Abstract
The genus Alternaria includes several of fungi that are darkly pigmented by DHN-melanin. These are pathogenic to plants but are also associated with human respiratory allergic diseases and with serious infections in immunocompromised individuals. The present work focuses on the alterations of the composition and structure of the hyphal cell wall of Alternaria alternata occuring under the catabolism of L-tyrosine and L-phenylalanine when cultured in minimal salt medium (MM). Under these growing conditions, we observed the released of a brown pigment into the culture medium. FTIR analysis demonstrates that the produced pigment is chemically identical to the pigment released when the fungus is grown in MM with homogentisate acid (HGA), the intermediate of pyomelanin, confirming that this pigment is pyomelanin. In contrast to other fungi that also synthesize pyomelanin under tyrosine metabolism, A. alternata inhibits DHN-melanin cell wall accumulation when pyomelanin is produced, and this is associated with reduced chitin cell wall content. When A. alternata is grown in MM containing L-phenylalanine, a L-tyrosine percursor, pyomelanin is synthesized but only at trace concentrations and A. alternata mycelia display an albino-like phenotype since DHN-melanin accumulation is inhibited. CmrA, the transcription regulator for the genes coding for the DHN-melanin pathway, is involved in the down-regulation of DHN-melanin synthesis when pyomelanin is being synthetized, since the CMRA gene and genes of the enzymes involved in DHN-melanin synthesis pathway showed a decreased expression. Other amino acids do not trigger pyomelanin synthesis and DHN-melanin accumulation in the cell wall is not affected. Transmission and scanning electron microscopy show that the cell wall structure and surface decorations are altered in L-tyrosine- and L-phenylalanine-grown fungi, depending on the pigment produced. In summary, growth in presence of L-tyrosine and L-phenylalanine leads to pigmentation and cell wall changes, which could be relevant to infection conditions where these amino acids are expected to be available.
Highlights
Alternaria alternata is the most common species of the genus Alternaria and it is the major environmental allergen associated with asthma and allergic rhinitis (Knutsen et al, 2012; Denning et al, 2014; Fukutomi and Taniguchi, 2015), described as an opportunistic agent of infection in immunocompromised patients
In MM supplemented with 5.5 mM of L-tyrosine (MMT), A. alternata produced a brown pigment bound to the hypha that was released into the medium (Figure 2A)
The anchorage of melanin to the cell wall has been associated to the cell wall chitin content and structure, another component that is responsible for the cell wall strength (Lenardon et al, 2010)
Summary
Alternaria alternata is the most common species of the genus Alternaria and it is the major environmental allergen associated with asthma and allergic rhinitis (Knutsen et al, 2012; Denning et al, 2014; Fukutomi and Taniguchi, 2015), described as an opportunistic agent of infection in immunocompromised patients. Melanins are a group of related pigments that share common physical and chemical characteristics (Eisenman and Casadevall, 2012). They are formed by the oxidative polymerization of phenolic or indolic compounds. Other melanins called alkaptomelanin are derived from L-tyrosine (Yabuuchi and Ohyama, 1972). This pigment is referred as alkaptomelanin when is produced by humans with alkaptonuria, a rare disease due to mutations in the homogentisate dioxygenase gene but is usually called pyomelanin when synthesized by microbes. Pyomelanin is a water-soluble brown pigment first identified in Pseudomonas aeruginosa (Yabuuchi and Ohyama, 1972)
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