Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose

Abstract

BackgroundProteins in the Glycoside Hydrolase family 32 (GH32) are carbohydrate-active enzymes known as invertases that hydrolyse the glycosidic bonds of complex saccharides. Fungi rely on these enzymes to gain access to and utilize plant-derived sucrose. In fungi, GH32 invertase genes are found in higher copy numbers in the genomes of pathogens when compared to closely related saprophytes, suggesting an association between invertases and ecological strategy. The aim of this study was to investigate the distribution and evolution of GH32 invertases in the Ceratocystidaceae using a comparative genomics approach. This fungal family provides an interesting model to study the evolution of these genes, because it includes economically important pathogenic species such as Ceratocystis fimbriata, C. manginecans and C. albifundus, as well as saprophytic species such as Huntiella moniliformis, H. omanensis and H. savannae.ResultsThe publicly available Ceratocystidaceae genome sequences, as well as the H. savannae genome sequenced here, allowed for the identification of novel GH32-like sequences. The de novo assembly of the H. savannae draft genome consisted of 28.54 megabases that coded for 7 687 putative genes of which one represented a GH32 family member. The number of GH32 gene family members appeared to be related to the ecological adaptations of these fungi. The pathogenic Ceratocystis species all contained two GH32 family genes (a putative cell wall and a putative vacuolar invertase), while the saprophytic Huntiella species had only one of these genes (a putative cell wall invertase). Further analysis showed that the evolution of the GH32 gene family in the Ceratocystidaceae involved transposable element-based retro-transposition and translocation. As an example, the activity of a Fot5-like element likely facilitated the assembly of the genomic regions harbouring the GH32 family genes in Ceratocystis.ConclusionsThis study provides insight into the evolutionary history of the GH32 gene family in Ceratocystidaceae. Our findings suggest that transposable elements shaped the evolution of the GH32 gene family, which in turn determines the sucrolytic activities and related ecological strategies of the Ceratocystidaceae species that harbour them. The study also provides insights into the role of carbohydrate-active enzymes in plant-fungal interactions and adds to our understanding of the evolution of these enzymes and their role in the life style of these fungi.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0550-7) contains supplementary material, which is available to authorized users.

The fructan syndrome: Evolutionary aspects and common themes among plants and microbes

“…These microbes lack specific levanases. Many different fungi employ various GH32 family hydrolases (Trollope, Wyk, Kotjomela, & Volschenk, ; Van der Nest et al, ); however, there have been no reports on fungal GH68 enzymes. 3D structures of two different fungal inulinases from Aspergillus amawori (PDB ID: 1Y4W) and Aspergillus ficuum ( PDB ID: 3RWK); and invertases / β‐fructofuranosidases from Schwanniomyces occidentalis (PDB ID: 3KF5), Aspergillus kawachii (PDB ID: 5XH9), Saccharomyces cerevisiae (PDB ID: 4EQV), and Xanthophyllomyces dendrorhous (PDB ID: 5ANN) have been obtained so far.…”

Contrasting carbon metabolism in saprotrophic and pathogenic microascalean fungi from Protea trees

“…albifundus growth on sucrose, the most common carbohydrate in plant phloem (Pritchard, 2007). This was further confounded by the recent description of two invertases predicted to facilitate sucrose uptake in C. albifundus (Van der Nest et al, 2015). It is possible that these invertases have affinities for storage carbohydrates other than sucrose, such as those mentioned above.…”

Patterns of coevolution between ambrosia beetle mycangia and the Ceratocystidaceae, with five new fungal genera and seven new species

“…Analysis B gave an older estimate for the crown of the family Ceratocystidaceae ( Table 2 ), but otherwise Analysis B estimates were younger or approximated those in Analysis A, and the chronological order of the node dates were similar in the two analyses. The estimated crown age for the Ceratocystidaceae at 80.3 Ma using Analysis A was somewhat older than the estimate of 61.9 Ma by Van der Nest et al (2015) , who used a similar secondary analysis and calibration points but many fewer taxa.…”