Transcriptomic Complexity of Aspergillus terreus Velvet Gene Family under the Influence of Butyrolactone I

Abstract

Filamentous fungi of the Ascomycota phylum are known to contain a family of conserved conidiation regulating proteins with distinctive velvet domains. In Aspergilli, this velvet family includes four proteins, VeA, VelB, VelC and VosA, and is involved in conidiation and secondary metabolism along with a global regulator LaeA. In A. terreus, the overexpression of LaeA has been observed to increase the biogenesis of the pharmaceutically-important secondary metabolite, lovastatin, while the role of the velvet family has not been studied. The secondary metabolism and conidiation of A. terreus have also been observed to be increased by butyrolactone I in a quorum-sensing manner. An enlightenment of the interplay of these regulators will give potential advancement to the industrial use of this fungus, as well as in resolving the pathogenic features. In this study, the Aspergillus terreus MUCL 38669 transcriptome was strand-specifically sequenced to enable an in-depth gene expression analysis to further investigate the transcriptional role of butyrolactone I in these processes. The sequenced transcriptome revealed intriguing properties of the velvet family transcripts, including the regulator laeA, and uncovered the velC gene in A. terreus. The reliability refining microarray gene expression analysis disclosed a positive regulatory role for butyrolactone I in laeA expression, as well as an influence on the expression of the canonical conidiation-regulating genes under submerged culture. All of this supports the suggested regulative role of butyrolactone I in A. terreus secondary metabolism, as well as conidiation.

Melanisation of Aspergillus terreus—Is Butyrolactone I Involved in the Regulation of Both DOPA and DHN Types of Pigments in Submerged Culture?

“…), indicating the increased secondary metabolism to occur prior to enhancing the gene expression of the pgm cluster. The biogenesis of the secondary metabolite lovastatin has been observed to be increased by butyrolactone I during the middle growth phase in the same growth conditions as used in this study [19,20], in agreement with the upregulated laeA gene expression profile [22]. Considering these observed occurrence patterns in chronological order, the activity of the pgm cluster appears to be enhanced after the increase in secondary metabolism in these submerged culture conditions under the influence of increased butyrolactone I biogenesis.…”

“…The microarray gene expression data was obtained and analysed as described in our related study [22]. The analysis contained one unusual step regarding the 60-mer oligonucleotide microarray probes that had been designed based on the available genomic sequence of strain NIH2624 [23].…”

“…Intriguingly, Schimmel et al reported increased sporulation along with secondary metabolism of A. terreus in submerged culture conditions, as a result of supplementing butyrolactone I, which was later implicated as a quorum sensing inducing molecule in A. terreus [19,20,21]. Butyrolactone I was recently suggested to be involved in the gene expression control of the key regulators of conidiation ( brlA , abaA and wetA ) as well as the global regulator laeA [22] in accordance with the previous study of Schimmel et al [19]. However, pigmentation has not been examined in the same growth conditions, to our knowledge.…”

Transcriptome Profiling-Based Analysis of Carbohydrate-Active Enzymes in Aspergillus terreus Involved in Plant Biomass Degradation

“…Typically isolated from soil and decomposing lignocellulosic plant biomass ( Reddy and Singh, 2002 ; He et al, 2004 ; Chantasingh et al, 2006 ), ligninolytic enzyme activities have been investigated in A. terreus , across diverse biorefinery applications, from bioethanol ( Sethi et al, 2017 ), to lovastatin ( Jahromi et al, 2012 ) and organic acid production ( Jiménez-Quero et al, 2017 ). Analysis of the transcriptome of this fungus has, however, focused only on secondary metabolism related to biogenesis of lovastatin ( Palonen et al, 2017 ), with no investigation, prior to this study, of global gene expression during hydrolysis of lignocellulosic plant biomass.…”

“…A number of these species are also efficient in secretion of hydrolytic enzymatic of importance for enzyme-based lignocellulosic biorefineries, with transcriptome analyses in recent years providing important information on gene expression and regulation mechanisms for genes encoding different cellulases, endoxylanases, β-xylosidases and pectinases during degradation of lignocellulosic biomass. Aspergillus terreus is frequently isolated from soil rhizospheres and decaying agricultural cellulosic materials in tropical and subtropical regions ( Wijeratne et al, 2003 ; Palonen et al, 2017 ). In addition to producing different statins that have been widely used in the treatment of heart disease, this species also produces important commercial enzymes employed in bioprocesses that include cellulases, xylanases, lipases and phytases ( Yadav et al, 1998 ; Varga et al, 2005 ; Chantasingh et al, 2006 ; Narra et al, 2012 ; Sharma et al, 2014 ; Pierce et al, 2017 ).…”