Expression from DIF1-motif promoters of hetR and patS is dependent on HetZ and modulated by PatU3 during heterocyst differentiation.

Yaru Du,Xudong Xu,Shuai Wang,Hong Wang,He Zhang,Qiqin Lei,Chao Li,Renqiu Kong,Ashutosh Kumar Rai

doi:10.1371/journal.pone.0232383

Abstract

HetR and PatS/PatX-derived peptides are the activator and diffusible inhibitor for cell differentiation and patterning in heterocyst-forming cyanobacteria. HetR regulates target genes via HetR-recognition sites. However, some genes (such as patS/patX) upregulated at the early stage of heterocyst differentiation possess DIF1 (or DIF+) motif (TCCGGA) promoters rather than HetR-recognition sites; hetR possesses both predicted regulatory elements. How HetR controls heterocyst-specific expression from DIF1 motif promoters remains to be answered. This study presents evidence that the expression from DIF1 motif promoters of hetR, patS and patX is more directly dependent on hetZ, a gene regulated by HetR via a HetR-recognition site. The HetR-binding site upstream of hetR is not required for the autoregulation of hetR. PatU3 (3′ portion of PatU) that interacts with HetZ may modulate the expression of hetR, hetZ and patS. These findings contribute to understanding of the mutual regulation of hetR, hetZ-patU and patS/patX in a large group of multicellular cyanobacteria.

Highlights

Cyanobacteria were the first group of microorganisms that performed oxygenic photosynthesis [1, 2]
In a hetR-minus mutant, heterocyst differentiation is not initiated, and genes otherwise expressed in heterocysts are mostly not upregulated after nitrogen stepdown
Co-expression of hetZ and hetP from PntcA enabled the hetR mutant, 7120hetR::C.CE2, to form functional heterocysts at the ends of filaments [34]. Such a phenotype was probably due to the lack of expression of patA, a gene required for heterocyst formation at intercalary positions, in vegetative cells of the hetR mutant [31]

Summary

Introduction

Cyanobacteria were the first group of microorganisms that performed oxygenic photosynthesis [1, 2]. In the early earth environment, nitrogen nutrient was a limiting factor for propagation of microbes. Under this selective pressure, nif genes spread among bacteria, and some cyanobacteria acquired the N2 fixation capability. With the rise of atmospheric oxygen, certain filamentous species developed the capability to form specialized N2-fixing cells, called heterocysts, to protect nitrogenase from inactivation by oxygen [3,4,5]. Heterocyst-forming cyanobacteria contribute significantly to nitrogen fixation in the earth’s biosphere [6,7,8]. In species from different genera of heterocyst-forming cyanobacteria, heterocysts are differentiated at one end, two ends, or intercalary positions of filaments [9].

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