Abstract
In response to deprivation of combined nitrogen, the filamentous cyanobacterium Anabaena sp. strain PCC 7120 develops heterocyst, which is specifically involved in the nitrogen fixation. In this study, we focused on the regulation of HanA, a histone-like protein, in heterocyst development. Electrophoretic mobility shift assay results showed that NtcA, a global nitrogen regulator necessary for heterocyst differentiation, could bind to two NtcA-binding motifs in the hanA promoter region. qPCR results also showed that NtcA may regulate the expression of hanA. By using the hanA promoter-controlled gfp as a reporter gene and performing western blot we found that the amount of HanA in mature heterocysts was decreased gradually.
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Boubrik F, Rouviere-Yaniv J (1995) Increased sensitivity to gamma irradiation in bacteria lacking protein HU. Proc Natl Acad Sci USA 92:3958–3962
Bramhill D, Kornberg A (1988) A model for initiation at origins of DNA replication. Cell 54:915–918
Cai Y, Wolk CP (1997) Anabaena sp. strain PCC 7120 responds to nitrogen deprivation with a cascade-like sequence of transcriptional activations. J Bacteriol 179:267–271
Chen H, Laurent S, Bédu S, Ziarelli F, Chen HL, Cheng Y, Zhang CC, Peng L (2006) Studying the signaling role of 2-oxoglutaric acid using analogs that mimic the ketone and ketal forms of 2-oxoglutaric acid. Chem Biol 13:849–856
Dixon NE, Kornberg A (1984) Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc Natl Acad Sci USA 81:424–428
Dri AM, Rouviere-Yaniv J, Moreau PL (1991) Inhibition of cell division in hupA hupB mutant bacteria lacking HU protein. J Bacteriol 173:2852–2863
Ehira S, Ohmori M (2006) NrrA, a nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 59:1692–1703
Fernández S, Rojo F, Alonso JC (1997) The Bacillus subtilis chromatin- associated protein Hbsu is involved in DNA repair and recombination. Mol Microbiol 23:1169–1179
Frías JE, Flores E, Herrero A (1994) Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14:823–832
Giangrossi M, Giuliodori AM, Gualerzi CO, Pon CL (2002) Selective expression of the beta-subunit of nucleoid-associated protein HU during cold shock in Escherichia coli. Mol Microbiol 44:205–216
Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183:411–425
Herrero A, Muro-Pastor AM, Valladares A, Flores E (2004) Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487
Jang J, Wang L, Jeanjean R, Zhang CC (2007) PrpJ, a PP2C-type protein phosphatase located on the plasma membrane, is involved in heterocyst maturation in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 64:247–358
Kano Y, Yoshino S, Wada M, Yokoyama K, Nobuhara M, Imamoto F (1985) Molecular cloning and nucleotide sequence of the HU-1gene of Escherichia coli. Mol Gen Genet 201:360–362
Kano Y, Wada M, Nagase T, Imamoto F (1986) Genetic characterization of the gene hupB encoding the HU-1 protein of Escherichia coli. Gene 45:37–44
Kano Y, Osato K, Wada M, Imamoto F (1987) Cloning and sequencing of the HU-2 gene of Escherichia coli. Mol Gen Genet 209:408–410
Khudyakov I, Wolk CP (1996) Evidence that the hanA gene coding for HU protein is essential for heterocyst differentiation in, and cyanophage A-4(L) sensitivity of, Anabaena sp. strain PCC 7120. J Bacteriol 178:3572–3577
Klint J, Rasmussen U, Bergman B (2007) FtsZ may have dual roles in the filamentous cyanobacterium Nostoc/Anabaena sp. strain PCC 7120. J Plant Physiol 164:11–18
Köhler P, Marahiel MA (1998) Mutational analysis of the nucleoid-associated protein HBsu of Bacillus subtilis. Mol Gen Genet 260:487–491
Laurent S, Chen H, Bédu S, Ziarelli F, Peng L, Zhang CC (2005) Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci USA 102:9907–9912
Li S, Waters R (1998) Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J Bacteriol 180:3750–3756
Li JH, Laurent S, Konde V, Bédu S, Zhang CC (2003) An increase in the level of 2-oxoglutarate promotes heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 149:3257–3263
López-Gomollón S, Hernández JA, Pellicer S, Angarica VE, Peleato ML, Fillat MF (2007) Cross-talk between iron and nitrogen regulatory networks in Anabaena (Nostoc) sp. PCC 7120: identification of overlapping genes in FurA and NtcA regulons. J Mol Biol 374:267–281
Mariscal V, Herrero A, Nenninger A, Mullineaux CW, Flores E (2011) Functional dissection of the three-domain SepJ protein joining the cells in cyanobacterial trichomes. Mol Microbiol 79:1077–1088
Mitschke J, Vioque A, Haas F, Hess WR, Muro-Pastor AM (2011) Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci USA 108:20130–20135
Miyabe I, Zhang QM, Kano Y, Yonei S (2000) Histone-like protein HU is required for recA gene-dependent DNA repair and SOS induction pathways in UV-irradiated Escherichia coli. Int J Radiat Biol 76:43–49
Morales P, Rouviere-Yaniv J, Dreyfus M (2002) The histone-like protein HU does not obstruct movement of T7 RNA polymerase in Escherichia coli cells but stimulates its activity. J Bacteriol 184:1565–1570
Morisato D, Kleckner N (1987) Tn10 transposition and circle formation in vitro. Cell 51:101–111
Nagaraja R, Haselkorn R (1994) Protein HU from the cyanobacterium Anabaena. Biochimie 76:1082–1089
Picossi S, Flores E, Herrero A (2014) ChIP analysis unravels an exceptionally wide distribution of DNA binding sites for the NtcA transcription factor in a heterocyst-forming cyanobacterium. BMC Genom. doi:10.1186/1471-2164-15-22
Sakr S, Jeanjean R, Zhang CC, Arcondeguy T (2006) Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 188:1396–1404
Shi L, Li JH, Cheng Y, Wang L, Chen WL, Zhang CC (2007) Two genes encoding protein kinases of the HstK family are involved in synthesis of the minor heterocyst-specific glycolipid in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 89:5075–5081
Su Z, Olman V, Mao F, Xu Y (2005) Comparative genomics analysis of NtcA regulons in cyanobacteria: regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res 33:5156–5171
Vázquez-Bermúdez MF, Flores E, Herrero A (2002a) Analysis of binding sites for the nitrogen-control transcription factor NtcA in the promoters of Synechococcus nitrogen-regulated genes. Biochim Biophys Acta 1578:95–98
Vázquez-Bermúdez MF, Herrero A, Flores E (2002b) 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett 512:71–74
Wada M, Kano Y, Ogawa T, Okazaki T, Imamoto F (1988) Construction and characterization of the deletion mutant of hupA and hupB genes in Escherichia coli. J Mol Biol 204:581–591
Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176:4473–4482
Wery M, Woldringh CL, Rouviere-Yaniv J (2001) HU-GFP and DAPI co-localize on the Escherichia coli nucleoid. Biochimie 83:193–200
Wu X, Iwai N, Chen WL (2011) Effects of S-(3,4-dichlorobenzyl) isothiourea on different cellular events in the cyanobacterium Anabaena sp. strain PCC 7120. Res Microbiol 162:375–381
Zhang CC, Libs L (1998) Cloning and characterisation of the pknD gene encoding an eukaryotic-type protein kinase in the cyanobacterium Anabaena sp. PCC7120. Mol Gen Genet 258:26–33
Zhang CC, Laurent S, Sakr S, Peng L, Bédu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375
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This study was supported by the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry, and the Natural Science Foundation of Nantong University (Grant No. 11Z034).
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Jing-jing Lu and Lei Shi have contributed to this work equally.
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Lu, Jj., Shi, L., Chen, Wl. et al. The regulation of HanA during heterocyst development in cyanobacterium Anabaena sp. PCC 7120. World J Microbiol Biotechnol 30, 2673–2680 (2014). https://doi.org/10.1007/s11274-014-1691-3
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DOI: https://doi.org/10.1007/s11274-014-1691-3