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The next step in heterocyst development is the activation of hetR. Remarkably, null mutants of hetR do not produce heterocysts whereas an overexpression of hetR leads to an increased heterocyst frequency [ 27, 32, 33]. The transcription of hetR is induced by NtcA through the action of an intermediate, nrrA [ 28]. The DNA-binding activity of HetR requires its homodimerization [ 34, 35]. Multiple transcription factors related to heterocyst formation are up-regulated by HetR, including hetR itself [ 35], ntcA [ 36] and patS [ 35]. To get further insights into HetL function, we wondered whether its activity would be mediated by its direct interaction with HetR. To test this, we used the bacterial two hybrid assay (BACTH), which is based on the reconstitution of adenylate cyclase (CyA) activity by two interacting proteins that bring the T18 and T25 domains of CyA into close proximity ( Karimova et al., 1998). T18 and T25 domains were fused to HetR and HetL proteins at their N-terminal extremities, and the dimerization ability of HetR was used as an internal control for this assay. The data in Figure 1B show that HetL displays a strong interaction with HetR. Interestingly, it seems that the HetR-hood domain is sufficient to mediate the interaction of HetR to HetL. Furthermore, this experiment indicated that HetL is able to form dimers (or oligomers) ( Figure 1B).

Rectangular boxes represent genes ( ntcA, hetR and patS) while rounded boxes and circles represent transcription factors (NtcA, HetR and PatS) and smaller molecules (2-OG and cN) respectively. Normal-tipped and flat-tipped arrows stand for up-regulating and down-regulating processes respectively. Dashed lines stand for indirect or imperfectly understood interactions. The accumulation of 2-OG enhances the DNA-binding activity of NtcA, which in turn up-regulates the transcription of ntcA and hetR. HetR activates ntcA and hetR (composing the central NtcA-HetR autoregulatory loop), the inhibitor patS and other genes that lead to nitrogen fixation and the morphological changes involved in heterocyst differentiation. 2-OG and cN levels are linked through the GS/GOGAT cycle (see Fig. 2). Higa KC, Rajagopalan R, Risser DD, Rivers OS, Tom SK, Videau P, et al. (2012) The RGSGR amino acid motif of the intercellular signalling protein, HetN, is required for patterning of heterocysts in Anabaena sp. strain PCC 7120. Mol microbiol 83: 682–693. pmid:22220907Fig 1. Main components and interactions involved in the reaction to combined nitrogen deprivation in cyanobacteria.

Borthakur PB, Orozco CC, Young-Robbins SS, Haselkorn R, Callahan SM: Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol. 2005, 57 (1): 111-123. 10.1111/j.1365-2958.2005.04678.x. Fiedler G, Muro-Pastor A (2001) NtcA-Dependent Expression of the devBCAOperon, Encoding a Heterocyst-Specific ATP-Binding Cassette Transporter in Anabaena spp. J Bacteriol 183: 3795–3799. pmid:11371545 Feldmann, E. A. et al. Differential binding between PatS C-terminal peptide fragments and HetR from Anabaena sp. PCC 7120. Biochemistry 51, 2436–42 (2012).

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Kumar K, Mella-Herrera R, Golden J (2010) Cyanobacterial heterocists. Cold Spring Harb Perspect Biol 2: a000315. pmid:20452939 It was important for us to choose a title which highlights the novelty that our study brings in relation to the state of art in the field. Nonetheless, we understand the importance of broad-significance titles and therefore decided to adopt the proposed one. This work did not involve human subjects, human material, or human data and therefore does not require ethical approval. Availability of supporting data Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012, 9 (7): 671-675. 10.1038/nmeth.2089. Zhang JY, Chen WL, Zhang CC: hetR and patS, two genes necessary for heterocyst pattern formation, are widespread in filamentous nonheterocyst-forming cyanobacteria. Microbiology. 2009, 155 (Pt 5): 1418-1426. 10.1099/mic.0.027540-0.

Vázquez-Bermúdez MF, Herrero A, Flores E (2003) Carbon supply and 2-oxoglutarate effects on expression of nitrate reductase and nitrogen-regulated genes in Synechococcus sp. strain PCC 7942. FEMS Microbiol Lett 221: 155–159. pmid:12725920 NtcA presents autoregulation [ 22, 24, 25] and indirectly activates the key gene that controls cell differentiation and pattern formation: hetR [ 26– 28]. To bind DNA, NtcA needs to homodimerize [ 29, 30]. In conclusion, the accumulation of 2-OG is the factor that triggers differentiation. In agreement with this idea, artificial increased levels of 2-OG result in heterocyst development even in the presence of ammonium [ 16, 18, 31]. The inhibitor PatS is regulated by HetR, and we assume no other influence. For simplicity, we implicitly include the effect of HetN in PatS, as their action is expected to be equivalent (see the previous section). This gives the simple transcription velocity:The Creative Commons Public Domain Dedication waiver ( https://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.