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Open Access Research article

Elucidating how the saprophytic fungus Aspergillus nidulans uses the plant polyester suberin as carbon source

Isabel Martins1, Diego O Hartmann1, Paula C Alves1, Celso Martins12, Helga Garcia1, Céline C Leclercq3, Rui Ferreira1, Ji He4, Jenny Renaut3, Jörg D Becker5 and Cristina Silva Pereira12*

Author Affiliations

1 Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da República, 2780-157 Oeiras, Portugal

2 Instituto de Biologia Experimental e Tecnológica (iBET), Av. da República, 2781-901 Oeiras, Portugal

3 Proteomics Platform, Centre de Recherche Public - Gabriel Lippmann, Belvaux, Luxembourg

4 Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, DHHS, 8717 Grovemont Circle, 20877 Gaithersburg, MD, USA (previously, the Scientific Computing department, Samuel Roberts Noble Foundation, USA

5 Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal

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BMC Genomics 2014, 15:613  doi:10.1186/1471-2164-15-613

Published: 21 July 2014

Abstract

Background

Lipid polymers in plant cell walls, such as cutin and suberin, build recalcitrant hydrophobic protective barriers. Their degradation is of foremost importance for both plant pathogenic and saprophytic fungi. Regardless of numerous reports on fungal degradation of emulsified fatty acids or cutin, and on fungi–plant interactions, the pathways involved in the degradation and utilisation of suberin remain largely overlooked. As a structural component of the plant cell wall, suberin isolation, in general, uses harsh depolymerisation methods that destroy its macromolecular structure. We recently overcame this limitation isolating suberin macromolecules in a near-native state.

Results

Suberin macromolecules were used here to analyse the pathways involved in suberin degradation and utilisation by Aspergillus nidulans. Whole-genome profiling data revealed the complex degrading enzymatic machinery used by this saprophytic fungus. Initial suberin modification involved ester hydrolysis and ω-hydroxy fatty acid oxidation that released long chain fatty acids. These fatty acids were processed through peroxisomal β-oxidation, leading to up-regulation of genes encoding the major enzymes of these pathways (e.g. faaB and aoxA). The obtained transcriptome data was further complemented by secretome, microscopic and spectroscopic analyses.

Conclusions

Data support that during fungal growth on suberin, cutinase 1 and some lipases (e.g. AN8046) acted as the major suberin degrading enzymes (regulated by FarA and possibly by some unknown regulatory elements). Suberin also induced the onset of sexual development and the boost of secondary metabolism.

Keywords:
Aspergillus nidulans; β-oxidation; Cutinase; Long chain fatty acids; Suberin; Whole-genome profiling