Frequent nonhomologous replacement of replicative helicase loaders by viruses in Vibrionaceae

Author:

Tominaga Kento1,Ozaki Shogo2ORCID,Sato Shohei2,Katayama Tsutomu2ORCID,Nishimura Yuki1,Omae Kimiho1,Iwasaki Wataru13456ORCID

Affiliation:

1. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba 277-0882, Japan

2. Department of Molecular Biology, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka 812-8582, Japan

3. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0032, Japan

4. Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba 277-0882, Japan

5. Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba 277-8564, Japan

6. Institute for Quantitative Biosciences, The University of Tokyo, Tokyo 113-0032, Japan

Abstract

Several microbial genomes lack textbook-defined essential genes. If an essential gene is absent from a genome, then an evolutionarily independent gene of unknown function complements its function. Here, we identified frequent nonhomologous replacement of an essential component of DNA replication initiation, a replicative helicase loader gene, in Vibrionaceae . Our analysis of Vibrionaceae genomes revealed two genes with unknown function, named vdhL1 and vdhL2 , that were substantially enriched in genomes without the known helicase-loader genes. These genes showed no sequence similarities to genes with known function but encoded proteins structurally similar with a viral helicase loader. Analyses of genomic syntenies and coevolution with helicase genes suggested that vdhL1/2 encodes a helicase loader. The in vitro assay showed that Vibrio harveyi VdhL1 and Vibrio ezurae VdhL2 promote the helicase activity of DnaB. Furthermore, molecular phylogenetics suggested that vdhL1 / 2 were derived from phages and replaced an intrinsic helicase loader gene of Vibrionaceae over 20 times. This high replacement frequency implies the host’s advantage in acquiring a viral helicase loader gene.

Funder

MEXT | JST | Core Research for Evolutional Science and Technology

MEXT | Japan Society for the Promotion of Science

MEXT

Publisher

Proceedings of the National Academy of Sciences

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