Evolutionary Changes in DnaA-Dependent Chromosomal Replication in Cyanobacteria.

Ryudo Ohbayashi,Chikara Furusawa,Yuu Hirose,Takayuki Fujiwara,Shunsuke Hirooka,Shin-Ya Miyagishima,Yu Kanesaki,Ryo Onuma,Yusuke Kobayashi

doi:10.3389/fmicb.2020.00786

Abstract

Replication of the circular bacterial chromosome is initiated at a unique origin (oriC) in a DnaA-dependent manner in which replication proceeds bidirectionally from oriC to ter. The nucleotide compositions of most bacteria differ between the leading and lagging DNA strands. Thus, the chromosomal DNA sequence typically exhibits an asymmetric GC skew profile. Further, free-living bacteria without genomes encoding dnaA were unknown. Thus, a DnaA-oriC-dependent replication initiation mechanism may be essential for most bacteria. However, most cyanobacterial genomes exhibit irregular GC skew profiles. We previously found that the Synechococcus elongatus chromosome, which exhibits a regular GC skew profile, is replicated in a DnaA-oriC-dependent manner, whereas chromosomes of Synechocystis sp. PCC 6803 and Nostoc sp. PCC 7120, which exhibit an irregular GC skew profile, are replicated from multiple origins in a DnaA-independent manner. Here we investigate the variation in the mechanisms of cyanobacterial chromosome replication. We found that the genomes of certain free-living species do not encode dnaA and such species, including Cyanobacterium aponinum PCC 10605 and Geminocystis sp. NIES-3708, replicate their chromosomes from multiple origins. Synechococcus sp. PCC 7002, which is phylogenetically closely related to dnaA-lacking free-living species as well as to dnaA-encoding but DnaA-oriC-independent Synechocystis sp. PCC 6803, possesses dnaA. In Synechococcus sp. PCC 7002, dnaA was not essential and its chromosomes were replicated from a unique origin in a DnaA-oriC independent manner. Our results also suggest that loss of DnaA-oriC-dependency independently occurred multiple times during cyanobacterial evolution and raises a possibility that the loss of dnaA or loss of DnaA-oriC dependency correlated with an increase in ploidy level.

Highlights

Precise chromosomal DNA replication is required for the inheritance of genetic information during cellular proliferation
The genome sequences of 54 cyanobacterial species deposited in the Pasteur Culture Collection were published in Shih et al (2013), and the complete genome sequences of >500 cyanobacterial species are available in public databases
It has been believed that dnaA is conserved among free-living bacteria (Yoshikawa and Ogasawara, 1991; Messer, 2002; Gao and Zhang, 2007; Katayama et al, 2010), our search revealed that the genomes of the free-living cyanobacterial species Cyanobacterium stanieri PCC 7202, Cyanobacterium sp

Summary

INTRODUCTION

Precise chromosomal DNA replication is required for the inheritance of genetic information during cellular proliferation. The replication origin was experimentally identified in the chromosome of the model cyanobacterium Synechococcus elongatus PCC 7942 (S. elongatus), which exhibits a regular GC skew (Watanabe et al, 2012) In this genome, oriC resides near dnaN, which corresponds to one of the two shift points of the GC skew (Watanabe et al, 2012) (Figure 1). PCC 7120 and the evolutionary relationships among DnaA-oriCdependent and independent species have not been examined To address this gap in our knowledge, here we conducted an up-to-date review of cyanobacterial genome sequences and found that certain free-living species do not encode dnaA.

MATERIALS AND METHODS

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT