Cyanobacterial heterocysts

Abstract

Many multicellular cyanobacteria produce specialized nitrogen-fixing heterocysts. During diazotrophic growth of the model organism Anabaena (Nostoc) sp. strain PCC 7120, a regulated developmental pattern of single heterocysts separated by about 10 to 20 photosynthetic vegetative cells is maintained along filaments. Heterocyst structure and metabolic activity function together to accommodate the oxygen-sensitive process of nitrogen fixation. This article focuses on recent research on heterocyst development, including morphogenesis, transport of molecules between cells in a filament, differential gene expression, and pattern formation.

Figure 1.

Heterocyst development in Anabaena PCC 7120. (A) Anabaena PCC 7120 grown in medium containing a source of combined nitrogen grows as filaments of photosynthetic vegetative cells. (B) In the absence of combined nitrogen, heterocysts differentiate at semiregular intervals, forming a developmental pattern of single heterocysts every 10 to 20 vegetative cells along filaments. Heterocysts are often larger than vegetative cells, have a thicker multilayered envelope, and usually contain cyanophycin granules at their poles adjacent to a vegetative cell.

Figure 2.

Heterocyst development in Anabaena PCC 7120. Filaments of the wild type carrying a patS-gfp reporter grown in medium containing nitrate are composed of vegetative cells (A), and have undergone heterocyst development 1 d after transfer to medium without combined nitrogen (B). A patS mutant strain carrying the same patS-gfp reporter grown in media containing nitrate contains a small number of heterocysts (C), and 1 d after transfer to medium without combined nitrogen shows a higher than normal frequency of heterocysts and an abnormal developmental pattern (D). (A, B, C, D) Merged DIC (grayscale), autofluorescence of photosynthetic pigments (red), and patS-gfp reporter fluorescence (green) microscopic images; arrowheads indicate heterocysts; asterisks indicate proheterocysts; size bar, 5 µm. (E, F) Transmission electron micrographs of wild-type vegetative cells (V) and a heterocyst (H) at the end of a filament; T, thylakoid membranes; PS, polysaccharide layer; GL, glycolipid layer; C, polar cyanophycin granule; size bar, 0.2 µm.

Figure 3.

Transmission electron micrograph of the junction between two vegetative cells. Arrowheads indicate microplasmodesmata, which are potential cell-to-cell channels. Note the "junctional space" between the cell wall peptidoglycan layers of the two cells, which may indicate a partial barrier between the periplasmic compartments of adjacent cells. IM, inner membrane; OM, outer membrane; P, periplasm; PG, peptidoglycan cell wall; JS, junctional space. Size bar, 0.5 µm.

Figure 4.

Developmentally regulated σ factors in Anabaena PCC 7120. The positions of the σ factor icons mark the times that GFP transcriptional reporters for the σ factor genes are up-regulated during heterocyst development. Filaments are composed of vegetative cells before nitrogen limitation. Immature proheterocysts are observed during approximately the same period of time when cells become committed to complete differentiation. Mature heterocysts are present by 20 h. See text for details.

Figure 5.

Model of regulatory interactions during heterocyst development. For clarity, the figure shows only selected genes, proteins, and events. Open boxes represent genes and gray ovals represent proteins. Lines ending in arrows and bars indicate positive and negative interactions, respectively. Dashed lines represent indirect and/or unknown interactions or missing steps. Short arrows are between genes and their products. See the text for details.