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Closely related fungi employ diverse enzymatic strategies to degrade plant biomass.

Benoit I, Culleton H, Zhou M, DiFalco M, Aguilar-Osorio G, Battaglia E, Bouzid O, Brouwer CP, El-Bushari HB, Coutinho PM, Gruben BS, Hildén KS, Houbraken J, Barboza LA, Levasseur A, Majoor E, Mäkelä MR, Narang HM, Trejo-Aguilar B, van den Brink J, vanKuyk PA, Wiebenga A, McKie V, McCleary B, Tsang A, Henrissat B, de Vries RP - Biotechnol Biofuels (2015)

Bottom Line: All tested Aspergilli have a similar genomic potential to degrade plant biomass, with the exception of A. clavatus that has a strongly reduced pectinolytic ability.In addition, significant differences were observed between the enzyme sets produced on these feedstocks, largely correlating with their polysaccharide composition.These data demonstrate that Aspergillus species and possibly also other related fungi employ significantly different approaches to degrade plant biomass.

View Article: PubMed Central - PubMed

Affiliation: Fungal Physiology, CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands ; Microbiology and Kluyver Centre for Genomics of Industrial Fermentation, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.

ABSTRACT

Background: Plant biomass is the major substrate for the production of biofuels and biochemicals, as well as food, textiles and other products. It is also the major carbon source for many fungi and enzymes of these fungi are essential for the depolymerization of plant polysaccharides in industrial processes. This is a highly complex process that involves a large number of extracellular enzymes as well as non-hydrolytic proteins, whose production in fungi is controlled by a set of transcriptional regulators. Aspergillus species form one of the best studied fungal genera in this field, and several species are used for the production of commercial enzyme cocktails.

Results: It is often assumed that related fungi use similar enzymatic approaches to degrade plant polysaccharides. In this study we have compared the genomic content and the enzymes produced by eight Aspergilli for the degradation of plant biomass. All tested Aspergilli have a similar genomic potential to degrade plant biomass, with the exception of A. clavatus that has a strongly reduced pectinolytic ability. Despite this similar genomic potential their approaches to degrade plant biomass differ markedly in the overall activities as well as the specific enzymes they employ. While many of the genes have orthologs in (nearly) all tested species, only very few of the corresponding enzymes are produced by all species during growth on wheat bran or sugar beet pulp. In addition, significant differences were observed between the enzyme sets produced on these feedstocks, largely correlating with their polysaccharide composition.

Conclusions: These data demonstrate that Aspergillus species and possibly also other related fungi employ significantly different approaches to degrade plant biomass. This makes sense from an ecological perspective where mixed populations of fungi together degrade plant biomass. The results of this study indicate that combining the approaches from different species could result in improved enzyme mixtures for industrial applications, in particular saccharification of plant biomass for biofuel production. Such an approach may result in a much better improvement of saccharification efficiency than adding specific enzymes to the mixture of a single fungus, which is currently the most common approach used in biotechnology.

No MeSH data available.


Related in: MedlinePlus

Taxonomic tree of the species used in this study and the numbers of glycoside hydrolases, polysaccharide lyases and carbohydrate esterases detected in their genomes. PPD plant polysaccharide degradation related. The number of unique genes per species is indicated behind their name in the taxonomic tree.
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Fig1: Taxonomic tree of the species used in this study and the numbers of glycoside hydrolases, polysaccharide lyases and carbohydrate esterases detected in their genomes. PPD plant polysaccharide degradation related. The number of unique genes per species is indicated behind their name in the taxonomic tree.

Mentions: Based on the Carbohydrate-Active enZymes (CAZy) [17] annotation pipeline, total numbers of glycoside hydrolases (GH), polysaccharide lyases (PL) and carbohydrate esterases (CE) vary among the species (Fig. 1; Table 2). The percentage of GH genes related to plant polysaccharide degradation (PPD) is 58–66% for all genomes, except that A. clavatus has 20–30% less GH genes than the others (Fig. 1), largely due to a reduction in pectinases (GH28, GH54, GH78, GH88) (Table 2). A. clavatus also contains the lowest percentage of PPD-related PL genes (71% as compared to >86%), which are also all related to pectin degradation. The variations in CAZy content are relatively small compared to previous studies with a more diverse set of fungal species [3–8]. This can be explained by their close phylogenetic relationships and their similar habitats, which would push genome evolution in a similar direction.Fig. 1


Closely related fungi employ diverse enzymatic strategies to degrade plant biomass.

Benoit I, Culleton H, Zhou M, DiFalco M, Aguilar-Osorio G, Battaglia E, Bouzid O, Brouwer CP, El-Bushari HB, Coutinho PM, Gruben BS, Hildén KS, Houbraken J, Barboza LA, Levasseur A, Majoor E, Mäkelä MR, Narang HM, Trejo-Aguilar B, van den Brink J, vanKuyk PA, Wiebenga A, McKie V, McCleary B, Tsang A, Henrissat B, de Vries RP - Biotechnol Biofuels (2015)

Taxonomic tree of the species used in this study and the numbers of glycoside hydrolases, polysaccharide lyases and carbohydrate esterases detected in their genomes. PPD plant polysaccharide degradation related. The number of unique genes per species is indicated behind their name in the taxonomic tree.
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4522099&req=5

Fig1: Taxonomic tree of the species used in this study and the numbers of glycoside hydrolases, polysaccharide lyases and carbohydrate esterases detected in their genomes. PPD plant polysaccharide degradation related. The number of unique genes per species is indicated behind their name in the taxonomic tree.
Mentions: Based on the Carbohydrate-Active enZymes (CAZy) [17] annotation pipeline, total numbers of glycoside hydrolases (GH), polysaccharide lyases (PL) and carbohydrate esterases (CE) vary among the species (Fig. 1; Table 2). The percentage of GH genes related to plant polysaccharide degradation (PPD) is 58–66% for all genomes, except that A. clavatus has 20–30% less GH genes than the others (Fig. 1), largely due to a reduction in pectinases (GH28, GH54, GH78, GH88) (Table 2). A. clavatus also contains the lowest percentage of PPD-related PL genes (71% as compared to >86%), which are also all related to pectin degradation. The variations in CAZy content are relatively small compared to previous studies with a more diverse set of fungal species [3–8]. This can be explained by their close phylogenetic relationships and their similar habitats, which would push genome evolution in a similar direction.Fig. 1

Bottom Line: All tested Aspergilli have a similar genomic potential to degrade plant biomass, with the exception of A. clavatus that has a strongly reduced pectinolytic ability.In addition, significant differences were observed between the enzyme sets produced on these feedstocks, largely correlating with their polysaccharide composition.These data demonstrate that Aspergillus species and possibly also other related fungi employ significantly different approaches to degrade plant biomass.

View Article: PubMed Central - PubMed

Affiliation: Fungal Physiology, CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands ; Microbiology and Kluyver Centre for Genomics of Industrial Fermentation, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.

ABSTRACT

Background: Plant biomass is the major substrate for the production of biofuels and biochemicals, as well as food, textiles and other products. It is also the major carbon source for many fungi and enzymes of these fungi are essential for the depolymerization of plant polysaccharides in industrial processes. This is a highly complex process that involves a large number of extracellular enzymes as well as non-hydrolytic proteins, whose production in fungi is controlled by a set of transcriptional regulators. Aspergillus species form one of the best studied fungal genera in this field, and several species are used for the production of commercial enzyme cocktails.

Results: It is often assumed that related fungi use similar enzymatic approaches to degrade plant polysaccharides. In this study we have compared the genomic content and the enzymes produced by eight Aspergilli for the degradation of plant biomass. All tested Aspergilli have a similar genomic potential to degrade plant biomass, with the exception of A. clavatus that has a strongly reduced pectinolytic ability. Despite this similar genomic potential their approaches to degrade plant biomass differ markedly in the overall activities as well as the specific enzymes they employ. While many of the genes have orthologs in (nearly) all tested species, only very few of the corresponding enzymes are produced by all species during growth on wheat bran or sugar beet pulp. In addition, significant differences were observed between the enzyme sets produced on these feedstocks, largely correlating with their polysaccharide composition.

Conclusions: These data demonstrate that Aspergillus species and possibly also other related fungi employ significantly different approaches to degrade plant biomass. This makes sense from an ecological perspective where mixed populations of fungi together degrade plant biomass. The results of this study indicate that combining the approaches from different species could result in improved enzyme mixtures for industrial applications, in particular saccharification of plant biomass for biofuel production. Such an approach may result in a much better improvement of saccharification efficiency than adding specific enzymes to the mixture of a single fungus, which is currently the most common approach used in biotechnology.

No MeSH data available.


Related in: MedlinePlus