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. 2020 Mar 16;9(3):217.
doi: 10.3390/pathogens9030217.

Description of Virulent Factors and Horizontal Gene Transfers of Keratitis-Associated Amoeba Acanthamoeba Triangularis by Genome Analysis

Issam Hasni  1   2 , Julien Andréani  1 , Philippe Colson  1 , Bernard La Scola  1
Affiliations

Description of Virulent Factors and Horizontal Gene Transfers of Keratitis-Associated Amoeba Acanthamoeba Triangularis by Genome Analysis

Issam Hasni et al. Pathogens. .

Abstract

Acanthamoeba triangularis strain SH 621 is a free-living amoeba belonging to Acanthamoeba ribo-genotype T4. This ubiquitous protist is among the free-living amoebas responsible for Acanthamoeba keratitis, a severe infection of human cornea. Genome sequencing and genomic comparison were carried out to explore the biological functions and to better understand the virulence mechanism related to the pathogenicity of Acanthamoeba keratitis. The genome assembly harbored a length of 66.43 Mb encompassing 13,849 scaffolds. The analysis of predicted proteins reported the presence of 37,062 ORFs. A complete annotation revealed 33,168 and 16,605 genes that matched with NCBI non-redundant protein sequence (nr) and Cluster of Orthologous Group of proteins (COG) databases, respectively. The Kyoto Encyclopedia of Genes and Genomes Pathway (KEGG) annotation reported a great number of genes related to carbohydrate, amino acid and lipid metabolic pathways. The pangenome performed with 8 available amoeba genomes belonging to genus Acanthamoeba revealed a core genome containing 843 clusters of orthologous genes with a ratio core genome/pangenome of less than 0.02. We detected 48 genes related to virulent factors of Acanthamoeba keratitis. Best hit analyses in nr database identified 99 homologous genes shared with amoeba-resisting microorganisms. This study allows the deciphering the genome of a free-living amoeba with medical interest and provides genomic data to better understand virulence-related Acanthamoeba keratitis.

Keywords: Acanthamoeba triangularis; free-living amoebae; genes; genome; keratitis; pathogenicity.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Characteristics of similarity search of each Acanthamoeba triangularis protein sequences assigned to a function in NCBI non-redundant protein sequence (nr) database. (A) taxonomical distribution. (B) E-value distribution. (C) Similarity distribution.
Figure 2
Figure 2
Representation of A. triangularis genes related to different clusters of gene categories.
Figure 3
Figure 3
Distribution of A. triangularis protein sequences involved in the metabolic pathway. The protein of A. triangularis was compared to the Kyoto Encyclopedia of Genes and Genomes Pathway (KEGG) database and the repartition of these protein sequences in the metabolic pathway was visualized.
Figure 4
Figure 4
Infection of human cornea by Acanthamoeba species. (a) Acanthamoeba detached from contaminated lens. (b) Acanthamoeba spp. attached and adhered to epithelial cells by receptor (mannose receptors and glycoproteins) and secreted metalloproteases to digest external environment. (c) Acanthamoeba spp. destroyed epithelium and Brownan’s membrane in order to penetrate within stroma environment (secretion of proteases, glycosidases, and hydrolytic enzymes). (d) Destruction of stromae. (e) Radial keratoneuritis (an infiltrate along the corneal nerves).
Figure 5
Figure 5
Representation of horizontal transfer analysis. Phylogenetic tree for A. triangularis protein of putative ARM origin. The tree was constructed using maximum-likelihood method based on hypothetical protein sequences of A. triangularis. The tree was performed with 21 homologous sequences of A. triangularis retrieved by BLASTp on NCBI. In red: hypothetical protein of A. triangularis SH621; in blue: the closest homolog from Candidatus Protochlamydia amoebophila; in orange: other homologs from chlamydia; in green: homologs from other amoebas; in black: homologs from other organisms.
Figure 6
Figure 6
Representation of horizontal transfer analysis. Phylogenetic tree for A. triangularis protein of putative ARM origin. The tree was constructed using maximum-likelihood method based on the signal peptidase I sequences of A. triangularis. The tree was performed with 30 homologous sequences of A. triangularis retrieved by BLASTp on NCBI. In red: signal peptidase I of A. triangularis; in orange: homologs from ARM (Pandoravirus strains); in black: homologs from other organisms.
Figure 7
Figure 7
Flower plot showing the core, dispensable, and strain-specific genes of the 8 Acanthamoeba species. The flower plot displays the core gene number (in the center), the dispensable gene number (in the annulus), and the strain-specific gene number (in the petals) for the 8 Acanthamoeba species. The numbers under the strain name denote the total number of related genes. Different colors indicate different Acanthamoeba T-genotype groups: T4 genotype in blue; T5 strains in yellow; T10 strains in red; T11 strains in green.
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