The ability of cyanobacteria to perform oxygenic photosynthesis is thought to have converted the early reducing atmosphere into an oxidizing one, which dramatically changed the composition of life forms on Earth by stimulating biodiversity and leading to the near-extinction of oxygen-intolerant organisms.
According to the endosymbiotic theory, chloroplasts in plants and eukaryotic algae have evolved from cyanobacterial ancestors via endosymbiosis. Cyanobacteria can be found in almost every terrestrial and aquatic habitat. Aquatic cyanobacteria are probably best known for the extensive and visible blooms that can form in both freshwater and the marine environment. These can have the appearance of blue-green paint or scum.
The association of toxicity with such blooms has frequently led to the closure of recreational waters when blooms are observed. Cyanobacteria include unicellular and colonial species. Colonies may form filaments, sheets, or even hollow balls. Some filamentous colonies show the ability to differentiate into several different cell types, including:. These molecules can be absorbed by plants and converted into protein and nucleic acids.
Many cyanobacteria form motile filaments called hormogonia, that travel from the main biomass to bud and form new colonies elsewhere. The cells in a hormogonium are often thinner than those found in the vegetative state, and the cells on either end of the motile chain may be tapered. Molecular composition of the outer membrane of Escherichia coli and the importance of protein-lipopolysaccharide interactions. Gray, M. The evolutionary origins of organelles.
Trends Genet. Groisman, E. Gunzel, D. Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Hahn, A.
The cell envelope. Enrique and H. Antonia, eds. Hancock, R. Alterations in outer membrane permeability. Hattori, M. Nature , — EMBO J. Heidrich, J. Hennig, R. IM30 triggers membrane fusion in cyanobacteria and chloroplasts. Hermans, C. An update on magnesium homeostasis mechanisms in plants. Metallomics 5 , Hertig, C. Hmiel, S. Magnesium transport in Salmonella typhimurium : characterization of magnesium influx and cloning of a transport gene.
Irving, H. Order of stability of metal complexes. Ishijima, S. Izawa, S. Effect of salts and electron transport on the conformation of isolated chloroplasts.
Light-scattering and volume changes. Cruz, J. Biochemistry 40 , — Role of ions in the regulation of light-harvesting. Kaneko, T. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. Sequence determination of the entire genome and assignment of potential protein-coding regions.
DNA Res. Kehres, D. Structure, properties and regulation of magnesium transport proteins. BioMetals 15 , — Keren, N. Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Kimura, T. Kirchhoff, H. Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43 , — Knoop, V. Genomics , — Kobayashi, N. Critical issues in the study of magnesium transport systems and magnesium deficiency symptoms in plants.
Krause, G. Light-induced movement of magnesium ions in intact chloroplasts. Spectroscopic determination with Eriochrome Blue SE. Kung, F. Metal ion content of Escherichia coli versus cell age.
Li, H. Plant Cell Physiol. Li, T. A putative magnesium transporter Slr involved in sodium tolerance in cyanobacterium Synechocystis sp. PCC Algal Res. Liberton, M. Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. Protoplasma , — Global proteomic analysis reveals an exclusive role of thylakoid membranes in bioenergetics of a model cyanobacterium. Liu, L. Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes.
Acta Bioenerget. Lunin, V. Lusk, J. Magnesium and the growth of Escherichia coli. Lyu, H. The fraE mutant has a distinct phenotype showing negligible nitrogenase activity, whereas the fraC and fraD mutants show nitrogenase activity lower than the wild type but detectable Merino-Puerto et al. Structurally, whereas the fraE mutant makes heterocysts that lack a well-formed heterocyst neck, the fraC and fraD mutants make heterocysts showing heterocyst necks in which the septal region of the heterocyst cytoplasmic membrane is withdrawn towards the heterocyst interior Merino-Puerto et al.
FraF is a pentapeptide-repeat protein with a structure, as predicted by Phyre2 www. Whereas the mechanism through which FraF restricts filament length is unknown, the presence of fraF in a filamentation gene cluster may indicate a role in counteracting the effect of positive filamentation proteins such as FraC, FraD and FraE.
It has been conjectured that since the pentapeptide repeat domain has the structure of a rectangular parallelepiped, pentapeptide repeat proteins may interact by stacking Liu and Wolk Possible interactions between these pentapeptide repeat proteins or between them and filamentation proteins are, however, yet to be investigated.
The fraH gene is in a chromosomal location distant from the other fra genes Kaneko et al. The increased expression of fraH under nitrogen deprivation may be related to a specific role of FraH in heterocyst differentiation Merino-Puerto et al.
FraH is a amino-acid protein composed of three domains: an N-terminal region with a putative double zinc ribbon domain residues 4—48 , a central domain residues 58— rich in Pro The zinc ribbon and FHA domains are known molecular interaction domains the latter frequently involving phosphoproteins , and the Pro-rich domain is reminiscent of plant cell wall extensins.
Finally, fraH is generally found in the genomes of heterocyst-forming cyanobacteria and frequently in other cyanobacteria downstream of the gene encoding 6-phosphogluconolactonase of the pentose phosphate pathway, alr in Anabaena.
In summary, FraH is a protein likely involved in protein—protein interactions that may have a role in the differentiation of the heterocyst polar regions. This may be related to the observation that the filament fragmentation phenotype of fraH mutants involves the frequent release of heterocysts from the filaments Bauer et al. Heterocyst differentiation takes place mainly in response to the external cue of combined nitrogen deprivation. During differentiation, the structural changes described earlier are accompanied by extensive modifications of cellular metabolism.
Thus, the phototropic metabolism of the mother vegetative cell is transformed to a photoheterotrophic metabolism that facilitates the function of the nitrogenase complex, which is expressed in the differentiated heterocyst. All these structural and metabolic changes result from the establishment of a pattern of gene expression that conspicuously differs from that taking place in the vegetative cells for more extensive reviews on this topic, see Xu, Elhai and Wolk ; Kumar, Mella-Herrera and Golden ; Herrero, Picossi and Flores Gene expression during heterocyst differentiation is orchestrated by two main transcription factors, NtcA and HetR.
Whereas HetR is specifically required for cellular differentiation Flaherty, Johnson and Golden , NtcA is a global regulator of universal distribution in cyanobacteria that belongs to the CRP family of transcription factors and responds primarily to the cue of nitrogen deficiency Picossi, Flores and Herrero At advanced stages of differentiation transcription activation by NtcA is aided by the small protein PipX Valladares et al.
The ntcA and hetR genes are subject to positive mutual regulation and to auto-regulation, and together they activate or repress many heterocyst differentiation genes in a hierarchical manner see Herrero, Picossi and Flores for a detailed description. Among the activated genes, patS and hetN have been identified to play a role in the establishment of the pattern of heterocyst distribution along the filament, which in Anabaena consists of linear arrays of heterocysts separated by about 10—15 vegetative cells.
The heterocysts are terminal cells that do not divide. Notably, under steady-state diazotrophic growth, the heterocyst pattern is maintained by differentiation of new heterocysts at about the center of the vegetative cell intervals, which increase through vegetative cell division.
In Anabaena the patS gene is transcribed at low levels during growth in the presence of ammonium, and its expression is activated early during differentiation in small cell clusters. Inactivation of patS increases the total number of heterocysts and leads to the multiple contiguous heterocysts Mch phenotype, whereas its over-expression in vegetative cells abolishes differentiation Yoon and Golden , ; Corrales-Guerrero, Flores and Herrero ; Corrales-Guerrero et al.
The primary patS gene product is a peptide of 17 amino acids that is processed in the producing cells to render a morphogen made of a C-terminal peptide—which could consist of five, six or eight amino acids—that is transferred to neighboring cells inhibiting their differentiation Yoon and Golden , ; Corrales-Guerrero, Flores and Herrero ; Hu et al.
Indeed, a gradient of PatS has been detected in cells that flank producing cells, with the amount of the morphogen decreasing with distance Corrales-Guerrero, Flores and Herrero In Anabaena inactivation of the hetN gene, which is expressed in the heterocysts, also leads to a Mch phenotype, although this phenotype is delayed with regard to that produced by patS inactivation Black and Wolk ; Higa et al.
The hetN gene encodes a protein that includes an internal ERGSGR peptide that is identical to the C-terminal hexapeptide of PatS, and could also generate an intercellular signal that would affect heterocyst differentiation negatively, involving the residues in common with PatS Higa et al.
In addition, in Anabaena , a peptide of 84 amino acids, PatC, has been reported to act in long-range maintenance of the heterocyst pattern Corrales-Guerrero, Flores and Herrero a. However, the possible intercellular movement of this peptide has not been studied yet. Besides regulation at the level of gene expression, the HetR transcription factor is subject to post-transcriptional regulation.
HetR can be phosphorylated with a negative impact of phosphorylation on the accumulation of HetR tetramers, which could represent the transcriptionally active form of HetR Valladares, Flores and Herrero On the other hand, regulation of the turnover of HetR has been reported, with several factors including HetF, a predicted protease, and PatA, with similarity to the CheY response regulator Risser and Callahan , as well as PatS and HetN, participating in this regulation. Indeed, negative regulation of the HetR protein levels by PatS and HetN has been suggested to determine gradients of HetR along the filament with concentrations increasing away from heterocysts Risser and Callahan In both developing and fully differentiated filaments of heterocyst-forming cyanobacteria, an exchange of substances, including nutrients and regulators, takes place, as will be detailed below.
These exchanges are crucial for differentiation and nutrition in the diazotrophic filament. However, intercellular communication likely occurs also in the undifferentiated filament of heterocyst formers as evidenced by the correlation of gene expression fluctuations between nearby cells Corrales-Guerrero et al. As an example, motility of filamentous cyanobacteria on surfaces, which is important to find favorable light and nutritional conditions, and motility of hormogonia, which is needed to establish symbiotic associations with plants, have been considered to involve the coordinated activity of molecular motors in the different cells of a filament, likely requiring cell-to-cell communication Khayatan, Meeks and Risser ; Wilde and Mullineaux The structural information discussed in previous sections suggests two possible pathways for intercellular molecular exchange in the cyanobacterial filaments: the continuous periplasm and direct cell—cell joining structures.
The question of whether a structurally continuous periplasm is also functionally continuous was addressed in Anabaena by expressing a periplasmic GFP in developing heterocysts. The GFP molecular mass, 27 kDa could be observed in the periphery of cells away from the producing cell but, importantly, a GFP engineered to be anchored to the cytoplasmic membrane remained exclusively in the producing cell Mariscal, Herrero and Flores ; Flores and Herrero Fig. These results imply that the GFP diffuses along the filament's periplasm, corroborating that the periplasm can be functionally continuous.
However, the GFP is not evenly distributed along the filament suggesting that barriers, likely corresponding to the peptidoglycan mesh, exist Mariscal, Herrero and Flores The possible presence of barriers has been emphasized by Zhang et al. In the case of GFP, the use of a heterologous targeting signal by Zhang et al.
In any case, contrasting results from different laboratories could arise from different growth conditions, which may result in peptidoglycan with a more relaxed or stretched structure Vollmer and Seligman However, there is agreement that the peptidoglycan mesh is unlikely to be an effective barrier for small molecules including metabolites Mariscal, Herrero and Flores ; Zhang et al. Functionally continuous periplasm in Anabaena. Overlay of cyanobacterial autofluorescence red and GFP fluorescence green is shown.
Cells producing the GFP are indicated by arrows. For communication through the periplasm, specific cytoplasmic membrane transporters exporters and importers for substances exchanged intercellularly should be present in vegetative cells and heterocysts.
Many transporters are present in the cytoplasmic membrane of a cyanobacterium such as Anabaena Hahn and Schleiff , including transporters for amino acids, oxoacids and sucrose Nicolaisen et al. If the periplasm were a significant communication conduit between cells, the outer membrane of heterocyst-forming cyanobacteria would be expected to be an effective barrier for intercellularly exchanged substances.
Indeed, mutants of some outer membrane components of Anabaena exhibit increased permeability for sucrose and glutamate, implying that the outer membrane represents a permeability barrier for these metabolites Nicolaisen et al. This feature could contribute to retention in the periplasm of the transferred metabolites, hampering their leakage to the external medium.
Although the outer membrane proteome of Anabaena includes some porins, these proteins are now known to have size- and charge-based selectivity, and porins through which intercellularly exchanged metabolites could be lost from the filament may be absent Hahn and Schleiff These reflections are consistent with the idea that the periplasm could be a communication conduit in the filament Flores et al.
Here we describe recent advances in the understanding of direct cell-to-cell communication in the filaments. A major contribution to this topic was the introduction of fluorescent probes to test intercellular molecular exchange Mullineaux et al.
The fluorescein derivatives calcein and 5-carboxyfluorescein 5-CF are provided to the filaments as acetoxymethyl ester derivatives that are hydrophobic and readily permeate into the cells, where they are hydrolyzed by cytoplasmic esterases producing fluorescent, hydrophilic substances. Because calcein and 5-CF are retained within the cells, fluorescence recovery after photobleaching FRAP experiments can then be performed Mullineaux et al.
In these experiments, the fluorescence of a given cell is bleached and its recovery is quantified over time, normally for less than 1 min. Importantly, the fluorescence recovered in the bleached cell corresponds to fluorescence lost from neighboring cells, indicating that recovery results from intercellular movement of the probe Mullineaux et al.
Additionally, movement always takes place down the concentration gradient of the fluorescent probe, which is indicative of diffusion. This in turn suggests the presence of communication conduits between the cells in the filament. Calcein Da and 5-CF Da are negatively charged molecules that represent artificial probes. Intercellular transfer of fluorescent tracers in Anabaena sepJ and fraC fraD mutants.
The recovery rate constant R for the transfer of the indicated tracers between vegetative cells of nitrate-grown filaments is represented as a percentage of the wild-type values for sepJ , fraC fraD and sepJ fraC fraD mutants. Finally, a sepJ fraC fraD mutant still shows substantial activity of intercellular transfer of probes Fig. Hence, a pathway or mechanism of intercellular molecular exchange independent of SepJ and the Fra proteins may additionally exist. Thus, the pathway s through which physiological substrates, including nutrients and regulators, are exchanged between cells in the filament await identification.
Nonetheless, significant information regarding regulators is being gained see below. In this section, we have covered information indicating that both the continuous periplasm and cell—cell joining complexes could be involved in intercellular molecular exchange in the filaments of heterocyst-forming cyanobacteria. A unifying hypothesis is that septal junctions are main mediators of cell—cell communication, and that material including metabolites and regulators leaked from the septal junctions is retained in the periplasm, from where it can then be recovered by the cells using cytoplasmic membrane transporters.
In the filament of heterocyst-forming cyanobacteria, intercellular molecular exchange and communication is of particular importance during diazotrophic growth, when different physiological and metabolic processes are compartmentalized in different cell types.
This compartmentalization imposes a requirement for the intercellular exchange of metabolic substances and the transfer of regulatory factors.
In addition to the intercellular exchange of fluorescent probes, solid support for the intercellular exchange of metabolites is available. Support came from the cell-specific localization of different enzymes of anabolic or catabolic pathways related to carbon and nitrogen utilization in either vegetative cells or heterocysts.
First, the system for N 2 fixation operating in oxic environments, including the Mo—nitrogenase complex Peterson and Wolk ; Bergman, Lindblad and Rai ; Elhai and Wolk and auxiliary proteins such as those of pathways for the provision of reductant and protection of nitrogenase from oxygen Masepohl et al. This implies that products of N 2 fixation generated in heterocysts are transferred to vegetative cells Wolk et al.
The ammonium resulting from N 2 reduction by nitrogenase is incorporated into carbon skeletons, mainly through the glutamine synthetase GS —glutamate synthase GOGAT pathway Wolk et al. Heterocysts contain high amounts of GS, but lack glutamate synthase Thomas et al. Thus glutamate, the substrate for ammonium incorporation by GS, should be provided to heterocysts by vegetative cells.
The glutamine produced by GS in heterocysts is to some extent conveyed to the vegetative cells, where it is converted to glutamate, from which nitrogen is distributed to most nitrogen-containing cellular compounds.
Indeed, isolated heterocysts have been shown to produce glutamine when supplemented with appropriate substrates Thomas et al. In addition, a part of the organic nitrogen produced in heterocysts is transiently incorporated into the reservoir polymer cyanophycin, which, as described earlier, is conspicuously accumulated at the heterocyst polar regions Fig.
Whereas cyanophycinase is much more abundant in heterocysts than in vegetative cells Gupta and Carr ; Picossi et al. Compartmentalization extends to arginine catabolism proteins, since agmatinase, and hence the arginine decarboxylase pathway, has been shown to be present at higher levels in vegetative cells than in heterocysts Burnat and Flores Hence, heterocysts acquire reduced carbon compounds from vegetative cells to serve as a source of reductant and energy. Lechno-Yossef, C.
Wolk and E. Flores, unpublished. Mutants of these transporters are impaired in diazotrophic growth, raising the possibility of a role in the intercellular transfer of sucrose.
Furthermore, studies on the substrate, cell specificity and mutant phenotypes of amino acid transporters located in the cytoplasmic membrane have suggested the possible participation of some of these transporters in the diazotrophic growth of Anabaena.
The ABC transporter N-I for hydrophobic amino acids and Gln is required for optimal diazotrophic growth and is specifically expressed in vegetative cells Picossi et al. The ABC transporter N-II for acidic and neutral polar amino acids, including Gln, is expressed in both vegetative cells and heterocysts and is also required for optimal diazotrophic growth Pernil et al. A possible role of sucrose and amino acid transporters in diazotrophic growth would imply a step of substrate localization in the periplasm during intercellular transfer.
Whether this is an obligatory step in the transfer or, as considered above, a result of metabolite leakage from septal junctions is unknown. Clearly, more studies are necessary to elucidate the pathways for intercellular exchange of carbon and nitrogen in the diazotrophic filament, as well as the role that membrane transporters may play in those pathways. In addition to the intercellular transfer of metabolites, the development of the diazotrophic filament of heterocyst-forming cyanobacteria involves movement of signaling molecules for the establishment and maintenance of a spatial pattern of heterocysts.
Several recent reports have dealt with the molecular actors that could participate in the intercellular movement of compounds that regulate heterocyst distribution along a filament. The HetC protein, which is homologous to ABC exporters, is required for heterocyst differentiation and is localized to membranes in the heterocyst poles Khudyakov and Wolk ; Corrales-Guerrero, Flores and Herrero a.
Besides the transport domain, HetC includes a putative peptidase domain whose deletion severely impairs differentiation Corrales-Guerrero, Flores and Herrero a. Epistasis analysis of the effects of inactivation or deletion of hetC and the genes patS and hetN encoding signaling molecules is consistent with a role of HetC in the processing and export of the PatS morphogen from heterocysts Corrales-Guerrero, Flores and Herrero a.
However, this may not be the only function of HetC. It is noteworthy that the requirement for HetC can be fully compensated by moderate over-expression of HetP. The involvement of HetC in the transfer of PatS and HetN has also been studied through their effects on degradation of the HetR transcription factor along a filament of cells Videau et al.
The reporter used in this study was a form of HetR with reduced activity fused to cyan fluorescent protein CFP , introduced in all the cells of the filament in a plasmid that also expressed yellow fluorescent protein YFP from the patS gene promoter used to detect prospective heterocysts that would express patS and hetN from their native loci.
It was observed that the spatial range of HetR—CFP fluorescence loss was reduced to zero in hetC , hetC patS , and hetC hetN genetic backgrounds at times when morphological signals of differentiation were observed for each strain. An involvement of HetC in the transfer of PatS and HetN from heterocysts to the neighboring vegetative cells was deduced. It was found that correlations in expression extend to about two to three cells under nitrogen-replete conditions and that this length scale does not appreciably vary at early times after nitrogen deprivation.
Furthermore, evidence was provided supporting the notion that these correlations are due primarily to cell—cell communication and not only to cell division effects. In addition to the wild type, fluctuations in the expression of hetR—gfp were studied in mutant backgrounds, and focus was placed on the involvement of putative septal junction proteins in the transfer of PatS and HetN. As mentioned above, these regulators seem to act on HetR, which additionally is autoregulated.
Thus, the fact that the coupling of correlations of the expression of hetR—gfp between cells along the filament, both in the presence of ammonium and at early times upon N step-down, was increased with regard to the wild type by deletion of patS , but decreased by deletion of sepJ , suggests a functional relationship between their products, PatS and SepJ, and could be explained by PatS being transferred through SepJ-dependent conduits Corrales-Guerrero et al.
At early times after nitrogen deprivation, the behavior of a hetN mutant or of a fraC fraD mutant was similar to that of the wild type.
The movement of PatS and HetN-derived inhibitors has also been studied in genetic mosaics built in Anabaena filaments Rivers, Videau and Callahan The constructs were generated by randomly introducing plasmids encoding the genes yfp and hetN or patS expressed from heterologous inducible promoters in some cells source cells of a parental strain with deleted patA and hetF genes, in which the HetR turnover is decreased.
Also in this case, the loss of fluorescence from CFP in cells away from source cells was used to estimate the range of the inhibitory signal. The signal range of HetN, but not of PatS, was found to be shortened by inactivation of sepJ , which was taken to suggest an involvement of SepJ in the intercellular transfer of a HetN-derived signal Rivers, Videau and Callahan Because sepJ deletion mutants conspicuously fragment under nitrogen deprivation and arrest heterocyst differentiation at an early stage, it has not been possible to study export from heterocysts in those mutants.
However, the pattern of heterocyst differentiation was studied in strains overexpressing sepJ in combination to patS or hetN deletions Mariscal et al. In the wild-type background, over-expression of sepJ decreased the number of heterocysts and increased the size of vegetative-cell intervals between heterocysts, whereas the patS deletion was epistatic over sepJ overexpression.
These results are consistent with an increased transfer of PatS and of a HetN-derived signal between vegetative cells involving SepJ. In summary, indications have been obtained for the involvement of the ABC exporter HetC on the transfer of the PatS morphogen and of a HetN-derived signal from the heterocysts to the vegetative cells, and of SepJ in the transfer of those regulators, at least between vegetative cells. However, direct characterization of the transport processes is a task for future research.
A scheme of the compartmentalization of enzymes, transporters, metabolites and regulators relevant for multicellularity in Anabaena , as discussed above, is presented in Fig. Scheme of part of a filament of Anabaena showing one heterocyst and adjacent vegetative cells and highlighting enzymes, transporters, metabolites and regulators thought to be involved in the multicellular physiology of this cyanobacterium.
Various analytical, numerical and computational approaches have been used to model developmental pattern formation in filamentous cyanobacteria. The necessity for models to capture essential features and mechanisms, and yet to remain tractable, forces the choice of as few as possible dynamical variables and unknown parameters Economou and Green ; Kirk, Babtie and Stumpf An early scheme aiming at describing the pattern of near regular intervals of vegetative cells separating consecutive heterocysts was formulated before any identification of specific genes in Anabaena was made Wilcox, Mitchison and Smith This scheme was based on the original insight of Fogg, who proposed that the diffusion of an inhibitory substance produced by heterocysts is responsible for this regularity Fogg According to this scheme, a substance X whose concentration specifies the state of development of a cell towards a heterocyst state promotes its own synthesis and that of its inhibitor Y.
In contrast to the diffusing inhibitor Y, X does not diffuse. It was further assumed that the inhibitor produced in heterocysts was destroyed in vegetative cells, setting up a gradient around heterocysts, and that when Y drops below a threshold level, development in a group of vegetative cells begins. Asymmetrical cell division and competitive interactions in this group prevent the formation of more than one heterocyst.
The scheme was proposed for its plausibility but not framed mathematically, so no quantitative comparisons with experimental data were made, in spite of its intuitive appeal.
Evidence that heterocysts inhibit the differentiation of vegetative cells in their vicinity was provided by Wolk , who made a statistical study of the formation of new heterocysts in fragmented filaments. Further support for the notion that heterocysts act as sources of a diffusible inhibitory substance rather than as sinks was provided by Wolk and Quine , who constructed one-dimensional tessellations commonly used to study crystal growth processes to model the distribution of interval lengths between heterocysts, both analytically and by computer simulations.
These tessellations consisted of spatial domains that grew out of nuclei generated stochastically both in space and time, until they touched. The lengths between interval centers played the role of inter-heterocyst intervals, and different domain growth mechanisms corresponded to different mechanisms for the propagation of the inhibitor along a filament. They found that model distributions approximated experimentally measured ones when the inhibitor moves along a filament by diffusion.
Here f and g , the reaction terms, are non-linear functions of u and v , and D u and D v the respective diffusion coefficients. A linear stability analysis shows that the homogeneous state may become unstable against the formation of stationary spatial patterns, when one of the species acts as an activator and the other as an inhibitor, and when the diffusion constant of the inhibitory chemical largely exceeds that of the activator Turing ; Segel and Jackson the precise condition is cast in terms of the diffusion lengths of both chemicals.
Many patterns can arise for the same value of model parameters and the pattern that actually appears is sensitively dependent on initial conditions and fine tuning of parameters Levin and Segel ; Mimura and Murray ; Castets et al.
Importantly, the characteristic length scale of the spatial patterns is intrinsic and independent of the size of the domain over which the equations are defined, like developmental patterns in filamentous cyanobacteria.
In spite of various commonalities, there are substantial differences between Turing's instability and the formation of developmental patterns in cyanobacteria, which we now discuss. The Turing instability requires diffusion of both the activator and the inhibitor species, with large differences in the two diffusivities. In fact, it can be shown mathematically that the instability cannot appear in any two-component reaction—diffusion model in which only one of the two species diffuses Ermentrout and Lewis ; Cantini et al.
Of note, no evidence for diffusion of the activator HetR between cells has been reported. It has been shown in recent years that stochastic Turing patterns may arise when only one species undergoes diffusion, provided that the discreteness of molecular species, dubbed intrinsic or demographic noise, is significant Butler and Goldenfeld , ; Biancalani, Fanelli and Di Patti ; Woolley et al.
However, these patterns are transient and fluctuating in time, whereas patterns in cyanobacteria are not: once the commitment point to differentiation has been crossed, at circa 8 h after nitrogen deprivation under laboratory conditions see, e. Yoon and Golden , heterocysts are terminally formed.
The equations for the Turing model are defined on a continuum spatial support of fixed size, whereas cyanobacterial developmental patterns are intrinsically discrete and filaments continually grow by cell growth and division.
The typical length scale of developmental patterns in cyanobacteria is only of the order of 10 cells Haselkorn , far from any continuum approximation. Moreover, the typical time scale for differentiation of a heterocyst is comparable to that of cell division of vegetative cells in growing filaments, under naturalistic conditions.
Filament growth through cell division may lead to non-trivial effects beyond dilution, such as an increase in intrinsic noise due to unequal binomial partition of molecular species that are present in small numbers upon cell division Swain, Elowitz and Siggia Lastly, patterns in cyanobacteria are quite robust, in contrast to the fine tuning of parameters required to observe a Turing instability. Given these differences, claims as to the adequacy of the two-component Turing model to describe development in filamentous cyanobacteria see, e.
Hu et al. Following Turing's original use of reaction—diffusion systems, numerous studies based on the same formalism have been proposed, which we now survey. Meinhardt and Gierer demonstrated pattern formation for specific reaction—diffusion equations involving diffusion of both activator and inhibitor substances, and whose reaction terms included autocatalysis of the activator Gierer and Meinhardt ; Meinhardt No identification of activator or inhibitor substances with specific genes or metabolites in cyanobacteria was made, and only a qualitative comparison between the patterns obtained from the equations and those observed in experiments was carried out.
Extension of Meinhardt and Gierer's model to a growing domain, in order to account for filament growth through cell division and the discrete nature of cyanobacterial filaments, was carried out using Lindenmayer or L-systems Hammel and Prusinkewicz ; Coen et al. Originally designed to simulate plant and fractal growth Lindenmayer , L-systems comprise recursive algorithms in which the state of a system is replaced in parallel by the next state using a set of predefined rules, as opposed to a sequential process.
Pattern formation similar to that observed in experiments was generated by this scheme, though no quantitative comparison with experiment was attempted. In contrast to de novo developmental patterns that necessarily arise from fluctuations in gene expression between cells in undifferentiated filaments, the problem of pattern maintenance is different. New heterocysts must form against the backdrop of morphogen gradients, and positional information as envisioned by Wolpert must be interpreted Wolpert A model of pattern maintenance has been proposed by Zhu, Callahan and Allen , who incorporated the effects of the HetR inhibitor HetN, in addition to the effects of PatS.
In their model, the concentration of HetN is high at heterocysts, and it diffuses to neighboring cells, forming a bowl-shaped profile between neighbor heterocysts. When HetN levels in the middle region decrease sufficiently through vegetative cell division, HetR accumulation is promoted, triggering in turn local PatS production and inhibiting the increase of HetR levels in nearby cells. To reproduce pattern maintenance as observed in experiments, the model requires that diffusion of either HetN or a HetN-derived signal is small enough relative to filament growth that levels near the middle of vegetative-cell intervals can drop to allow for HetR levels to grow.
In addition, the model included external noise of the same amplitude in all the dynamical equations. Unified Model of Chromatophore and Chloroplast Formation Imagine a proto-algal cell living in seawater, in which the concentration of inorganic phosphate is very low.
Figure 5. Additional Notes on the Models 6. Multiple Gene Transfers from Cyanobacteria and Other Bacteria For simplicity, the models in Figure 4 and Figure 5 are drawn with a minimal number of arrows that indicate gene transfers to the chloroplast.
Eukaryotic Nature of Chloroplast Envelope Microscopic observation of a plant or algal cell gives us an impression that chloroplast is a single entity, namely, a package of thylakoid membranes wrapped with envelope membranes. Conclusions: Flexible Views on the Origin The present article focuses on the phylogenetic origin of the similarity of cyanobacteria and chloroplasts.
Table 2 The similarity of chloroplasts and cyanobacteria turned out to be explained by different mechanisms. Click here for additional data file. Institutional Review Board Statement Not applicable. Informed Consent Statement Not applicable. Data Availability Statement Data are available from related publications and supplements.
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