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. 2022 Dec;13(1):1502-1514.
doi: 10.1080/21505594.2022.2117679.

In silico analysis and a comparative genomics approach to predict pathogenic trehalase genes in the complete genome of Antarctica Shigella sp. PAMC28760

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In silico analysis and a comparative genomics approach to predict pathogenic trehalase genes in the complete genome of Antarctica Shigella sp. PAMC28760

Prasansah Shrestha et al. Virulence. 2022 Dec.

Abstract

Although four Shigella species (S. flexneri, S. sonnei, S. dysenteriae, and S. boydii) have been reported, S. sp. PAMC 28760, an Antarctica isolate, is the only one with a complete genome deposited in NCBI database as an uncharacterized isolate. Because it is the world's driest, windiest, and coldest continent, Antarctica provides an unfavourable environment for microorganisms. Computational analysis of genomic sequences of four Shigella species and our uncategorized Antarctica isolates Shigella sp. PAMC28760 was performed using MP3 (offline version) program to predict trehalase encoding genes as a pathogenic or non-pathogenic form. Additionally, we employed RAST and Prokka (offline version) annotation programs to determine locations of periplasmic (treA) and cytoplasmic (treF) trehalase genes in studied genomes. Our results showed that only 56 out of 134 Shigella strains had two different trehalase genes (treF and treA). It was revealed that the treF gene tends to be prevalent in Shigella species. In addition, both treA and treF genes were present in our strain S. sp. PAMC28760. The main objective of this study was to predict the prevalence of two different trehalase genes (treF and treA) in the complete genome of Shigella sp. PAMC28760 and other complete genomes of Shigella species. Till date, it is the first study to show that two types of trehalase genes are involved in Shigella species, which could offer insight on how the bacteria use accessible carbohydrate like glucose produced from the trehalose degradation pathway, and importance of periplasmic trehalase involvement in bacterial virulence.

Keywords: HMM; MP3; SVM; Shigella sp.; prokka; trehalase.

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Conflict of interest statement

No potential conflict of interest was reported by the author(s).

Figures

Figure 1.
Figure 1.
(a) Circular phylogenetic analysis of the complete genomes of Shigella: Phylogenetic tree showing the relationships of genomes of a total 134 Shigella strains including an Antarctica isolate Shigella sp. PAMC28760 (represented in red text), and their phylogenetic position. This analysis was prepared using MEGA X based on 16S rRNA sequences with neighbour-joining method with 1,000-replicate bootstrap. (b) Heatmap generated with OrthoANI values calculated using the OAT software to determine the close relationship of strain S. sp. PAMC28760 with S. flexneri ATCC29903(T), S. sonnei CECT4887(T), E. coli ATCC11775(T), S. boydii GTC779(T), E. fergusonii ATCC35469(T), S. dysenteriae ATCC13313(T), and E. albertii TW07627(T).
Figure 2.
Figure 2.
Circular genome comparison using CGView ServerBETA (http://cgview.Ca/) tool for the representation of genome and features of the S. sp. PAMC28760. The contents of the featured rings (starting with the outermost ring to the centre) are as follows. Ring 1, combined ORFs in forward and reverse strands; Ring 2, trehalose degradative genes, combined forward and reverse strand, and CDS (including tRNA and rRNA) in forward and reverse strands; Ring 3, GC skew plot, values above average are depicted in green, and below average in purple; Ring 4, GC content plot; and Ring 5, Sequence ruler.
Figure 3.
Figure 3.
Cytoplasmic trehalase (TreF) amino acid sequence alignment with a characterized trehalase (TreF). TreF (GH37) from E. coli K-12 substr. MG1655, trehalase from S. flexneri C32, trehalase from Shigella sp. PAMC28760, and trehalase from S. boydii ATCC49812. The signature motif 1 and signature motif 2 represent two highly conserved sequence segments that belong to the GH37 family. The “#” symbol denotes the catalytic sites of Asp312 and Glu496. the three black boxes represent conserved regions (CR3–CR5).
Figure 4.
Figure 4.
Venn diagram categorizes trehalase genes involved in the complete genomes of four Shigella species along with uncategorized Shigella sp. PAMC28760. Green circle represents the cytoplasmic trehalase (treF), whereas red circle represents the periplasmic trehalase (treA). The number outside the circles represents the absence of both trehalase genes.
Figure 5.
Figure 5.
Circular phylogenetic tree based on trehalase genes (treF/treA) sequence in the complete genomes of Shigella strains with reference to the characterized trehalase of E. coli strain K-12 substrain MG165 using a neighbour-joining tree method with 1,000-replicate bootstrap. The pink highlighted boxes represent the characterized trehalase genes (treF and treA), whereas the red text indicates the strain (Shigella sp. PAMC28760) under study.
Figure 6.
Figure 6.
Trehalose degradative pathways. Six different trehalose degradative pathways are found in organisms (bacteria, fungi, yeast, Arthropoda, and plants). Among them, only two degradation pathways (Trehalose degradation pathway II (cytosolic) and VI (periplasmic)) are found in Shigella species.
Figure 7.
Figure 7.
Schematic diagram of the trehalose metabolism pathway in Gram-negative bacteria is formulated from Kosciow et al., 2014 and Purvis et al., 2005. The green boxes represent the trehalose synthesis genes (otsA, trehalose-6-phosphate phosphatase; otsB, trehalose-6-phosphate synthase; and treC, trehalose-6-phosphate hydrolase), whereas grey boxes represent the trehalose degrading genes (treA, periplasmic trehalase; and treF, cytoplasmic trehalase). At cytoplasm, trehalose is degraded by cytoplasmic trehalase gene (treF). The plasma membrane, stretch-activated proteins (SAP) facilitate the exit of trehalose under hypotonic conditions to the periplasm where it further degraded by periplasmic trehalase gene (treA).

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