NrrA, a Nitrogen-regulated Response Regulator Protein, Controls Glycogen Catabolism in the Nitrogen-fixing Cyanobacterium Anabaena sp. Strain PCC 7120

Shigeki Ehira,Masayuki Ohmori

doi:10.1074/jbc.m111.289124

Abstract

Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium in which certain vegetative cells differentiate into heterocysts that are specialized cells for nitrogen fixation. Heterocysts are unable to carry out photosynthesis and depend on vegetative cells for carbohydrate to generate ATP and reductants required for nitrogen fixation. Thus, carbohydrate metabolism is very important for nitrogen fixation in the filamentous cyanobacteria; however, its regulatory mechanism remains unknown. In the present study, a nitrogen-regulated response regulator NrrA, which is a transcriptional regulator involved in heterocyst differentiation, was shown to control glycogen catabolism. The transcript levels of genes involved in glycogen catabolism, such as glgP1 and xfp-gap1-pyk1-talB operon, were decreased by the nrrA disruption. Moreover, glycogen accumulation and depression of nitrogenase activities were observed in this disruptant. NrrA bound specifically to the promoter region of glgP1, encoding a glycogen phosphorylase, and to the promoter region of sigE, encoding a group 2 σ factor of RNA polymerase. SigE activated expression of the xfp operon, encoding enzymes of glycolysis and the pentose phosphate pathway. It is concluded that NrrA controls not only heterocyst differentiation but also glycogen catabolism in Anabaena sp. strain PCC 7120.

Highlights

Carbohydrate catabolism provides the energy for nitrogen fixation in filamentous cyanobacteria
In the filamentous cyanobacterium Anabaena sp. strain PCC 7120, we found that the nrrA gene encoding a response regulator of the OmpR family is involved in the regulation of heterocyst differentiation [11]
We demonstrated that NrrA controlled glycogen catabolism in Anabaena PCC 7120 (Fig. 8)

Summary

Background

Carbohydrate catabolism provides the energy for nitrogen fixation in filamentous cyanobacteria. Strain PCC 7120 is a filamentous cyanobacterium in which certain vegetative cells differentiate into heterocysts that are specialized cells for nitrogen fixation. A nitrogen-regulated response regulator NrrA, which is a transcriptional regulator involved in heterocyst differentiation, was shown to control glycogen catabolism. Strain PCC 7120 (hereafter Anabaena PCC 7120), we found that the nrrA gene encoding a response regulator of the OmpR family is involved in the regulation of heterocyst differentiation [11]. Several genes up-regulated by nitrogen deprivation in Anabaena PCC 7120 are involved in carbon metabolism, such as glycogen degradation, glgP1 (all1272); sucrose metabolism, invB (alr0819) and spsB (all4376); the oxidative pentose phosphate pathway, zwf (all4019), gnd (alr5275), talA (all4020), and talB (all2563); and glycolysis, gap (all2566) and pyk (all2564) [11].

EXPERIMENTAL PROCEDURES

RESULTS

DISCUSSION