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

[1]  J Hacker,et al.  Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. , 1990, Microbial pathogenesis.

[2]  M. G. Kidwell.  Lateral transfer in natural populations of eukaryotes. , 1993, Annual review of genetics.

[3]  J Hacker,et al.  Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution , 1997, Molecular microbiology.

[4]  T. Whittam,et al.  Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Koonin,et al.  Horizontal gene transfer in prokaryotes: quantification and classification. , 2001, Annual review of microbiology.

[6]  J. Hacker,et al.  Ecological fitness, genomic islands and bacterial pathogenicity , 2001, EMBO reports.

[7]  Steven J. M. Jones,et al.  IslandPath: aiding detection of genomic islands in prokaryotes , 2003, Bioinform..

[8]  Qiang Tu,et al.  Detecting pathogenicity islands and anomalous gene clusters by iterative discriminant analysis. , 2003, FEMS microbiology letters.

[9]  Claudiu T. Supuran,et al.  Carbonic anhydrase inhibitors. Inhibition of mitochondrial isozyme V with aromatic and heterocyclic sulfonamides. , 2004, Journal of medicinal chemistry.

[10]  Dirk Springael,et al.  Horizontal gene transfer and microbial adaptation to xenobiotics: new types of mobile genetic elements and lessons from ecological studies. , 2004, Trends in microbiology.

[11]  Carsten Damm,et al.  Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models , 2006, BMC Bioinformatics.

[12]  J. Heitman,et al.  Carbonic Anhydrase and CO2 Sensing during Cryptococcus neoformans Growth, Differentiation, and Virulence , 2005, Current Biology.

[13]  Christopher M Thomas,et al.  Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria , 2005, Nature Reviews Microbiology.

[14]  C. Supuran,et al.  Carbonic anhydrase inhibitors. Inhibition of the transmembrane isozyme XII with sulfonamides-a new target for the design of antitumor and antiglaucoma drugs? , 2005, Bioorganic & medicinal chemistry letters.

[15]  C. Supuran,et al.  Carbonic anhydrase inhibitors: X-ray and molecular modeling study for the interaction of a fluorescent antitumor sulfonamide with isozyme II and IX. , 2006, Journal of the American Chemical Society.

[16]  C. Supuran,et al.  Carbonic anhydrase inhibitors: the beta-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. , 2007, Bioorganic & medicinal chemistry letters.

[17]  Stephen Lory,et al.  MobilomeFINDER: web-based tools for in silico and experimental discovery of bacterial genomic islands , 2007, Nucleic Acids Res..

[18]  Andrea Scozzafava,et al.  Carbonic anhydrase inhibitors. DNA cloning, characterization, and inhibition studies of the human secretory isoform VI, a new target for sulfonamide and sulfamate inhibitors. , 2007, Journal of medicinal chemistry.

[19]  Sarang Aravamuthan,et al.  Identification of compositionally distinct regions in genomes using the centroid method , 2007, Bioinform..

[20]  V. M. Luque-Almagro,et al.  Characterization of the Pseudomonas pseudoalcaligenes CECT5344 Cyanase, an Enzyme That Is Not Essential for Cyanide Assimilation , 2008, Applied and Environmental Microbiology.

[21]  Fiona S. L. Brinkman,et al.  Evaluation of genomic island predictors using a comparative genomics approach , 2008, BMC Bioinformatics.

[22]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[23]  C. Supuran,et al.  Carbonic anhydrase inhibitors. Inhibition of the beta-class enzymes from the fungal pathogens Candida albicans and Cryptococcus neoformans with aliphatic and aromatic carboxylates. , 2009, Bioorganic & medicinal chemistry.

[24]  Fiona S. L. Brinkman,et al.  The Association of Virulence Factors with Genomic Islands , 2009, PloS one.

[25]  D. Crook,et al.  Genomic islands: tools of bacterial horizontal gene transfer and evolution , 2008, FEMS microbiology reviews.

[26]  D. Gautheret,et al.  Transcription attenuation in bacteria: theme and variations. , 2009, Briefings in functional genomics & proteomics.

[27]  E. Flemetakis,et al.  Molecular and biochemical analysis of the α class carbonic anhydrases in Caenorhabditis elegans , 2010, Molecular Biology Reports.

[28]  E. Flemetakis,et al.  Molecular and biochemical analysis of the β class carbonic anhydrases in Caenorhabditis elegans , 2010, Molecular biology reports.

[29]  K. Dobrinski,et al.  Expression and Function of Four Carbonic Anhydrase Homologs in the Deep-Sea Chemolithoautotroph Thiomicrospira crunogena , 2010, Applied and Environmental Microbiology.

[30]  C. Supuran,et al.  Characterization of the first beta-class carbonic anhydrase from an arthropod (Drosophila melanogaster) and phylogenetic analysis of beta-class carbonic anhydrases in invertebrates , 2010, BMC Biochemistry.

[31]  Fiona S. L. Brinkman,et al.  Detecting genomic islands using bioinformatics approaches , 2010, Nature Reviews Microbiology.

[32]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[33]  S. Pöggeler,et al.  Carbonic anhydrases in fungi. , 2010, Microbiology.

[34]  R. Aminov.  Horizontal Gene Exchange in Environmental Microbiota , 2011, Front. Microbio..

[35]  T. Tatusova,et al.  Entrez Gene: gene-centered information at NCBI , 2010, Nucleic Acids Res..

[36]  Comparative molecular analysis of chemolithoautotrophic bacterial diversity and community structure from coastal saline soils, Gujarat, India , 2012, BMC Microbiology.

[37]  N. Dickenson,et al.  Three functional β-carbonic anhydrases in Pseudomonas aeruginosa PAO1: role in survival in ambient air. , 2013, Microbiology.

[38]  C. Supuran,et al.  Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from Leishmania donovani chagasi, the protozoan parasite responsible for leishmaniasis. , 2013, Journal of medicinal chemistry.

[39]  Bioinformatic analysis of beta carbonic anhydrase sequences from protozoans and metazoans , 2014, Parasites & Vectors.

[40]  Minh Anh Nguyen,et al.  Ultrafast Approximation for Phylogenetic Bootstrap , 2013, Molecular biology and evolution.

[41]  J. P. Cárdenas,et al.  Architecture and Gene Repertoire of the Flexible Genome of the Extreme Acidophile Acidithiobacillus caldus , 2013, PloS one.

[42]  C. Supuran,et al.  Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum--the η-carbonic anhydrases. , 2014, Bioorganic & medicinal chemistry letters.

[43]  Giseli Capaci Rodrigues,et al.  Design, synthesis, and evaluation of hydroxamic acid derivatives as promising agents for the management of Chagas disease. , 2014, Journal of medicinal chemistry.

[44]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[45]  Jinling Huang,et al.  Horizontal gene transfer: building the web of life , 2015, Nature Reviews Genetics.

[46]  M. Rämet,et al.  β carbonic anhydrase is required for female fertility in Drosophila melanogaster , 2015, Frontiers in Zoology.

[47]  C. Supuran,et al.  Ascaris lumbricoides β carbonic anhydrase: a potential target enzyme for treatment of ascariasis , 2015, Parasites & Vectors.

[48]  H. Heipieper,et al.  Adaptation in Toxic Environments: Arsenic Genomic Islands in the Bacterial Genus Thiomonas , 2015, PloS one.

[49]  C. Supuran,et al.  An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? , 2015, Journal of enzyme inhibition and medicinal chemistry.

[50]  C. Supuran,et al.  The β-carbonic anhydrase from the malaria mosquito Anopheles gambiae is highly inhibited by sulfonamides. , 2015, Bioorganic & medicinal chemistry.

[51]  Matthew R. Laird,et al.  IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis , 2015, Nucleic Acids Res..

[52]  P. Mather,et al.  Analysis, characterisation and expression of gill-expressed carbonic anhydrase genes in the freshwater crayfish Cherax quadricarinatus. , 2015, Gene.

[53]  C. Supuran,et al.  New light on bacterial carbonic anhydrases phylogeny based on the analysis of signal peptide sequences , 2016, Journal of enzyme inhibition and medicinal chemistry.

[54]  Harlan R. Barker,et al.  Horizontal transfer of β-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes , 2016, Parasites & Vectors.

[55]  C. Nagasato,et al.  Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum , 2016, Proceedings of the National Academy of Sciences.

[56]  P. Bork,et al.  ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data , 2016, Molecular biology and evolution.

[57]  D. Heckel,et al.  Horizontal Gene Transfer Contributes to the Evolution of Arthropod Herbivory , 2016, Genome biology and evolution.

[58]  Itay Mayrose,et al.  ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules , 2016, Nucleic Acids Res..

[59]  Thomas K. F. Wong,et al.  ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates , 2017, Nature Methods.

[60]  C. Supuran,et al.  Carbonic anhydrases from Trypanosoma and Leishmania as anti-protozoan drug targets. , 2017, Bioorganic & medicinal chemistry.

[61]  G. Muyzer,et al.  Comparative Genome Analysis of Three Thiocyanate Oxidizing Thioalkalivibrio Species Isolated from Soda Lakes , 2017, Front. Microbiol..

[62]  I. Coppens,et al.  A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of Toxoplasma gondii Is Important for Rhoptry Biogenesis and Virulence , 2017, mSphere.

[63]  C. Supuran,et al.  Comparison of the anion inhibition profiles of the β- and γ-carbonic anhydrases from the pathogenic bacterium Burkholderia pseudomallei. , 2017, Bioorganic & medicinal chemistry.

[64]  S. Djordjevic,et al.  Genomic islands 1 and 2 carry multiple antibiotic resistance genes in Pseudomonas aeruginosa ST235, ST253, ST111 and ST175 and are globally dispersed , 2017, The Journal of antimicrobial chemotherapy.

[65]  O. Reva,et al.  EuGI: a novel resource for studying genomic islands to facilitate horizontal gene transfer detection in eukaryotes , 2018, BMC Genomics.

[66]  M. Rämet,et al.  beta carbonic anhydrase is required for female fertility in Drosophila melanogaster Syrjänen , 2022 .