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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:22220907 Heterocyst pattern was first speculated to be controlled by a pentapeptide RGSGR (designated as PatS5), a motif which was identified first as the C-terminal five residues of PatS 16 and later within a putative ketoacyl reductase HetN 17. Binding of PatS5 to HetR may abolish the DNA-binding capacity of HetR 11, a proposed mechanism to prevent the occurrence of multiple contiguous heterocysts ( Fig. 1). The in vitro binding assays suggested that two PatS5 molecules bind to a HetR homodimer at a dissociation constant K d of 227 nM 18, most likely at the proximity of the C-terminal region 18. Notably, HetR has a higher affinity towards a hexapeptide ERGSGR (termed PatS6, at a K d of 7 nM), compared to that of PatS5 19. However, the in vivo experiments suggested that the last eight residues could recreate the full activity of the native PatS 20. Thus the bona fide active form of PatS under physiological conditions remains unknown. In this work, we develop a simple mathematical model by incorporating the recent experimental results on the genetic regulatory network of cyanobacteria into the theoretical machinery of system biology.

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. Buchler NE, Gerland U, Hwa T (2003) On schemes of combinatorial transcription logic. Proc Natl Acad Sci 100: 5136–5141. pmid:12702751 Huang X, Dong Y, Zhao J (2004) HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. P Natl Acad Sci USA 101: 4848–4853.

Acknowledgments

Schematic representation of the diffusion processes that sustain the heterocyst pattern. Heterocysts produce cN and PatS. cN diffuses along the filament where, due to the action of the GS/GOGAT cycle (see Fig. 2), decreases the levels of 2-OG breaking the autoregulatory core NtcA-HetR. Early during the differentiation, PatS (or other derivative of it, see the text) diffuses along the filament inhibiting HetR. Both processes combined prevent the differentiation of the rest of vegetative cells and explain the formation of the pattern. Ramasubramanian TS, Wei TF, Oldham aK, Golden JW (1996) Transcription of the Anabaena sp. strain PCC 7120 ntcA gene: multiple transcripts and NtcA binding. J Bacteriol 178: 922–926. pmid:8550535 By reducing the flow of cN from the exterior of the cell ( l n = 0) we find that a stable fixed point appears in the upper branch, a heterocyst state, while the vegetative state gets closer to the bifurcation region, thus becoming more susceptible to perturbations that can make the system reach the upper branch. In the absence of cN, the cyanobacterium would evolve from state A to state B in the lower branch until a perturbation pushes it to the upper branch, eventually becoming an heterocyst due to the field acting on that branch ( Fig. 5B and C). Distinct from the previously reported HTH motif 25, the DNA-binding motif of HetR is composed of three helices: the two canonical helices α4 and α5, in addition to an auxiliary helix α10 from the symmetric subunit. Moreover, both the flap and the hood domains adopt novel folds; thus HetR represents a novel transcription factor. The DNA-binding pattern of Anabaena HetR Mitchison GJ, Wilcox M, Smith RJ (1976) Measurement of an inhibitory zone. Science 191: 866–868. pmid:814620

Valladares A, Muro-pastor AM, Herrero A, Flores E (2004) The NtcA-Dependent P 1 Promoter Is Utilized for glnA Expression in N 2—Fixing Heterocysts of Anabaena sp. Strain PCC 7120. J Bacteriol 186: 7337–7343. pmid:15489445 which constitutes the model for a cyanobacteria filament. To account for environment variability we add white noise, G i, *( t), of the same amplitude, ⟨ G i, *( t) G i, *( t ′)⟩ = ξδ( t − t ′), for all the components of the system. Based on these equations, we investigate the conditions that lead to a heterocyst pattern. It is easy to notice that they correspond to an activator-inhibitor system of cells coupled in a reaction-diffusion scheme [ 50]. This kind of system produces regular pattern formation [ 51– 53]. Turing (linear stability) analysis of equations (16) (see S2 text) provides insight on the periodicity of patterns. It is interesting to show that the minimum periodicity observed in such analysis is larger than 1, which means that a single bacteria is unable to differentiate. Kondo, S. & Miura, T. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616–1620 (2010). Buikema WJ, Haselkorn R: Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev. 1991, 5 (2): 321-330. 10.1101/gad.5.2.321.Purified HetR and mutants were dialyzed against a buffer containing 1 M NaCl, 5% (v/v) glycerol and 10 mM Tris-Cl, pH 7.8 for 12 hr. The data were collected on an iTC200 (MicroCal) at 25 °C by injecting an initial 0.4 μl aliquot and the following 19 consecutive 2 μl aliquots. The sample cell was loaded with 200 μl protein while the injection syringe was loaded with 40 μl PatS6. The wild-type HetR, mutants E254A and D256A were diluted to a final concentration of 10 μM, whereas the concentration of mutants R223W, E253A, D270A, D278A, D270A/D278A and HetR Hood was 50 μM. The concentration of PatS6 was 15 times (150 or 750 μM) to that of the full-length protein or 40 times (2 mM) to that of HetR Hood. EMSA assays Morelli LG, Uriu K, Ares S, Oates AC (2013) Computational Approaches to Developmental Patterning. Science 336: 187–191. Alternatively, it can be assumed that in the (pro)heterocyst the affinity of HetR for HetL must be higher than that for PatS. Bli and ITC experiments showed that in vitro, the affinity of HetR for PatS is 10-fold higher than for HetL (compare data of Figure 2C and Figure 3). One might speculate that in vivo, and especially in the (pro)heterocyst, the affinity of HetR for HetL increases either due to a modification of HetR or to its interaction with another factor. HetR has been shown to be regulated by phosphorylation ( Valladares et al., 2016; Roumezi et al., 2019), if this posttranslational modification occurs only in the developing cell it could explain a high affinity of HetR for HetL specifically in the heterocyst. In addition, the observation that the overexpression of hetL in vegetative cells, from petE or rbcL promoters, did not lead to their differentiation into heterocsyts is rather in favor of a mechanism promoting the association between HetR and HetL specifically in the heterocyst. Resolving the structure of HetR-HetL complex and following the behavior of HetL protein and PatS in vivo will provide more information about the dynamics and the nature of HetR complexes in the two cell types through the differentiation process. Yoon Hs, Golden JW (2001) PatS and Products of Nitrogen Fixation Control Heterocyst Pattern PatS and Products of Nitrogen Fixation Control Heterocyst Pattern. J Bacteriol 183: 2605–2613. pmid:11274121 Young-Robbins SS, Risser DD, Moran JR, Haselkorn R, Callahan SM: Transcriptional regulation of the heterocyst patterning gene patA from Anabaena sp. strain PCC 7120. J Bacteriol. 2010, 192 (18): 4732-4740. 10.1128/JB.00577-10.

Mitchison GJ, Smith RJ, Road H (1973) Pattern formation in the blue-green alga, anabaena. I. Basic Mechanisms. J Cell Sci 12: 707–723. pmid:4198321Wolk, C. P. Physiological basis of the pattern of vegetative growth of a blue-green alga. Proc. Natl. Acad. Sci. USA 57, 1246–51 (1967). KUALA LUMPUR: Malaysia’s Hydrogen Economy and Technology Roadmap (HETR) has been launched, pushing the country to the forefront of energy transition and to becoming a regional leader in the renewable energy (RE) industry. Kumar K, Mella-Herrera RA, Golden JW: Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol. 2010, 2 (4): a000315-10.1101/cshperspect.a000315. Sequencing reads from the experimental HetR-6xHis sample were randomly assigned to three files and the full ChIP-seq analysis was performed on each sample as a technical replicate. ChIP-seq reads from the three HetR-6xHis samples and the WT sample were aligned to NCBI's current build of the Anabaena genome with CLC Genomics Workbench 5. ChIP peaks were called using a 100 bp window and a false discovery rate of 5% with the WT sample as the control using CLC's ChIP Analysis pipeline. ChIP peaks were excluded from the final data set if they were not present in at least two of the three technical replicates. All peaks were verified by eye prior to further analysis. Promoter-gfp reporter fusion construction

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. Wu X, Liu D, Lee MH, James W, Golden JW (2004) patS Minigenes Inhibit Heterocyst Development of Anabaena sp. Strain PCC 7120 patS Minigenes Inhibit Heterocyst Development of Anabaena sp. Strain PCC 7120. J Bacteriol 186: 6422–6429. pmid:15375122 Muro-Pastor, A. M., Valladares, A., Flores, E. & Herrero, A. Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol. Microbiol. 44, 1377–85 (2002). 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. Similar to the structures of Fischerella HetR 23, 24, each Anabaena HetR subunit contains three distinct domains: the N-terminal DBD (residues 1–98), the middle flap domain (residues 99–216) and a slightly smaller C-terminal hood domain (residues 217–299) ( Fig. 2a). The DBD has a HTH motif (α4 and α5) that inserts into the major groove of DNA. Notably, the partially palindromic DNA sequence in our structure is exactly the same as the HetR recognition sequence in the hetP promoter 12, whereas the DNA sequence in the previous Fischerella HetR structures is derived from the hetP promoter region but modified to be perfectly palindromic 24. Due to a sequence identity of 90% between Anabaena and Fischerella HetR proteins, the two DNA-complexed structures (PDB 4YRV and 4IZZ) are quite similar to each other with a root-mean-square deviation (RMSD) of 1.0 Å over 462 Cα atoms. In both structures, HetR adopts an active conformation, with the two 33.0 Å-apart HTH motifs perfectly accommodated in a successive DNA major groove. Moreover, the two flap domains in both complex structures adopt the same conformation and orientation ( Fig. 2b), which are stabilized by the duplex DNA via interactions with the two α10 helices.The last stages of heterocyst development cause the physiological changes of the cell aimed at creating an anaerobic environment that sustains nitrogen fixation. To this end, two new membrane layers are biosynthesized to decrease the entry of oxygen into the cell [ 44]. The morphogenesis of these two layers is controlled by two family of genes, hep and hgl, that are indirectly up-regulated by HetR [ 35]. After these morphological changes the genes in charge of nitrogen fixation, nif genes, are expressed. These genes encode, among others, the enzyme nitrogenase, which ultimately performs nitrogen fixation. Schirrmeister B, Antonelli A, Bagheri H (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11: 45. pmid:21320320