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

Appl Environ Microbiol. 2018 Jul 17;84(15):e00771-18. doi: 10.1128/AEM.00771-18. Print 2018 Aug 1.

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.

Keywords: evolution; genomic island; mobile genetic element; β-carbonic anhydrase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacteria / chemistry
  • Bacteria / classification
  • Bacteria / enzymology*
  • Bacteria / genetics*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Carbonic Anhydrases / chemistry
  • Carbonic Anhydrases / genetics*
  • Carbonic Anhydrases / metabolism
  • Chromosomes, Bacterial / genetics
  • Chromosomes, Bacterial / metabolism
  • Eukaryota / classification
  • Eukaryota / enzymology
  • Eukaryota / genetics*
  • Evolution, Molecular
  • Gene Transfer, Horizontal*
  • Genomic Islands*
  • Phylogeny
  • Plasmids / genetics
  • Plasmids / metabolism
  • Sequence Alignment

Substances

  • Bacterial Proteins
  • Carbonic Anhydrases