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Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis.

Abramyan J, Stajich JE - MBio (2012)

Bottom Line: Such shifts in lifestyle are generally accompanied by various degrees of genomic modifications, yet neither its mode of pathogenicity nor any factors associated with it have ever been identified.The expansion of CBM18 in B. dendrobatidis is exceptional in its size and diversity compared to other pathogenic species of fungi, making this genomic feature unique in an evolutionary context as well as in pathogenicity.Due to the alarming rate of worldwide spread and associated decline in amphibian populations, it is imperative to incorporate novel genomic and genetic techniques into the study of this species.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, California, USA.

ABSTRACT

Unlabelled: Batrachochytrium dendrobatidis is the causative agent of chytridiomycosis, which is considered one of the driving forces behind the worldwide decline in populations of amphibians. As a member of the phylum Chytridiomycota, B. dendrobatidis has diverged significantly to emerge as the only pathogen of adult vertebrates. Such shifts in lifestyle are generally accompanied by various degrees of genomic modifications, yet neither its mode of pathogenicity nor any factors associated with it have ever been identified. Presented here is the identification and characterization of a unique expansion of the carbohydrate-binding module family 18 (CBM18), specific to B. dendrobatidis. CBM (chitin-binding module) expansions have been likened to the evolution of pathogenicity in a variety of fungus species, making this expanded group a prime candidate for the identification of potential pathogenicity factors. Furthermore, the CBM18 expansions are confined to three categories of genes, each having been previously implicated in host-pathogen interactions. These correlations highlight this specific domain expansion as a potential key player in the mode of pathogenicity in this unique fungus. The expansion of CBM18 in B. dendrobatidis is exceptional in its size and diversity compared to other pathogenic species of fungi, making this genomic feature unique in an evolutionary context as well as in pathogenicity.

Importance: Amphibian populations are declining worldwide at an unprecedented rate. Although various factors are thought to contribute to this phenomenon, chytridiomycosis has been identified as one of the leading causes. This deadly fungal disease is cause by Batrachochytrium dendrobatidis, a chytrid fungus species unique in its pathogenicity and, furthermore, its specificity to amphibians. Despite more than two decades of research, the biology of this fungus species and its deadly interaction with amphibians had been notoriously difficult to unravel. Due to the alarming rate of worldwide spread and associated decline in amphibian populations, it is imperative to incorporate novel genomic and genetic techniques into the study of this species. In this study, we present the first reported potential pathogenicity factors in B. dendrobatidis. In silico studies such as this allow us to identify putative targets for more specific molecular analyses, furthering our hope for the control of this pathogen.

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Related in: MedlinePlus

Domain positions on corresponding genes. CBM18 (chitin-binding module 18) domains are represented by black boxes with the phylogenetic domain groups labeled in yellow. Gray boxes represent non-CBM (chitin-binding module) domains identified on some genes. All domain lengths and positions are calculated on an amino acid level, beginning from the first residue of the gene. Widths of boxes and interdomain spaces are representative of relative domain lengths and spaces, respectively. Genes are color coded according to type. An unrooted cladogram generated from a Bayesian tree shows the phylogenetic relationships between genes. TL, tyrosinase-like; DL, deacetylase-like; LL, lectin-like; DE, deacetylase domain; TYR, tyrosinase domain; aa, amino acids.
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fig1: Domain positions on corresponding genes. CBM18 (chitin-binding module 18) domains are represented by black boxes with the phylogenetic domain groups labeled in yellow. Gray boxes represent non-CBM (chitin-binding module) domains identified on some genes. All domain lengths and positions are calculated on an amino acid level, beginning from the first residue of the gene. Widths of boxes and interdomain spaces are representative of relative domain lengths and spaces, respectively. Genes are color coded according to type. An unrooted cladogram generated from a Bayesian tree shows the phylogenetic relationships between genes. TL, tyrosinase-like; DL, deacetylase-like; LL, lectin-like; DE, deacetylase domain; TYR, tyrosinase domain; aa, amino acids.

Mentions: When the CBM18 Pfam domain HMM was used to search against the predicted protein coding genes from the B. dendrobatidis genome, with an E value cutoff of 0.01, we identified 67 domain copies located on 18 genes (Fig. 1). The number of domains per locus ranged from a single domain to 11. The significance of this finding was furthered by our analysis of the closest sequenced genome of another chytridiomycete, Homolaphlyctis polyrhiza. H. polyrhiza has only 10 CBM18 copies. The B. dendrobatidis chitin-binding domain had a homologous (cysteine) pattern of X3CGX7CX4CCSX4CX6CX3C. This motif is also conserved between the B. dendrobatidis CBM18 and the hevein domain of plants (see Fig. S1 in the supplemental material). In addition to the CBMs, some of these genes also contained additional binding domains such as a tyrosinase domain (tyrosinase like [TL]) and a deacetylase domain (deacetylase-like [DL]) as identified using PHOG Universal Proteome Explorer, v.2.0. The third group consisted of genes with no secondary domains (lectin-like [LL]) (Fig. 1). Although other organisms have larger numbers of genes with CBMs, the 11 copies of CBM18 on BDEG_01757 likely represent one of the largest expansion within a gene (http://www.cazy.org/). Corresponding BDEG numbers also reflect the clustering of certain groups of genes with respect to chromosomal position (e.g., BDEG_06104 to BDEG_06106, BDEG_05514, BDEG_05516, BDEG_05519, BDEG_05521, and BDEG_05523), indicative of a tandem duplication pattern.


Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis.

Abramyan J, Stajich JE - MBio (2012)

Domain positions on corresponding genes. CBM18 (chitin-binding module 18) domains are represented by black boxes with the phylogenetic domain groups labeled in yellow. Gray boxes represent non-CBM (chitin-binding module) domains identified on some genes. All domain lengths and positions are calculated on an amino acid level, beginning from the first residue of the gene. Widths of boxes and interdomain spaces are representative of relative domain lengths and spaces, respectively. Genes are color coded according to type. An unrooted cladogram generated from a Bayesian tree shows the phylogenetic relationships between genes. TL, tyrosinase-like; DL, deacetylase-like; LL, lectin-like; DE, deacetylase domain; TYR, tyrosinase domain; aa, amino acids.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3569864&req=5

fig1: Domain positions on corresponding genes. CBM18 (chitin-binding module 18) domains are represented by black boxes with the phylogenetic domain groups labeled in yellow. Gray boxes represent non-CBM (chitin-binding module) domains identified on some genes. All domain lengths and positions are calculated on an amino acid level, beginning from the first residue of the gene. Widths of boxes and interdomain spaces are representative of relative domain lengths and spaces, respectively. Genes are color coded according to type. An unrooted cladogram generated from a Bayesian tree shows the phylogenetic relationships between genes. TL, tyrosinase-like; DL, deacetylase-like; LL, lectin-like; DE, deacetylase domain; TYR, tyrosinase domain; aa, amino acids.
Mentions: When the CBM18 Pfam domain HMM was used to search against the predicted protein coding genes from the B. dendrobatidis genome, with an E value cutoff of 0.01, we identified 67 domain copies located on 18 genes (Fig. 1). The number of domains per locus ranged from a single domain to 11. The significance of this finding was furthered by our analysis of the closest sequenced genome of another chytridiomycete, Homolaphlyctis polyrhiza. H. polyrhiza has only 10 CBM18 copies. The B. dendrobatidis chitin-binding domain had a homologous (cysteine) pattern of X3CGX7CX4CCSX4CX6CX3C. This motif is also conserved between the B. dendrobatidis CBM18 and the hevein domain of plants (see Fig. S1 in the supplemental material). In addition to the CBMs, some of these genes also contained additional binding domains such as a tyrosinase domain (tyrosinase like [TL]) and a deacetylase domain (deacetylase-like [DL]) as identified using PHOG Universal Proteome Explorer, v.2.0. The third group consisted of genes with no secondary domains (lectin-like [LL]) (Fig. 1). Although other organisms have larger numbers of genes with CBMs, the 11 copies of CBM18 on BDEG_01757 likely represent one of the largest expansion within a gene (http://www.cazy.org/). Corresponding BDEG numbers also reflect the clustering of certain groups of genes with respect to chromosomal position (e.g., BDEG_06104 to BDEG_06106, BDEG_05514, BDEG_05516, BDEG_05519, BDEG_05521, and BDEG_05523), indicative of a tandem duplication pattern.

Bottom Line: Such shifts in lifestyle are generally accompanied by various degrees of genomic modifications, yet neither its mode of pathogenicity nor any factors associated with it have ever been identified.The expansion of CBM18 in B. dendrobatidis is exceptional in its size and diversity compared to other pathogenic species of fungi, making this genomic feature unique in an evolutionary context as well as in pathogenicity.Due to the alarming rate of worldwide spread and associated decline in amphibian populations, it is imperative to incorporate novel genomic and genetic techniques into the study of this species.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, California, USA.

ABSTRACT

Unlabelled: Batrachochytrium dendrobatidis is the causative agent of chytridiomycosis, which is considered one of the driving forces behind the worldwide decline in populations of amphibians. As a member of the phylum Chytridiomycota, B. dendrobatidis has diverged significantly to emerge as the only pathogen of adult vertebrates. Such shifts in lifestyle are generally accompanied by various degrees of genomic modifications, yet neither its mode of pathogenicity nor any factors associated with it have ever been identified. Presented here is the identification and characterization of a unique expansion of the carbohydrate-binding module family 18 (CBM18), specific to B. dendrobatidis. CBM (chitin-binding module) expansions have been likened to the evolution of pathogenicity in a variety of fungus species, making this expanded group a prime candidate for the identification of potential pathogenicity factors. Furthermore, the CBM18 expansions are confined to three categories of genes, each having been previously implicated in host-pathogen interactions. These correlations highlight this specific domain expansion as a potential key player in the mode of pathogenicity in this unique fungus. The expansion of CBM18 in B. dendrobatidis is exceptional in its size and diversity compared to other pathogenic species of fungi, making this genomic feature unique in an evolutionary context as well as in pathogenicity.

Importance: Amphibian populations are declining worldwide at an unprecedented rate. Although various factors are thought to contribute to this phenomenon, chytridiomycosis has been identified as one of the leading causes. This deadly fungal disease is cause by Batrachochytrium dendrobatidis, a chytrid fungus species unique in its pathogenicity and, furthermore, its specificity to amphibians. Despite more than two decades of research, the biology of this fungus species and its deadly interaction with amphibians had been notoriously difficult to unravel. Due to the alarming rate of worldwide spread and associated decline in amphibian populations, it is imperative to incorporate novel genomic and genetic techniques into the study of this species. In this study, we present the first reported potential pathogenicity factors in B. dendrobatidis. In silico studies such as this allow us to identify putative targets for more specific molecular analyses, furthering our hope for the control of this pathogen.

Show MeSH
Related in: MedlinePlus