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Involvement of ?-Carbonic Anhydrase Genes in Bacterial Genomic Islands and Their Horizontal Transfer to Protists.

ABSTRACT: Genomic islands (GIs) are a type of mobile genetic element (MGE) that are present in bacterial chromosomes. They consist of a cluster of genes that produce proteins that contribute to a variety of functions, including, but not limited to, the regulation of cell metabolism, antimicrobial resistance, pathogenicity, virulence, and resistance to heavy metals. The genes carried in MGEs can be used as a trait reservoir in times of adversity. Transfer of genes using MGEs, occurring outside reproduction, is called horizontal gene transfer (HGT). Previous data have shown that numerous HGT events have occurred through endosymbiosis between prokaryotes and eukaryotes. ?-Carbonic anhydrase (?-CA) enzymes play a critical role in the biochemical pathways of many prokaryotes and eukaryotes. We previously suggested the horizontal transfer of ?-CA genes from plasmids of some prokaryotic endosymbionts to their protozoan hosts. In this study, we set out to identify ?-CA genes that might have been transferred between prokaryotic and protist species through HGT in GIs. Therefore, we investigated prokaryotic chromosomes containing ?-CA-encoding GIs and utilized multiple bioinformatics tools to reveal the distinct movements of ?-CA genes among a wide variety of organisms. Our results identify the presence of ?-CA genes in GIs of several medically and industrially relevant bacterial species, and phylogenetic analyses reveal multiple cases of likely horizontal transfer of ?-CA genes from GIs of ancestral prokaryotes to protists.IMPORTANCE The evolutionary process is mediated by mobile genetic elements (MGEs), such as genomic islands (GIs). A gene or set of genes in the GIs is exchanged between and within various species through horizontal gene transfer (HGT). Based on the crucial role that GIs can play in bacterial survival and proliferation, they were introduced as environment- and pathogen-associated factors. Carbonic anhydrases (CAs) are involved in many critical biochemical pathways, such as the regulation of pH homeostasis and electrolyte transfer. Among the six evolutionary families of CAs, ?-CA gene sequences are present in many bacterial species, which can be horizontally transferred to protists during evolution. This study shows the involvement of bacterial ?-CA gene sequences in the GIs and suggests their horizontal transfer to protists during evolution.

SUBMITTER: Zolfaghari Emameh R

PROVIDER: S-EPMC6052266 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Involvement of β-Carbonic Anhydrase Genes in Bacterial Genomic Islands and Their Horizontal Transfer to Protists.

Zolfaghari Emameh Reza R Barker Harlan R HR Hytönen Vesa P VP Parkkila Seppo S

Applied and environmental microbiology 20180717 15

Genomic islands (GIs) are a type of mobile genetic element (MGE) that are present in bacterial chromosomes. They consist of a cluster of genes that produce proteins that contribute to a variety of functions, including, but not limited to, the regulation of cell metabolism, antimicrobial resistance, pathogenicity, virulence, and resistance to heavy metals. The genes carried in MGEs can be used as a trait reservoir in times of adversity. Transfer of genes using MGEs, occurring outside reproduction ...[more]

PMID: 29802189

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Project description:BACKGROUND: Despite the high prevalence of parasitic infections, and their impact on global health and economy, the number of drugs available to treat them is extremely limited. As a result, the potential consequences of large-scale resistance to any existing drugs are a major concern. A number of recent investigations have focused on the effects of potential chemical inhibitors on bacterial and fungal carbonic anhydrases. Among the five classes of carbonic anhydrases (alpha, beta, gamma, delta and zeta), beta carbonic anhydrases have been reported in most species of bacteria, yeasts, algae, plants, and particular invertebrates (nematodes and insects). To date, there has been a lack of knowledge on the expression and molecular structure of beta carbonic anhydrases in metazoan (nematodes and arthropods) and protozoan species. METHODS: Here, the identification of novel beta carbonic anhydrases was based on the presence of the highly-conserved amino acid sequence patterns of the active site. A phylogenetic tree was constructed based on codon-aligned DNA sequences. Subcellular localization prediction for each identified invertebrate beta carbonic anhydrase was performed using the TargetP webserver. RESULTS: We verified a total of 75 beta carbonic anhydrase sequences in metazoan and protozoan species by proteome-wide searches and multiple sequence alignment. Of these, 52 were novel, and contained highly conserved amino acid residues, which are inferred to form the active site in beta carbonic anhydrases. Mitochondrial targeting peptide analysis revealed that 31 enzymes are predicted with mitochondrial localization; one was predicted to be a secretory enzyme, and the other 43 were predicted to have other undefined cellular localizations. CONCLUSIONS: These investigations identified 75 beta carbonic anhydrases in metazoan and protozoan species, and among them there were 52 novel sequences that were not previously annotated as beta carbonic anhydrases. Our results will not only change the current information in proteomics and genomics databases, but will also suggest novel targets for drugs against parasites.

Dataset Information

Involvement of ?-Carbonic Anhydrase Genes in Bacterial Genomic Islands and Their Horizontal Transfer to Protists.

Publications

Involvement of β-Carbonic Anhydrase Genes in Bacterial Genomic Islands and Their Horizontal Transfer to Protists.

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