Evolution of Family 18 Glycoside Hydrolases: Diversity, Domain Structures and Phylogenetic Relationships

Karlsson, Magnus; Stenlid, Jan

doi:10.1159/000151220

Cited by 86 publications

(87 citation statements)

References 134 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Orthologues to CHIA2 in N. crassa (gh18-3) and T. reesei (chi18-3) are also predicted to be localized in mitochondria and to carry similar mutations (Karlsson & Stenlid, 2009;Seidl et al, 2005). High transcript levels of the chiA2 gene were observed on chitin and during carbon-starvation conditions.…”

Section: Discussionmentioning

confidence: 98%

“…Chitinases (EC 3.2.1.14) are hydrolytic enzymes responsible for cleavage of the 1,4-b-glycosidic linkage in chitin polymers (Gooday, 1990). According to the carbohydrateactive enzymes (CAZy) classification, fungal chitinases belong exclusively to glycoside hydrolases (GH) family 18 (Cantarel et al, 2009;Karlsson & Stenlid, 2009). They are categorized, depending on the cleavage patterns, as endochitinases, which can cleave the chitin chain at random positions, and as exochitinases, which are able to degrade the chitin polymer from the exposed termini releasing chitobiose products (Horn et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea

et al. 2015

Self Cite

View full text Add to dashboard Cite

Clonostachys rosea is a mycoparasitic fungal species that is an efficient biocontrol agent against many plant diseases. During mycoparasitic interactions, one of the most crucial steps is the hydrolysis of the prey's fungal cell wall, which mainly consists of glucans, glycoproteins and chitin. Chitinases are hydrolytic enzymes responsible for chitin degradation and it is suggested that they play an important role in fungal-fungal interactions. Fungal chitinases belong exclusively to the glycoside hydrolase (GH) family 18.These GH18 proteins are categorized into three distinct phylogenetic groups (A, B and C), subdivided into several subgroups. In this study, we identified 14 GH18 genes in the C. rosea genome, which is remarkably low compared with the high numbers found in mycoparasitic Trichoderma species. Phylogenetic analysis revealed that C. rosea contains eight genes in group A, two genes in group B, two genes in group C, one gene encoding a putative ENGase (endo-b-N-acetylglucosaminidase) and the ech37 gene, which is of bacterial origin. Gene expression analysis showed that only two genes had higher transcription levels during fungal-fungal interactions, while eight out of 14 GH18 genes were triggered by chitin. Furthermore, deletion of the C group chiC2 gene decreased the growth inhibitory activity of C. rosea culture filtrates against Botrytis cinerea and Rhizoctonia solani, although the biocontrol ability of C. rosea against B. cinerea was not affected. In addition, a potential role of the CHIC2 chitinase in the sporulation process was revealed. These results provide new information about the role of GH18 proteins in mycoparasitic interactions.

show abstract

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea

et al. 2015

Self Cite

View full text Add to dashboard Cite

show abstract

“…The point mutant MtNFH1(D148A) lacked enzyme activity (Fig. 1B, e), indicating that the canonical DXDXE motif of functional glycosyl hydrolase family 18 enzymes (Karlsson and Stenlid, 2009) is also critical for the hydrolysis of NFs. Furthermore, kinetic data of a MtNFH1 mutant protein, modified in the region of the predicted binding cleft for the fatty acid chain (Table III), provide support for the modeled MtNFH1-NF interaction.…”

Section: Discussionmentioning

confidence: 99%

“…Class V chitinases of plants, also classified as pathogenrelated protein family 11 (PR-11) proteins, form a separate clade within the phylogenetic tree of family 18 glycoside hydrolases (Karlsson and Stenlid, 2009). A phylogenetic tree of class V chitinases and closely related proteins is shown Supplemental Figure S1.…”

mentioning

confidence: 99%

The Nodulation Factor Hydrolase of Medicago truncatula: Characterization of an Enzyme Specifically Cleaving Rhizobial Nodulation Signals

et al. 2013

View full text Add to dashboard Cite

Nodule formation induced by nitrogen-fixing rhizobia depends on bacterial nodulation factors (NFs), modified chitin oligosaccharides with a fatty acid moiety. Certain NFs can be cleaved and inactivated by plant chitinases. However, the most abundant NF of Sinorhizobium meliloti, an O-acetylated and sulfated tetramer, is resistant to hydrolysis by all plant chitinases tested so far. Nevertheless, this NF is rapidly degraded in the host rhizosphere. Here, we identify and characterize MtNFH1 (for Medicago truncatula Nod factor hydrolase 1), a legume enzyme structurally related to defense-related class V chitinases (glycoside hydrolase family 18). MtNFH1 lacks chitinase activity but efficiently hydrolyzes all tested NFs of S. meliloti. The enzyme shows a high cleavage preference, releasing exclusively lipodisaccharides from NFs. Substrate specificity and kinetic properties of MtNFH1 were compared with those of class V chitinases from Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum), which cannot hydrolyze tetrameric NFs of S. meliloti. The Michaelis-Menten constants of MtNFH1 for NFs are in the micromolar concentration range, whereas nonmodified chitin oligosaccharides represent neither substrates nor inhibitors for MtNFH1. The three-dimensional structure of MtNFH1 was modeled on the basis of the known structure of class V chitinases. Docking simulation of NFs to MtNFH1 predicted a distinct binding cleft for the fatty acid moiety, which is absent in the class V chitinases. Point mutation analysis confirmed the modeled NF-MtNFH1 interaction. Silencing of MtNFH1 by RNA interference resulted in reduced NF degradation in the rhizosphere of M. truncatula. In conclusion, we have found a novel legume hydrolase that specifically inactivates NFs.

show abstract

“…It does not accumulate over time and therefore likely has high turnover rates (12,19). Bacterial degradation of chitin usually involves an initial extracellular hydrolysis of the (134)-␤-linkage, catalyzed by excreted glycoside hydrolase (GH) family 18 chitinases, which are phylogenetically subdivided into groups A, B, and C. Lateral gene transfer has been discussed as a reason for their widespread but phylogenetically incoherent distribution among bacterial phyla (17). This implies that populations carrying this function may vary greatly in other ecological traits.…”

mentioning

confidence: 99%

Global Phylogeography of Chitinase Genes in Aquatic Metagenomes

Beier

Jones

Mohit

et al. 2011

Appl Environ Microbiol

View full text Add to dashboard Cite

Phylogeny-based analysis of chitinase and 16S rRNA genes from metagenomic data suggests that salinity is a major driver for the distribution of both chitinolytic and total bacterial communities in aquatic systems. Additionally, more acidic chitinase proteins were observed with increasing salinity. Congruent habitat separation was further observed for both genes according to latitude and proximity to the coastline. However, comparison of chitinase and 16S rRNA genes extracted from different geographic locations showed little congruence in distribution. There was no indication that dispersal limited the global distribution of either gene.In recent years, progress has been made in elucidating factors that underlie the biogeography of bacterial community assemblages (5,13,23,25). However, function cannot easily be inferred from such studies, since specific functional guilds may be present in low abundances and function is difficult to predict from taxonomic affiliations. To target and analyze the diversity of functional groups, biogeographical studies of protein coding genes is an attractive alternative to studies based on taxonomy markers (e.g., see references 10, 13, 16, 28, and 35). By using a phylogeny-based approach to assess the biogeography of functional guilds, information regarding underlying ecological and evolutionary community assembly processes can be accessed (16).Marine chitinolytic communities play key roles in global nitrogen and carbon cycles. Chitinases are responsible for the hydrolysis of chitin, which is one of the most abundant biopolymers on earth. It does not accumulate over time and therefore likely has high turnover rates (12,19). Bacterial degradation of chitin usually involves an initial extracellular hydrolysis of the (134)-␤-linkage, catalyzed by excreted glycoside hydrolase (GH) family 18 chitinases, which are phylogenetically subdivided into groups A, B, and C. Lateral gene transfer has been discussed as a reason for their widespread but phylogenetically incoherent distribution among bacterial phyla (17). This implies that populations carrying this function may vary greatly in other ecological traits. Environmental factors could consequently act directly on an organism's ability to degrade chitin, independently of the taxonomic background of the organism carrying this trait.In this study, we used metagenomic data provided by the Global Ocean Sampling expedition (GOS) (32, 33) to test if specific environmental conditions in aquatic habitats shape the chitinase gene assemblages or if limitations in dispersal are important for the distribution of chitinolytic communities. The phylogeography of chitinase genes was also compared to that of the 16S rRNA gene as a universal taxonomic marker. Divergent distribution patterns between the two genes would indicate if there are environmental factors or distribution mechanisms that are specifically relevant for chitinolytic microorganisms. The respective communities were compared among habitats defined by either salinity, latitude, proximity to th...

show abstract

Evolution of Family 18 Glycoside Hydrolases: Diversity, Domain Structures and Phylogenetic Relationships

Cited by 86 publications

References 134 publications

Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea

Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea

The Nodulation Factor Hydrolase of Medicago truncatula: Characterization of an Enzyme Specifically Cleaving Rhizobial Nodulation Signals

Global Phylogeography of Chitinase Genes in Aquatic Metagenomes

Contact Info

Product

Resources

About