Abstract

Foreign AT-rich genes drive bacterial adaptation to new niches while challenging the existing regulation network. Here we report that MucR, a conserved regulator in α-proteobacteria, balances adaptation and regulatory integrity in Sinorhizobium fredii, a facultative microsymbiont of legumes. Chromatin immunoprecipitation sequencing coupled with transcriptomic data reveal that average transcription levels of both target and non-target genes, under free-living and symbiotic conditions, increase with their conservation levels. Targets involved in environmental adaptation and symbiosis belong to genus or species core and can be repressed or activated by MucR in a condition-dependent manner, implying regulatory integrations. However, most targets are enriched in strain-specific genes of lower expression levels and higher AT%. Within each conservation levels, targets have higher AT% and average transcription levels than non-target genes and can be further up-regulated in the mucR mutant. This is consistent with higher AT% of spacers between −35 and −10 elements of promoters for target genes, which enhances transcription. The MucR recruitment level linearly increases with AT% and the number of a flexible pattern (with periodic repeats of Ts) of target sequences. Collectively, MucR directly represses AT-rich foreign genes with predisposed high transcription potential while progressive erosions of its target sites facilitate regulatory integrations of foreign genes.

Highlights

  • The distribution and abundance of organisms can be proximally explained in the scenario of the multi-dimensional niche while its ultimate explanation demands evolutionary understanding [1]

  • MucR1 in S. fredii CCBAU45436 (SF45436) has the conserved prokaryotic zinc-finger motif X2Cys-X2-Cys-X9-His-X3-His-X2 (Fig. 1A) that is a characterized feature of ROS_MUCR (PF05443) family protein widely distributed in αproteobacteria (Fig. 1B)

  • Western blot using both free-living cells and symbiotic bacteroids demonstrated the specificity of monoclonal anti-GST antibody (Fig. 1D) that was used in subsequent chromatin immunoprecipitation (ChIP)-seq experiment

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Summary

Introduction

The distribution and abundance of organisms can be proximally explained in the scenario of the multi-dimensional niche while its ultimate explanation demands evolutionary understanding [1]. The modern synthesis of evolution summarized by Julian Huxley in 1942 can be briefly outlined by its core tenet that “adaptive evolution” is a process, in which natural selection acts on heritable variability originating from accidental genetic changes, leading to increased frequency of advantageous variants and adaptation [2, 3]. This adaptive evolution framework is still the root of the current standard evolutionary theory which recognizes four evolutionary processes (selection, mutation, recombination, and genetic drift) and only considers selection as a directional force increasing organismal adaptation [3]. The maintenance and recruitment mechanism of foreign genes in the regulation scenario is a key to understand adaptation, speciation and the “home life” of living organisms, though it is largely unexplored

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