Dataset Information

Horizontal transfer of ?-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes.

ABSTRACT: Horizontal gene transfer (HGT) is a movement of genetic information occurring outside of normal mating activities. It is especially common between prokaryotic endosymbionts and their protozoan, insect, and nematode hosts. Although beta carbonic anhydrase (?-CA) plays a crucial role in metabolic functions of many living organisms, the origin of ?-CA genes in eukaryotic species remains unclear.This study was conducted using phylogenetics, prediction of subcellular localization, and identification of ?-CA, transposase, integrase, and resolvase genes on the MGEs of bacteria. We also structurally analyzed ?-CAs from protozoans, insects, and nematodes and their putative prokaryotic common ancestors, by homology modelling.Our investigations of a number of target genomes revealed that genes coding for transposase, integrase, resolvase, and conjugation complex proteins have been integrated with ?-CA gene sequences on mobile genetic elements (MGEs) which have facilitated the mobility of ?-CA genes from bacteria to protozoan, insect, and nematode species. The prokaryotic origin of protozoan, insect, and nematode ?-CA enzymes is supported by phylogenetic analyses, prediction of subcellular localization, and homology modelling.MGEs form a complete set of enzymatic tools, which are relevant to HGT of ?-CA gene sequences from prokaryotes to protozoans, insects, and nematodes.

SUBMITTER: Zolfaghari Emameh R

PROVIDER: S-EPMC4793742 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Horizontal transfer of β-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes.

Zolfaghari Emameh Reza R Barker Harlan R HR Tolvanen Martti E E ME Parkkila Seppo S Hytönen Vesa P VP

Parasites & vectors 20160316

<h4>Background</h4>Horizontal gene transfer (HGT) is a movement of genetic information occurring outside of normal mating activities. It is especially common between prokaryotic endosymbionts and their protozoan, insect, and nematode hosts. Although beta carbonic anhydrase (β-CA) plays a crucial role in metabolic functions of many living organisms, the origin of β-CA genes in eukaryotic species remains unclear.<h4>Methods</h4>This study was conducted using phylogenetics, prediction of subcellula ...[more]

PMID: 26983858

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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.

Project description: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.

Dataset Information

Horizontal transfer of ?-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes.

Publications

Horizontal transfer of β-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes.

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