The horizontal gene transfer of perchlorate reduction genomic island in three bacteria from an ecological niche

Appl Microbiol Biotechnol. 2024 Dec;108(1):22. doi: 10.1007/s00253-023-12827-3. Epub 2023 Dec 30.

Abstract

Three new strains of dissimilatory perchlorate-reducing bacteria (DPRB), QD19-16, QD1-5, and P3-1, were isolated from an active sludge. Phylogenetic trees based on 16S rRNA genes indicated that QD19-16, QD1-5, and P3-1 belonged to Brucella, Acidovorax, and Citrobacter, respectively, expanding the distribution of DPRB in the Proteobacteria. The three strains were gram-negative and facultative anaerobes with rod-shaped cells without flagella, which were 1.0-1.6 μm long and 0.5-0.6 μm wide. The three DPRB strains utilized similar broad spectrum of electron donors and acceptors and demonstrated a similar capability to reduce perchlorate within 6 days. The enzyme activity of perchlorate reductase in QD19-16 toward chlorate was higher than that toward perchlorate. The high sequence similarity of the perchlorate reductase operon and chlorite dismutase genes in the perchlorate reduction genomic islands (PRI) of the three strains implied that they were monophyletic origin from a common ancestral PRI. Two transposase genes (tnp1 and tnp2) were found in the PRIs of strain QD19-16 and QD1-5, but were absent in the strain P3-1 PRI. The presence of fragments of IR sequences in the P3-1 PRI suggested that P3-1 PRI had previously contained these two tnp genes. Therefore, it is plausible to suggest that a common ancestral PRI transferred across the strains Brucella sp. QD19-16, Acidovorax sp. QD1-5, and Citrobacter sp. P3-1 through horizontal gene transfer, facilitated by transposases. These results provided a direct evidence of horizontal gene transfer of PRI that could jump across phylogenetically unrelated bacteria through transposase. KEY POINTS: • Three new DPRB strains can effectively remove high concentration of perchlorate. • The PRIs of three DPRB strains are acquired from a single ancestral PRI. • PRIs are incorporated into different bacteria genome through HGT by transposase.

Keywords: Dissimilatory perchlorate-reducing bacteria; Ecological niche; Horizontal gene transfer; Perchlorate reduction genomic island; Proteobacteria.

MeSH terms

  • Bacteria / genetics
  • Ecosystem
  • Gene Transfer, Horizontal
  • Genomic Islands*
  • Oxidation-Reduction
  • Oxidoreductases / genetics
  • Perchlorates*
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • Transposases / genetics

Substances

  • perchlorate
  • Perchlorates
  • RNA, Ribosomal, 16S
  • Oxidoreductases
  • Transposases