Special Issue "Developmental Biology in Cyanobacteria"

A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Life Sciences".

Deadline for manuscript submissions: closed (30 September 2018)

Special Issue Editors

Guest Editor
Prof. Dr. Antonia Herrero Moreno

Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas, Universidad de Sevilla, Seville, Spain
Website | E-Mail
Interests: transcriptional regulation; NtcA transcription factor; bacterial cell differentiation; membrane transport; intercellular communication
Guest Editor
Prof. Dr. Enrique Flores García

Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas, Universidad de Sevilla, Seville, Spain
Website | E-Mail
Interests: transcriptional regulation; NtcA transcription factor; bacterial cell differentiation; membrane transport; intercellular communication

Special Issue Information

Dear Colleagues,

Filamentous, heterocyst-forming cyanobacteria constitute a genuine example of bacterial multicellularity. During cell division, the resulting daughter cells do not separate as in unicellular bacteria, but they remain bound by an unsplit outer membrane, which determines the presence of a continuous shared periplasm, and by proteinaceous structures—Septal juntions—that in addition to adhesion provide conduits for intercellular exchange of metabolites and regulatory molecules. Additionally, these cyanobacteria can undertake different developmental paths in response to diverse environmental cues. One of them is the differentiation of some cells of the filament into heterocysts, cells specialized in the fixation of atmospheric nitrogen, that takes place under conditions of nitrogen scarcity.

Heterocyst differentiation involves multiple morphological and biochemical changes to allow the efficient operation of the nitrogenase complex, including the provision of reducing equivalents and energy and the conformation of a micro-oxic cytoplasm. All these cellular changes result from an extensive program of gene expression regulation, which remarkably exhibits a precise spatiotemporal specificity. Indeed, heterocysts are semiregularly distributed, frequently occurring separated by stretches of ca. 10 to 15 vegetative cells along the filament, as found in the model strain Anabaena sp. PCC 7120. Because the heterocysts donate fixed nitrogen to the vegetative cells, whereas these perform the photosynthetic fixation of CO2 and provide the heterocysts with reduced carbon, the cyanobacterial diazotrophic filament fulfill the ultimate feature of multicellular organisms, namely the division of labor between different cell types.

This Special Issue of Life includes review and original research articles dealing with the complexity of heterocyst-forming cyanobacteria, gene expression regulation during heterocyst differentiation, heterocyst patterning and intercellular communication.

Prof. Dr. Antonia Herrero Moreno
Prof. Dr. Enrique Flores García
Guest Editors

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Keywords

  • Anabaena
  • bacterial developmental patterns
  • cell-to-cell gene-expression noise
  • intercellular communication
  • multicellular cyanobacteria
  • nitrogen fixation
  • transcriptional regulation

Published Papers (8 papers)

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Research

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Open AccessArticle Manipulation of Pattern of Cell Differentiation in a hetR Mutant of Anabaena sp. PCC 7120 by Overexpressing hetZ Alone or with hetP
Received: 2 October 2018 / Revised: 23 November 2018 / Accepted: 27 November 2018 / Published: 30 November 2018
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Abstract
In the filamentous cyanobacterium, Anabaena sp. PCC 7120, single heterocysts differentiate at semi-regular intervals in response to nitrogen stepdown. HetR is a principal regulator of heterocyst differentiation, and hetP and hetZ are two genes that are regulated directly by HetR. In a hetR [...] Read more.
In the filamentous cyanobacterium, Anabaena sp. PCC 7120, single heterocysts differentiate at semi-regular intervals in response to nitrogen stepdown. HetR is a principal regulator of heterocyst differentiation, and hetP and hetZ are two genes that are regulated directly by HetR. In a hetR mutant generated from the IHB (Institute of Hydrobiology) substrain of PCC 7120, heterocyst formation can be restored by moderate expression of hetZ and hetP. The resulting heterocysts are located at terminal positions. We used a tandem promoter, PrbcLPpetE, to express hetZ and hetP strongly in the hetR mutant. Co-expression of hetZ and hetP enabled the hetR mutant to form multiple contiguous heterocysts at both terminal and intercalary positions. Expression of hetZ, alone resulted in terminally located heterocysts, whereas expression of hetP, alone produced enlarged cells in strings. In the absence of HetR, formation of heterocysts was insensitive to the peptide inhibitor, RGSGR. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Open AccessCommunication Biosensors-Based In Vivo Quantification of 2-Oxoglutarate in Cyanobacteria and Proteobacteria
Received: 29 September 2018 / Revised: 24 October 2018 / Accepted: 25 October 2018 / Published: 27 October 2018
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Abstract
2-oxoglutarate (α-ketoglutarate; 2-OG) is an intermediate of the Krebs cycle, and constitutes the carbon skeleton for nitrogen assimilation and the synthesis of a variety of compounds. In addition to being an important metabolite, 2-OG is a signaling molecule with a broad regulatory repertoire [...] Read more.
2-oxoglutarate (α-ketoglutarate; 2-OG) is an intermediate of the Krebs cycle, and constitutes the carbon skeleton for nitrogen assimilation and the synthesis of a variety of compounds. In addition to being an important metabolite, 2-OG is a signaling molecule with a broad regulatory repertoire in a variety of organisms, including plants, animals, and bacteria. Although challenging, measuring the levels and variations of metabolic signals in vivo is critical to better understand how cells control specific processes. To measure cellular 2-OG concentrations and dynamics, we designed a set of biosensors based on the fluorescence resonance energy transfer (FRET) technology that can be used in vivo in different organisms. For this purpose, we took advantage of the conformational changes of two cyanobacterial proteins induced by 2-OG binding. We show that these biosensors responded immediately and specifically to different 2-OG levels, and hence allowed to measure 2-OG variations in function of environmental modifications in the proteobacterium Escherichia coli and in the cyanobacterium Anabaena sp. PCC 7120. Our results pave the way to study 2-OG dynamics at the cellular level in uni- and multi-cellular organisms. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Open AccessArticle The Ser/Thr Kinase PknH Is Essential for Maintaining Heterocyst Pattern in the Cyanobacterium Anabaena sp. Strain PCC 7120
Received: 6 July 2018 / Revised: 21 August 2018 / Accepted: 22 August 2018 / Published: 24 August 2018
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Abstract
In the filamentous cyanobacterium Anabaena sp. strain, PCC 7120, heterocysts (which are nitrogen-fixing cells) are formed in the absence of combined nitrogen in the medium. Heterocysts are separated from one another by 10 to 15 vegetative cells along the filaments, which consist of [...] Read more.
In the filamentous cyanobacterium Anabaena sp. strain, PCC 7120, heterocysts (which are nitrogen-fixing cells) are formed in the absence of combined nitrogen in the medium. Heterocysts are separated from one another by 10 to 15 vegetative cells along the filaments, which consist of a few hundred of cells. hetR is necessary for heterocyst differentiation; and patS and hetN, expressed in heterocysts, play important roles in heterocyst pattern formation by laterally inhibiting the expression of hetR in adjacent cells. The results of this study indicated that pknH, which encodes a Ser/Thr kinase, was also involved in heterocyst pattern formation. In the pknH mutant, the heterocyst pattern was normal within 24 h after nitrogen deprivation, but multiple contiguous heterocysts were formed from 24 to 48 h. A time-lapse analysis of reporter strains harboring a fusion between gfp and the hetR promoter indicated that pknH was required to suppress hetR expression in cells adjacent to the preexisting heterocysts. These results indicated that pknH was necessary for the lateral inhibition of heterocyst differentiation to maintain the heterocyst pattern. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Open AccessArticle The ABC Transporter Components HgdB and HgdC are Important for Glycolipid Layer Composition and Function of Heterocysts in Anabaena sp. PCC 7120
Received: 5 June 2018 / Revised: 21 June 2018 / Accepted: 28 June 2018 / Published: 2 July 2018
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Abstract
Anabaena sp. PCC 7120 is a filamentous cyanobacterium able to fix atmospheric nitrogen in semi-regularly spaced heterocysts. For correct heterocyst function, a special cell envelope consisting of a glycolipid layer and a polysaccharide layer is essential. We investigated the role of the genes [...] Read more.
Anabaena sp. PCC 7120 is a filamentous cyanobacterium able to fix atmospheric nitrogen in semi-regularly spaced heterocysts. For correct heterocyst function, a special cell envelope consisting of a glycolipid layer and a polysaccharide layer is essential. We investigated the role of the genes hgdB and hgdC, encoding domains of a putative ABC transporter, in heterocyst maturation. We investigated the subcellular localization of the fusion protein HgdC-GFP and followed the differential expression of the hgdB and hgdC genes during heterocyst maturation. Using a single recombination approach, we created a mutant in hgdB gene and studied its phenotype by microscopy and analytical chromatography. Although heterocysts are formed in the mutant, the structure of the glycolipid layer is aberrant and also contains an atypical ratio of the two major glycolipids. As shown by a pull-down assay, HgdB interacts with the outer membrane protein TolC, which indicates a function as a type 1 secretion system. We show that the hgdB-hgdC genes are essential for the creation of micro-oxic conditions by influencing the correct composition of the glycolipid layer for heterocyst function. Our observations confirm the significance of the hgdB-hgdC gene cluster and shed light on a novel mode of regulation of heterocyst envelope formation. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Review

Jump to: Research

Open AccessReview Metalloproteins in the Biology of Heterocysts
Received: 30 January 2019 / Revised: 18 March 2019 / Accepted: 28 March 2019 / Published: 3 April 2019
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Abstract
Cyanobacteria are photoautotrophic microorganisms present in almost all ecologically niches on Earth. They exist as single-cell or filamentous forms and the latter often contain specialized cells for N2 fixation known as heterocysts. Heterocysts arise from photosynthetic active vegetative cells by multiple morphological [...] Read more.
Cyanobacteria are photoautotrophic microorganisms present in almost all ecologically niches on Earth. They exist as single-cell or filamentous forms and the latter often contain specialized cells for N2 fixation known as heterocysts. Heterocysts arise from photosynthetic active vegetative cells by multiple morphological and physiological rearrangements including the absence of O2 evolution and CO2 fixation. The key function of this cell type is carried out by the metalloprotein complex known as nitrogenase. Additionally, many other important processes in heterocysts also depend on metalloproteins. This leads to a high metal demand exceeding the one of other bacteria in content and concentration during heterocyst development and in mature heterocysts. This review provides an overview on the current knowledge of the transition metals and metalloproteins required by heterocysts in heterocyst-forming cyanobacteria. It discusses the molecular, physiological, and physicochemical properties of metalloproteins involved in N2 fixation, H2 metabolism, electron transport chains, oxidative stress management, storage, energy metabolism, and metabolic networks in the diazotrophic filament. This provides a detailed and comprehensive picture on the heterocyst demands for Fe, Cu, Mo, Ni, Mn, V, and Zn as cofactors for metalloproteins and highlights the importance of such metalloproteins for the biology of cyanobacterial heterocysts. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
Open AccessReview Heterocyst Thylakoid Bioenergetics
Received: 9 December 2018 / Revised: 7 January 2019 / Accepted: 18 January 2019 / Published: 25 January 2019
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Abstract
Heterocysts are specialized cells that differentiate in the filaments of heterocystous cyanobacteria. Their role is to maintain a microoxic environment for the nitrogenase enzyme during diazotrophic growth. The lack of photosynthetic water oxidation in the heterocyst puts special constraints on the energetics for [...] Read more.
Heterocysts are specialized cells that differentiate in the filaments of heterocystous cyanobacteria. Their role is to maintain a microoxic environment for the nitrogenase enzyme during diazotrophic growth. The lack of photosynthetic water oxidation in the heterocyst puts special constraints on the energetics for nitrogen fixation, and the electron transport pathways of heterocyst thylakoids are slightly different from those in vegetative cells. During recent years, there has been a growing interest in utilizing heterocysts as cell factories for the production of fuels and other chemical commodities. Optimization of these production systems requires some consideration of the bioenergetics behind nitrogen fixation. In this overview, we emphasize the role of photosynthetic electron transport in providing ATP and reductants to the nitrogenase enzyme, and provide some examples where heterocysts have been used as production facilities. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Open AccessReview Cyanobacterial Septal Junctions: Properties and Regulation
Received: 12 November 2018 / Revised: 12 December 2018 / Accepted: 16 December 2018 / Published: 20 December 2018
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Abstract
Heterocyst-forming cyanobacteria are multicellular organisms that grow as chains of cells (filaments or trichomes) in which the cells exchange regulators and nutrients. In this article, we review the morphological, physiological and genetic data that have led to our current understanding of intercellular communication [...] Read more.
Heterocyst-forming cyanobacteria are multicellular organisms that grow as chains of cells (filaments or trichomes) in which the cells exchange regulators and nutrients. In this article, we review the morphological, physiological and genetic data that have led to our current understanding of intercellular communication in these organisms. Intercellular molecular exchange appears to take place by simple diffusion through proteinaceous structures, known as septal junctions, which connect the adjacent cells in the filament and traverse the septal peptidoglycan through perforations known as nanopores. Proteins that are necessary to produce, and that may be components of, the septal junctions―SepJ, FraC and FraD―have been identified in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 model. Additionally, several proteins that are necessary to produce a normal number of nanopores and functional septal junctions have been identified, including AmiC-type amidases, peptidoglycan-binding proteins and some membrane transporters. Available reports and reevaluation of intercellular molecular transfer data for some mutants of Anabaena suggest that the septal junctions can be regulated, likely by a mechanism of gating. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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Open AccessReview Noise–Seeded Developmental Pattern Formation in Filamentous Cyanobacteria
Received: 26 September 2018 / Revised: 24 October 2018 / Accepted: 5 November 2018 / Published: 9 November 2018
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Abstract
Under nitrogen-poor conditions, multicellular cyanobacteria such as Anabaena sp. PCC 7120 undergo a process of differentiation, forming nearly regular, developmental patterns of individual nitrogen-fixing cells, called heterocysts, interspersed between intervals of vegetative cells that carry out photosynthesis. Developmental pattern formation is mediated by [...] Read more.
Under nitrogen-poor conditions, multicellular cyanobacteria such as Anabaena sp. PCC 7120 undergo a process of differentiation, forming nearly regular, developmental patterns of individual nitrogen-fixing cells, called heterocysts, interspersed between intervals of vegetative cells that carry out photosynthesis. Developmental pattern formation is mediated by morphogen species that can act as activators and inhibitors, some of which can diffuse along filaments. We survey the limitations of the classical, deterministic Turing mechanism that has been often invoked to explain pattern formation in these systems, and then, focusing on a simpler system governed by birth-death processes, we illustrate pedagogically a recently proposed paradigm that provides a much more robust description of pattern formation: stochastic Turing patterns. We emphasize the essential role that cell-to-cell differences in molecular numbers—caused by inevitable fluctuations in gene expression—play, the so called demographic noise, in seeding the formation of stochastic Turing patterns over a much larger region of parameter space, compared to their deterministic counterparts. Full article
(This article belongs to the Special Issue Developmental Biology in Cyanobacteria)
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