Relationships between the ABC-Exporter HetC and Peptides that Regulate the Spatiotemporal Pattern of Heterocyst Distribution in Anabaena

Corrales-Guerrero, Laura; Flores, Enrique; Herrero, Antonia

doi:10.1371/journal.pone.0104571

Cited by 26 publications

(63 citation statements)

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“…In other words, inactivation of patS or hetN would be expected to restore heterocyst function in a hetC background and yield a pattern of heterocysts typical of the patS or hetN single mutants. A similar epistasis analysis was recently reported (25). However, our epistasis results differ substantially, probably as a consequence of the nature of the mutations in hetC, and so are reported here.…”

Section: Deletion Of Pats or Hetn Is Epistatic To Deletion Of Hetcsupporting

confidence: 86%

“…S1 in the supplemental material). The phenotype of strain UHM232 is similar to that of the recently reported peptidase domain mutant and, unlike the early developmental role speculated for hetC based on mutants that have been reported to make small dividing proheterocyst-like cells (22), no small cells were observed in this or the previous work (25). The nonpolar nature of the mutations in these two strains suggests that they represent the true hetC-null phenotype.…”

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystssupporting

confidence: 78%

“…A lack of inhibitor export could result in inhibition of differentiation of these source cells rather than inhibitor export to, and inhibition of, neighboring cells, as occurs in the wild type (24). The findings of a recent epistasis analysis with hetC and patS null mutants were consistent with this hypothesis (25).…”

mentioning

confidence: 66%

“…Strains of Anabaena with an otherwise wild-type genetic background that have hetC inactivated with the incorporation of foreign DNA, either a transposon or an omega interposon, do not make heterocysts (21,25). However, a strain with the predicted peptidase domain cleanly deleted differentiates a reduced number of heterocysts that are inactive (25).…”

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystsmentioning

confidence: 99%

“…However, a strain with the predicted peptidase domain cleanly deleted differentiates a reduced number of heterocysts that are inactive (25). In the former case, the mutation has the potential to be polar, and in the latter, only one domain of the protein is removed.…”

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystsmentioning

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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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: Deletion Of Pats or Hetn Is Epistatic To Deletion Of Hetcsupporting

confidence: 86%

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystssupporting

confidence: 78%

mentioning

confidence: 66%

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystsmentioning

confidence: 99%

Section: A Hetc Mutant Forms Morphologically Distinct Heterocystsmentioning

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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Cyanobacterial Heterocysts

Muro‐Pastor

Maldener

2019

Encyclopedia of Life Sciences

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Cyanobacteria are phototrophic bacteria carrying out oxygen‐producing photosynthesis. Besides showing the capability of building their cellular carbon from carbon dioxide (CO 2 ), available in the atmosphere, several strains of cyanobacteria have also acquired the ability to fix molecular dinitrogen (N 2 ), a ubiquitous source of nitrogen. As the enzyme responsible for nitrogen fixation (nitrogenase) is highly sensitive to oxygen, nitrogen fixation and oxygenic photosynthesis cannot take place simultaneously in cyanobacterial cells. To solve this problem, some filamentous strains are able to restrict N 2 fixation to a specialised cell type, the heterocyst. Heterocysts are morphologically distinct, terminally differentiated cells that develop, in the absence of alternative sources of combined nitrogen, mostly in a semiregular pattern along the filaments. Thus, a filament containing heterocysts provides division of labour between vegetative cells (photosynthetic CO 2 fixation) and heterocysts (anaerobic N 2 fixation). These cyanobacteria represent true multicellular organisms with profound morphological cell differentiation and sophisticated intercellular communication systems, ultimately orchestrated by complex gene expression patterns. Key Concepts Although bacteria, some filamentous cyanobacteria are true multicellular organisms, showing different cell types performing specialised tasks. When lacking a source of combined nitrogen, these cyanobacteria start a program of cell differentiation resulting in a pattern of semiregularly spaced heterocysts along the filament. Heterocysts differentiate from vegetative cells, which carry out oxygenic photosynthesis, and provide a microoxic environment for the activity of oxygen‐labile nitrogenase. Nitrogenase is the enzyme responsible for N 2 fixation and allows the organism to live from sunlight, air (CO 2 and N 2 ) and some minerals. The two cell types rely on each other and exchange metabolites and signalling molecules, via septal junctions mediating cell‐to‐cell contact. Two transcription factors, HetR and NtcA, regulate the changes in gene expression during heterocyst differentiation. The pattern of spaced heterocysts is regulated by inhibitor gradients that promote the decay of HetR, confirming mathematical models of two‐dimensional pattern formation in heterocystous cyanobacteria.

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Molecular circuit of heterocyst differentiation in cyanobacteria

Harish

Seth²

2020

J Basic Microbiol

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Differentiation commitment is one of the most complex mechanisms to study in biological science. One of the model systems used for understanding differentiation complexity is heterocyst development in cyanobacteria. Cyanobacteria have the capability of biological nitrogen fixation due to highly differentiated heterocyst cells. Once the nitrogen deficiency signal is perceived by the cyanobacteria, few of its vegetative cells commit toward the development of heterocyst. Heterocyst provides a microoxic environment that is essential for the nitrogenase complex to fix the atmospheric dinitrogen. The entire process of development of heterocyst can be divided into different steps, such as (a) sensing signal and differentiation induction, (b) positional (pattern) determination of heterocyst in the filament, (c) formation of extracellular thick heterocyst‐specific layers, and (d) assembly of nitrogen‐fixing machinery. Many of the key regulators that are essential for heterocyst formation in these different steps have been identified. Recently, the role of small RNA and interruption DNA elements that influence the heterocyst formation and function has also been identified. In this review article, we have outlined the current understanding of the entire molecular circuit of heterocyst development in a simplistic way. This article focuses on explaining key concepts related to heterocyst development and discusses recent discoveries in this line.

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Relationships between the ABC-Exporter HetC and Peptides that Regulate the Spatiotemporal Pattern of Heterocyst Distribution in Anabaena

Cited by 26 publications

References 40 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

Cyanobacterial Heterocysts

Molecular circuit of heterocyst differentiation in cyanobacteria

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