Rapid functional activation of horizontally transferred eukaryotic intron-containing genes in the bacterial recipient

Author:

Yuan Wen12,Yu Jing13,Li Zhichao12ORCID

Affiliation:

1. National Technology Innovation Center of Synthetic Biology , Tianjin  300308 , China

2. Key Laboratory of Systems Microbial Biotechnology, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences , Tianjin  300308 , China

3. Biodesign Center, Key Laboratory of Engineering Biology for Low-carbon Manufacturing, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences , Tianjin 300308,  China

Abstract

Abstract Horizontal gene transfer has occurred across all domains of life and contributed substantially to the evolution of both prokaryotes and eukaryotes. Previous studies suggest that many horizontally transferred eukaryotic genes conferred selective advantages to bacterial recipients, but how these eukaryotic genes evolved into functional bacterial genes remained unclear, particularly how bacteria overcome the expressional barrier posed by eukaryotic introns. Here, we first confirmed that the presence of intron would inactivate the horizontally transferred gene in Escherichia coli even if this gene could be efficiently transcribed. Subsequent large-scale genetic screens for activation of gene function revealed that activation events could rapidly occur within several days of selective cultivation. Molecular analysis of activation events uncovered two distinct mechanisms how bacteria overcome the intron barrier: (i) intron was partially deleted and the resulting stop codon-removed mutation led to one intact foreign protein or (ii) intron was intactly retained but it mediated the translation initiation and the interaction of two split small proteins (derived from coding sequences up- and downstream of intron, respectively) to restore gene function. Our findings underscore the likelihood that horizontally transferred eukaryotic intron-containing genes could rapidly acquire functionality if they confer a selective advantage to the prokaryotic recipient.

Funder

National Key Research and Development Program of China

Tianjin Synthetic Biotechnology Innovation Capacity Improvement Project

The ability establishment of sustainable use for valuable Chinese medicine resources

Publisher

Oxford University Press (OUP)

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