Evolution of Tn4371family ICE;traRmediated coordination of cargo gene upregulation and horizontal transfer

Abstract

AbstractICEKKS102Tn4677, which has been shown to transfer horizontally, carriesbphoperon for mineralization of PCBs/biphenyl and belongs to an ICE Tn4371family. In this study we investigated the role oftraRgene encoding a LysR-type transcriptional regulator, which is conserved in sequence, positioning, and directional orientation among Tn4371family ICEs. ThetraRbelonged tobphoperon and its overexpression on solid medium resulted in modest upregulation oftraG(3-fold) and marked upregulation ofxis(80-fold), and enhanced ICE excision, and notably ICE transfer frequency. We propose the evolutional roles oftraR, which upon insertion to the current position, connected the cargo gene activation and ICE-transfer. This property of ICE, transferring under environmental conditions that lead to cargo gene activation, would give fitness advantages to the host bacteria, thereby resulting in efficient dissemination of the Tn4371family ICEs.SignificanceOnly ICEKKS102Tn4677is proven to transfer among the widely disseminating Tn4371family ICEs from β and γ-proteobacteria. We showed that thetraRgene in ICEKKS102Tn4677conserved in the ICE family with fixed location and direction is co-transcribed with the cargo gene and activates ICE transfer. We propose that capturing oftraRby an ancestral ICE to the current position established ICE Tn4371family ICEs. Our findings provide insights into the evolutionary processes that led to the widespread distribution of the Tn4371family of ICEs across bacterial species.