A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger

• Published in: PloS one Vol. 11; no. 11; p. e0165755
• Main Authors: Paege, Norman, Jung, Sascha, Schäpe, Paul, Müller-Hagen, Dirk, Ouedraogo, Jean-Paul, Heiderich, Caroline, Jedamzick, Johanna, Nitsche, Benjamin M, van den Hondel, Cees A, Ram, Arthur F, Meyer, Vera
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 11.11.2016; Public Library of Science (PLoS)
• Subjects: Amino Acid Sequence; Analysis; Antifungal agents; Aspergillus; Aspergillus niger; Aspergillus niger - genetics; Aspergillus niger - metabolism; Autophagy; Autophagy - genetics; Bioinformatics; Biological evolution; Biology; Biology and Life Sciences; Biotechnology; Cell death; Cell survival; Compartments; Core protein; Cultivation; Cysteine; Fluorescence; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Fungicides; Gene expression; Gene Expression Profiling; Gene Expression Regulation, Fungal; Genes; Genomes; Heat-Shock Proteins - genetics; Heat-Shock Proteins - metabolism; Hyphae - genetics; Hyphae - metabolism; Machinery and equipment; Medicine and Health Sciences; Meta-analysis; Metabolism; Network analysis; Nutrients; Osmotic Pressure; Oxidative Stress; Phagocytosis; Phylogenetics; Physiological aspects; Polypeptides; Promoter Regions, Genetic; Proteins; Regulators; Repressor Proteins - genetics; Repressor Proteins - metabolism; Research and Analysis Methods; Secondary Metabolism - genetics; Sequence Alignment; Sequence Homology, Amino Acid; Starvation; Transcription; Transcriptome; Netherlands; Germany
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0165755

Understanding the genetic, molecular and evolutionary basis of cysteine-stabilized antifungal proteins (AFPs) from fungi is important for understanding whether their function is mainly defensive or associated with fungal growth and development. In the current study, a transcriptome meta-analysis of the Aspergillus niger γ-core protein AnAFP was performed to explore co-expressed genes and pathways, based on independent expression profiling microarrays covering 155 distinct cultivation conditions. This analysis uncovered that anafp displays a highly coordinated temporal and spatial transcriptional profile which is concomitant with key nutritional and developmental processes. Its expression profile coincides with early starvation response and parallels with genes involved in nutrient mobilization and autophagy. Using fluorescence- and luciferase reporter strains we demonstrated that the anafp promoter is active in highly vacuolated compartments and foraging hyphal cells during carbon starvation with CreA and FlbA, but not BrlA, as most likely regulators of anafp. A co-expression network analysis supported by luciferase-based reporter assays uncovered that anafp expression is embedded in several cellular processes including allorecognition, osmotic and oxidative stress survival, development, secondary metabolism and autophagy, and predicted StuA and VelC as additional regulators. The transcriptomic resources available for A. niger provide unparalleled resources to investigate the function of proteins. Our work illustrates how transcriptomic meta-analyses can lead to hypotheses regarding protein function and predict a role for AnAFP during slow growth, allorecognition, asexual development and nutrient recycling of A. niger and propose that it interacts with the autophagic machinery to enable these processes.