New light on bacterial carbonic anhydrases phylogeny based on the analysis of signal peptide sequences

Supuran, Claudiu T.; Capasso, Clemente

doi:10.1080/14756366.2016.1201479

Cited by 77 publications

(62 citation statements)

References 66 publications

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“…Our previous phylogenetic analysis suggested that ␤-CA genes have crossed species boundaries on multiple occasions (8). The present identification of ␤-CA genes within bacterial GIs also strongly suggests that prokaryotic ␤-CA genes have been horizontally transferred between and within different species (47). Specifically, we see what appears to be a very clear case of HGT of a ␤-CA from prokaryotic GIs to the protists T. vaginalis FIG 3 Sequence conservation analysis.…”

Section: Discussionsupporting

confidence: 58%

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

Emameh

Barker

Hytönen

et al. 2018

Appl Environ Microbiol

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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. β-Carbonic anhydrase (β-CA) enzymes play a critical role in the biochemical pathways of many prokaryotes and eukaryotes. We previously suggested the horizontal transfer of β-CA genes from plasmids of some prokaryotic endosymbionts to their protozoan hosts. In this study, we set out to identify β-CA genes that might have been transferred between prokaryotic and protist species through HGT in GIs. Therefore, we investigated prokaryotic chromosomes containing β-CA-encoding GIs and utilized multiple bioinformatics tools to reveal the distinct movements of β-CA genes among a wide variety of organisms. Our results identify the presence of β-CA genes in GIs of several medically and industrially relevant bacterial species, and phylogenetic analyses reveal multiple cases of likely horizontal transfer of β-CA genes from GIs of ancestral prokaryotes to protists. 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, β-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 β-CA gene sequences in the GIs and suggests their horizontal transfer to protists during evolution.

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Section: Discussionsupporting

confidence: 58%

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

Emameh

Barker

Hytönen

et al. 2018

Appl Environ Microbiol

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“…In our investigation on the bacterial CAs, it has also been noted that bor c-CA primary structures belonging to some pathogenic Gram-negative bacteria are typified by a secretory signal peptide of 18 or more amino acid residues 7,8 . These findings coupled with the evidence that also the bacterial i-CAs have a putative secretory signal peptide suggest that the b-, cand/or i-CAs characterised by the presence of a signal peptide might have in the Gram-negative bacteria a periplasmic localisation supporting or complementing the same role of the a-CAs 7,8 . Figure 3 shows the alignment of the i-CA amino acid sequences identified in B. territorii and T. pseudonana.…”

Section: Primary Sequence and Phylogenetic Analysismentioning

confidence: 76%

“…Since the CA hydratase/dehydratase activity contributes to numerous physiological functions involving dissolved inorganic carbon, CAs are crucial biomolecules in many physiological and pathological conditions in all types of organisms 6 . In the last years, and especially, to the rapid emergence of the bacterial antibiotic resistance that is occurring worldwide, the understanding of the function of bacterial CAs has increased significantly 7,8 . CAs are essential for the survival of the microbes and their pathogenicity and virulence 9,10 .…”

Section: Introductionmentioning

confidence: 99%

Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii

Prete

Nocentini

Capasso

2020

Journal of Enzyme Inhibition and Medicinal Chemistry

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The carbonic anhydrases (CAs, EC 4.2.1.1) catalyse a simple but physiologically crucial reversible reaction, the carbon dioxide hydration with the production of bicarbonate and protons. In the last years, and especially, to the rapid emergence of the bacterial antibiotic resistance that is occurring worldwide, the understanding of the function of bacterial CAs has increased significantly. Recently, a new CA-class (i-CA) was discovered in the marine diatom T. pseudonana. It has been reported that bacterial genomes may contain genes with relevant homology to the diatom i-class CA. Still, the catalytic activity of the enzyme encoded by the gene was not investigated. Thus, herein, for the first time, we cloned, expressed, and purified the recombinant bacterial i-CA (acronym BteCAi) identified in the genome of Burkholderia territorii. The recombinant BteCAi resulted in a good catalyst for the hydration of CO 2 to bicarbonate and protons, with a k cat of 3.0 Â 10 5 s À1 and k cat /K M of 3.9 Â 10 7 M À1 s À1 , and is also sensitive to inhibition by the sulphonamide acetazolamide. Furthermore, with the aid of the protonography, it has been demonstrated that BteCAi can be present as a dimer. This result is corroborated by the construction of a molecular model of BteCAi, which showed that the enzyme is formed by two equivalent monomers having a structure similar to a butterfly.

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“…Enzymes belonging to ζ-CAs classes present hydrolytic activity in ester groups, and hence P-nitrophenyl acetate hydrolysis to P-nitrophenol acetate is used as a measure of carbonic anhydrase activity. According to Supuran and Capasso (2016), genes encoding for α-CAs are present in Gram negative bacteria whereas genes encoding β-Cas and γ-Cas are found in Gram negative and Gram positive bacteria, with the exception of Helicobacter pylori, which presents encoding genes for three families (α-, β-, and ζ-CAs classes).…”

Section: Genetic Factors Involved In Enzymatic Activity (Ue and Ca) Imentioning

confidence: 99%

Microbially Induced Calcium Carbonate Precipitation (MICP) and Its Potential in Bioconcrete: Microbiological and Molecular Concepts

et al. 2019

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In this review, we discuss microbiological and molecular concepts of Microbially Induced Calcium Carbonate Precipitation (MICP) and their role in bioconcrete. MICP is a widespread biochemical process in soils, caves, freshwater, marine sediments, and hypersaline habitats. MICP is an outcome of metabolic interactions between diverse microbial communities with organic and/or inorganic compounds present in the environment. Some of the major metabolic processes involved in MICP at different levels are urea hydrolysis, denitrification, dissimilatory sulfate reduction, and photosynthesis. Currently, MICP directed by urea hydrolysis, denitrification, and dissimilatory sulfate reduction has been reported to aid in the development of bioconcrete and has demonstrated an improvement in the mechanical and durability properties of concrete. Bioconcrete is a promising sustainable technology which reduces negative environmental impact caused by CO 2 emissions from the construction sector, as well as in terms of economic benefits by way of promoting a self-healing process of concrete structures. Among the metabolic processes mentioned above, urea hydrolysis is the most applied in concrete repair mechanisms. MICP by urea hydrolysis is induced by a series of reactions driven by urease (Ur) and carbonic anhydrase (CA). Catalytic activity of these two enzymes depends on diverse parameters, which are currently being studied under laboratory conditions to better understand the biochemical mechanisms involved and their regulation in microorganisms. It is clearly evident that microbiological and molecular components are essential to improving the process and performance of bioconcrete.

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New light on bacterial carbonic anhydrases phylogeny based on the analysis of signal peptide sequences

Cited by 77 publications

References 66 publications

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

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

Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii

Microbially Induced Calcium Carbonate Precipitation (MICP) and Its Potential in Bioconcrete: Microbiological and Molecular Concepts

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