1080/21501203.2019.1631896
Cite this article:
Freitas DF, Vieira-Da-Motta O, Da Silva Mathias L, et al. Synthesis and role of melanin for tolerating in vitro rumen digestion in Duddingtonia flagrans, a nematode-trapping fungus. Mycology, 2019, 10(4): 229-242. https://doi.org/10.1080/21501203.2019.1631896

203

Views

7

Crossref

6

Web of Science

6

Scopus

Altmetrics
Received: 25 October 2018
Accepted: 07 June 2019
Published: 20 June 2019
© 2019 The Author(s).

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Return