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Compartmentalized function through cell differentiation in filamentous cyanobacteria

Key Points

  • Filamentous cyanobacteria such as Anabaena and Nostoc are oxygenic photoautotrophs that grow as trichomes in which some cells can differentiate to become specialized in different functions, producing a multicellular organism.

  • Cyanobacteria bear a Gram-negative type of cell envelope, carrying an outer membrane outside of the cytoplasmic membrane and murein sacculus. In filamentous cyanobacteria, whereas the cytoplasmic membrane and murein sacculus surround each cell, the outer membrane is continuous along the filament, defining a continuous periplasmic space that could represent a communication conduit between cells.

  • At the intercellular septa, protein complexes, of which SepJ (also known as Alr2338) is an identified component, help to keep cells together in the filament and might also have a role in intercellular communication, which can be probed with a fluorescent tracer, such as calcein.

  • In response to the environmental cue of nitrogen deficiency, some cells positioned at semi-regular intervals in the filament differentiate into N2-fixing heterocysts, a process that involves a specific programme of gene expression. Two proteins that are key to this process are the cyanobacterial nitrogen control transcription factor NtcA and heterocyst differentiation control protein (HetR), which are needed for differentiation to take place.

  • Differentiation of too many vegetative cells into heterocysts is prevented by inhibitors such as the small, diffusible heterocyst inhibition-signalling peptide (PatS) or a PatS-related compound, which are produced by the differentiating heterocysts.

  • The developed Anabaena filament containing two types of interdependent cells, the CO2-fixing vegetative cells and the N2-fixing heterocysts, is a fascinating case of multicellularity in the bacterial world that we are only starting to understand.

Abstract

Within the wide biodiversity that is found in the bacterial world, Cyanobacteria represents a unique phylogenetic group that is responsible for a key metabolic process in the biosphere — oxygenic photosynthesis — and that includes representatives exhibiting complex morphologies. Many cyanobacteria are multicellular, growing as filaments of cells in which some cells can differentiate to carry out specialized functions. These differentiated cells include resistance and dispersal forms as well as a metabolically specialized form that is devoted to N2 fixation, known as the heterocyst. In this Review we address cyanobacterial intercellular communication, the supracellular structure of the cyanobacterial filament and the basic principles that govern the process of heterocyst differentiation.

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Figure 1: Cell types in heterocyst-forming cyanobacteria.
Figure 2: The complex life cycles of some heterocyst-forming cyanobacteria.
Figure 3: Putative structures for intercellular communication.
Figure 4: The heterocyst and the heterocyst-vegetative cell septum.
Figure 5: Progress of heterocyst differentiation.
Figure 6: A complex gene promoter region.

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Acknowledgements

Work in the authors' laboratory was supported by research grants BFU2008-03811 (to E.F.) and BFU2007-60457 (to A.H.) from Ministerio de Ciencia e Innovación and grant CVI-1896 (to E.F.) from Junta de Andalucía (Spain).

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Correspondence to Enrique Flores.

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DATABASES

Entrez Genome Project

Anabaena sp. PCC 7120

Anabaena variabilis ATCC 29413

Escherichia coli

Nostoc punctiforme PCC 73102

Synechocystis sp. PCC 6803

Trichodesmium erythraeum IMS101

FURTHER INFORMATION

Enrique Flores and Antonia Herrero's homepage

CyanoBase

Gordon and Betty Moore Foundation Microbial Genome Sequencing Project

US Department of Energy Joint Genome Institute

Glossary

Oxygenic photosynthesis

A biological process that converts light energy into chemical energy and splits water to release oxygen.

Hypha

A branching cellular filament that forms the mycelium of actinobacteria and fungi.

Fruiting body

A cell aggregate where spores are formed in some myxobacteria and fungi.

Primary productivity

The production of organic compounds from CO2.

Heterocyst

A terminally differentiated N2-fixing cell found in some filamentous cyanobacteria.

Akinete

A cyanobacterial spore that tolerates cold and desiccation but not heat.

Hormogonium

A short filament made of small cells that serve a dispersal function in some filamentous cyanobacteria.

Murein sacculus

Also known as peptidoglycan. A large polymer surrounding the bacterial cell as a mesh and consisting of amino sugars and amino acids.

Lipopolysaccharide

A major component of the outer membrane of Gram-negative bacteria, consisting of a lipid covalently bound to a long polysaccharide that faces the extracellular medium.

β-Barrel

A protein domain made of β-strands that forms a closed structure with an internal opening.

Anoxic

Containing no oxygen.

Micro-oxic

Containing very low amounts of oxygen.

Monophyletic

Concerning a group of organisms that have evolved from a common ancestor.

Epistasis analysis

Investigation of the interaction between genes, such that a gene with a mutant phenotype that prevails is said to be epistatic over another related gene.

Diazotrophic physiology

The physiology related to the growth of an organism that uses N2 as a source of nitrogen.

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Flores, E., Herrero, A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8, 39–50 (2010). https://doi.org/10.1038/nrmicro2242

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