Mutation of <scp>sepJ</scp> reduces the intercellular signal range of a <scp>hetN</scp>‐dependent paracrine signal, but not of a <scp>patS</scp>‐dependent signal, in the filamentous cyanobacterium <scp>A</scp>nabaena sp. strain <scp>PCC</scp> 7120

Rivers, Orion S.; Videau, Patrick; Callahan, Sean M.

doi:10.1111/mmi.12836

Cited by 23 publications

(30 citation statements)

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“…Cells were routinely viewed and imaged as previously described (27). Confocal microscopy and determination of the signal ranges of patS-and hetN-dependent activities using ImageJ were conducted as previously described (12), and EcFbFP was imaged as described previously (36). Heterocyst-specific exopolysaccharides were stained with alcian blue as previously described (28).…”

Section: Methodsmentioning

confidence: 99%

“…A fluorescent form of HetR produced in all cells acts as an indicator of patS-and/or hetN-encoded signal activity adjacent to source cells because each of the signals independently promotes degradation of HetR with a concomitant decrease in fluorescence. This system was recently used to show that the number of vegetative cells affected by the hetN paracrine signal, the signal range, was reduced in strains lacking SepJ, a channel-forming protein that facilitates intercytoplasmic communication between adjacent cells (12). Channels connecting the cells of Anabaena filaments were recently visualized by electron tomography, but the composition of these channels is unknown (26).…”

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confidence: 99%

“…In addition to regulating the transcription of a large number of morphogenesis and metabolism genes, HetR positively autoregulates its own production and is necessary for induction of transcription of patS and hetN (16)(17)(18). The full-length 17-amino-acid (17-aa) patS-encoded peptides and 287-aa hetN-encoded peptides do not appear to move from cell to cell, and the presumed fragments that do are unknown (3,12). However, experimental evidence suggests a Cterminal 5-, 6-, or 8-aa peptide cleavage product in the case of patS (3,13,19).…”

mentioning

confidence: 99%

“…The patS and hetN genes encode developmental signals that have many of the characteristics of morphogens (3,7,12). These signals move from source cells to neighboring vegetative cells to prevent their differentiation (3,7,13,14).…”

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confidence: 99%

“…Two approaches for detection of the patS-and hetN-encoded signals have recently been described; an antibody directed against the RGSGR peptide motif has been used to visualize the patSencoded signal in cells adjacent to heterocysts (3), and patS/hetNdependent degradation of HetR has been used to examine signal activity in cells adjacent to source cells producing the patS-and/or hetN-encoded signal (5,12). In the latter approach, source cells can be genetically engineered to produce one of the signals or can be vegetative cells or heterocysts in which transcription of patS or hetN or both has been induced by removal of combined nitrogen.…”

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ABC Transporter Required for Intercellular Transfer of Developmental Signals in a Heterocystous Cyanobacterium

et al. 2015

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In the filamentous cyanobacterium Anabaena, patS and hetN encode peptide-derived signals with many of the properties of morphogens. These signals regulate the formation of a periodic pattern of heterocysts by lateral inhibition of differentiation. Here we show that intercellular transfer of the patS-and hetN-dependent developmental signals from heterocysts to vegetative cells requires HetC, a predicted ATP-binding cassette transporter (ABC transporter). Relative to the wild type, in a hetC mutant differentiation resulted in a reduced number of heterocysts that were incapable of nitrogen fixation, but deletion of patS or hetN restored heterocyst number and function in a hetC background. These epistasis results suggest that HetC is necessary for conferring self-immunity to the inhibitors on differentiating cells. Nine hours after induction of differentiation, HetC was required for neither induction of transcription of patS nor intercellular transfer of the patS-encoded signal to neighboring cells. Conversely, in strains lacking HetC, the patS-and hetN-encoded signals were not transferred from heterocyst cells to adjacent vegetative cells. The results support a model in which the patS-dependent signal is initially transferred between vegetative cells in a HetCindependent fashion, but some time before morphological differentiation of heterocysts is complete, transfer of both signals transitions to a HetC-dependent process. IMPORTANCEHow chemical cues that regulate pattern formation in multicellular organisms move from one cell to another is a central question in developmental biology. In this study, we show that an ABC transporter, HetC, is necessary for transport of two developmental signals between different types of cells in a filamentous cyanobacterium. ABC transporters are found in organisms as diverse as bacteria and humans and, as the name implies, are often involved in the transport of molecules across a cellular membrane. The activity of HetC was shown to be required for signaling between heterocysts, which supply fixed nitrogen to the organism, and other cells, as well as for conferring immunity to self-signaling on developing heterocysts. Differentiation of heterocysts by filamentous cyanobacteria represents a simple but elegant model of biological patterning. In response to a shortage of combined nitrogen, linear filaments of Anabaena sp. strain PCC 7120 (here, Anabaena) form a periodic pattern of single, terminally differentiated, nitrogen-fixing heterocysts separated by approximately 10 totipotent vegetative cells. The spacing between heterocysts reflects the metabolic interdependence of the two cell types; fixed nitrogen is supplied to vegetative cells from heterocysts, and in return, heterocysts receive a source of carbon and reductant to compensate for their lack of photosystem II and the Calvin cycle (for a review of heterocyst differentiation, see reference 1). As filaments lengthen by growth and division of vegetative cells, subsequent rounds of heterocyst differentiation place new hetero...

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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ABC Transporter Required for Intercellular Transfer of Developmental Signals in a Heterocystous Cyanobacterium

et al. 2015

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Impaired cell-cell communication in the multicellular cyanobacterium Anabaena affects carbon uptake, photosynthesis, and the cell wall

et al. 2021

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Mathematical study of pattern formation accompanied by heterocyst differentiation in multicellular cyanobacterium

Ishihara

Tachikawa

Iwasaki

2015

Journal of Theoretical Biology

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The filamentous cyanobacterium, Anabaena sp. PCC 7120, is one of the simplest models of a multicellular system showing cellular differentiation. In nitrogen-deprived culture, undifferentiated vegetative cells differentiate into heterocysts at ~10-cell intervals along the cellular filament. As undifferentiated cells divide, the number of cells between heterocysts (segment length) increases, and a new heterocyst appears in the intermediate region. To understand how the heterocyst pattern is formed and maintained, we constructed a one-dimensional cellular automaton (CA) model of the heterocyst pattern formation. The dynamics of vegetative cells is modeled by a stochastic transition process including cell division, differentiation and increase of cell age (maturation). Cell division and differentiation depend on the time elapsed after the last cell division, the "cell age". The model dynamics was mathematically analyzed by a two-step Markov approximation. In the first step, we determined steady state of cell age distribution among vegetative cell population. In the second step, we determined steady state distribution of segment length among segment population. The analytical solution was consistent with the results of numerical simulations. We then compared the analytical solution with the experimental data, and quantitatively estimated the immeasurable intercellular kinetics. We found that differentiation is initially independent of cellular maturation, but becomes dependent on maturation as the pattern formation evolves. Our mathematical model and analysis enabled us to quantify the internal cellular dynamics at various stages of the heterocyst pattern formation.

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Mutation of sepJ reduces the intercellular signal range of a hetN‐dependent paracrine signal, but not of a patS‐dependent signal, in the filamentous cyanobacterium Anabaena sp. strain PCC 7120

Cited by 23 publications

References 41 publications

ABC Transporter Required for Intercellular Transfer of Developmental Signals in a Heterocystous Cyanobacterium

ABC Transporter Required for Intercellular Transfer of Developmental Signals in a Heterocystous Cyanobacterium

Impaired cell-cell communication in the multicellular cyanobacterium Anabaena affects carbon uptake, photosynthesis, and the cell wall

Mathematical study of pattern formation accompanied by heterocyst differentiation in multicellular cyanobacterium

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