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

Abstract

Background: Carbohydrate catabolism provides the energy for nitrogen fixation in filamentous cyanobacteria. Results: A nitrogen-regulated response regulator NrrA controlled glycogen catabolism in the filamentous cyanobacterium Anabaena sp. PCC 7120. Conclusion: NrrA controls not only cellular differentiation but also carbohydrate metabolism. Significance: A molecular network regulating glycogen metabolism in the nitrogen-fixing cyanobacteria is proposed.

NrrA directly regulates expression of the fraF gene and antisense RNAs for fraE in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120

“…3). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (Fig. 3a).…”

“…NrrA bound to probes D1, D2 and D3 in a similar way to P2395, but no interaction between D4 and NrrA was observed (), indicating that a sequence required for NrrA binding to the fraF promoter was present in the region from −205 to −184. We have previously indicated that the sequence AA(A/T)GTCA is required for NrrA binding to the glgP1 and hetR promoters (Ehira & Ohmori, 2006b, 2011). Eight nucleotides downstream of these sequences, we found incomplete inverted sequences ().…”

“…The NrrA recognition sequence was determined by analysis of the promoter region of fraF (). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (). Deletion up to the upstream side of the IR sequence within the fraF promoter (probe D4) also abolished the interaction between NrrA and the fraF promoter ().…”

NrrA directly regulates expression of the fraF gene and antisense RNAs for fraE in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120

“…3). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (Fig. 3a).…”

“…NrrA bound to probes D1, D2 and D3 in a similar way to P2395, but no interaction between D4 and NrrA was observed (), indicating that a sequence required for NrrA binding to the fraF promoter was present in the region from −205 to −184. We have previously indicated that the sequence AA(A/T)GTCA is required for NrrA binding to the glgP1 and hetR promoters (Ehira & Ohmori, 2006b, 2011). Eight nucleotides downstream of these sequences, we found incomplete inverted sequences ().…”

“…The NrrA recognition sequence was determined by analysis of the promoter region of fraF (). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (). Deletion up to the upstream side of the IR sequence within the fraF promoter (probe D4) also abolished the interaction between NrrA and the fraF promoter ().…”

Regulation of Genes Involved in Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 by a Group 2 Sigma Factor SigC

“…PCC 6803, sigE is also induced by nitrogen starvation under the control of NtcA, while no induction of sigC and sigG is observed [ 33 , 34 ]. In Anabaena PCC 7120, NtcA and NrrA, which are highly expressed in differentiating heterocysts [ 6 , 35 ], bind to the promoter regions of sigE and are involved in the regulation of sigE expression [ 22 , 25 ]. In response to nitrogen deprivation, hetR is necessary for upregulation of ntcA , and NtcA induces the expression of nrrA [ 9 , 17 ].…”

“…The transcript levels of 68 genes were lower in DRsigEK than in the WT strain, including the xfp operon whose expression is activated by sigE [ 25 ] ( Table 5 ). In addition to nif genes ( nifV1 , nifZ , and nifU ), genes required for the synthesis of the glycolipid layer of the heterocyst envelop, namely, devBC [ 40 ] and hglT [ 41 ], and the hetN gene, which suppresses heterocyst differentiation [ 42 ], were downregulated by disruption of sigE .…”

NrrA directly regulates expression of the fraF gene and antisense RNAs for fraE in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120

“…3). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (Fig. 3a).…”

“…NrrA bound to probes D1, D2 and D3 in a similar way to P2395, but no interaction between D4 and NrrA was observed (), indicating that a sequence required for NrrA binding to the fraF promoter was present in the region from −205 to −184. We have previously indicated that the sequence AA(A/T)GTCA is required for NrrA binding to the glgP1 and hetR promoters (Ehira & Ohmori, 2006b, 2011). Eight nucleotides downstream of these sequences, we found incomplete inverted sequences ().…”

“…The NrrA recognition sequence was determined by analysis of the promoter region of fraF (). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (). Deletion up to the upstream side of the IR sequence within the fraF promoter (probe D4) also abolished the interaction between NrrA and the fraF promoter ().…”

Regulation of Genes Involved in Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 by a Group 2 Sigma Factor SigC

“…PCC 6803, sigE is also induced by nitrogen starvation under the control of NtcA, while no induction of sigC and sigG is observed [ 33 , 34 ]. In Anabaena PCC 7120, NtcA and NrrA, which are highly expressed in differentiating heterocysts [ 6 , 35 ], bind to the promoter regions of sigE and are involved in the regulation of sigE expression [ 22 , 25 ]. In response to nitrogen deprivation, hetR is necessary for upregulation of ntcA , and NtcA induces the expression of nrrA [ 9 , 17 ].…”

“…The transcript levels of 68 genes were lower in DRsigEK than in the WT strain, including the xfp operon whose expression is activated by sigE [ 25 ] ( Table 5 ). In addition to nif genes ( nifV1 , nifZ , and nifU ), genes required for the synthesis of the glycolipid layer of the heterocyst envelop, namely, devBC [ 40 ] and hglT [ 41 ], and the hetN gene, which suppresses heterocyst differentiation [ 42 ], were downregulated by disruption of sigE .…”

NrrA directly regulates expression of the fraF gene and antisense RNAs for fraE in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120

“…3). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (Fig. 3a).…”

“…NrrA bound to probes D1, D2 and D3 in a similar way to P2395, but no interaction between D4 and NrrA was observed (), indicating that a sequence required for NrrA binding to the fraF promoter was present in the region from −205 to −184. We have previously indicated that the sequence AA(A/T)GTCA is required for NrrA binding to the glgP1 and hetR promoters (Ehira & Ohmori, 2006b, 2011). Eight nucleotides downstream of these sequences, we found incomplete inverted sequences ().…”

“…The NrrA recognition sequence was determined by analysis of the promoter region of fraF (). In a previous study (Ehira & Ohmori, 2011), we have shown that the sequence AAAGTCA within the glgP1 promoter and the sequence AATGTCA within the hetR promoter, which include the upstream side of the IR sequence, are indispensable for the binding of NrrA (). Deletion up to the upstream side of the IR sequence within the fraF promoter (probe D4) also abolished the interaction between NrrA and the fraF promoter ().…”

Regulation of Genes Involved in Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 by a Group 2 Sigma Factor SigC

“…PCC 6803, sigE is also induced by nitrogen starvation under the control of NtcA, while no induction of sigC and sigG is observed [ 33 , 34 ]. In Anabaena PCC 7120, NtcA and NrrA, which are highly expressed in differentiating heterocysts [ 6 , 35 ], bind to the promoter regions of sigE and are involved in the regulation of sigE expression [ 22 , 25 ]. In response to nitrogen deprivation, hetR is necessary for upregulation of ntcA , and NtcA induces the expression of nrrA [ 9 , 17 ].…”

“…The transcript levels of 68 genes were lower in DRsigEK than in the WT strain, including the xfp operon whose expression is activated by sigE [ 25 ] ( Table 5 ). In addition to nif genes ( nifV1 , nifZ , and nifU ), genes required for the synthesis of the glycolipid layer of the heterocyst envelop, namely, devBC [ 40 ] and hglT [ 41 ], and the hetN gene, which suppresses heterocyst differentiation [ 42 ], were downregulated by disruption of sigE .…”