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Chapter 4 : Heterocyst Formation in Anabaena

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Abstract:

Heterocysts are differentiated cyanobacterial cells whose principal known function is the fixation of dinitrogen (N), an oxygen (O)-sensitive process, under aerobic conditions. Cyclic AMP, which plays a role in signal transduction in prokaryotes as well as eukaryotes, is present in sp., is responsive to nitrogen deprivation, and can disrupt the normal pattern of heterocyst formation. In sp., nitrate assimilation responds rapidly to nitrogen deprivation. The contiguous genes nirA, encoding nitrite reductase; nrtA, -B, - C, and -D, encoding nitrate transport proteins; and narB, encoding nitrate reductase, are rapidly and strongly induced in response to nitrogen stepdown. The fatty acyl portion of such lipids might be expected to be generated by a fatty acid or polyketide synthase. Indeed, it was found that mutations in closely positioned genes denoted hetN and hgIB (hetM), hgIC, and hgID that encode proteins that show a potential functional relationship to such synthases resulted in a lack of heterocyst envelope glycolipids. By means of a diversity of genetic approaches, including transposon mutagenesis, complementation of mutations induced by UV light and chemicals, response to added cosmids, and site-specific mutagenesis, numerous other genes that participate in differentiation of sp. have been identified. There may be independent regulation of the formation of the glycolipid and polysaccharide portions of the heterocyst envelope and of the (as yet little studied) maturation of the interior of the heterocyst.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 1
FIGURE 1

Light micrograph of filaments of Anabaena sp. strain PCC 7120. (A to C) Wild-type cells; those in panel C contain constitutively promoted extra copies of the patS gene on a pDU1-based shuttle vector. (D) patS mutant. The cells were grown with (A) and without (B to D) fixed nitrogen. Heterocysts (arrowheads) are absent from the nitrate-grown wild type, are present at semiregular intervals along the filaments of the wild type deprived of fixed nitrogen, are repressed by PatS, and are present in clusters and at abnormally close intervals in the nitrogen-deprived patS mutant. (An electron micrograph of a heterocyst of wild-type Anabaena sp. strain PCC 7120 may be seen in Fig. 6D .) (Reprinted from Yoon and Golden, 1998.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 2
FIGURE 2

Working model of certain genetic dependency relationships expressed in response to nitrogen stepdown. The thick arrows indicate a likelihood that that which follows the arrow depends upon that which precedes the arrow. For example, ntcA, but not hanA, is required for uptake and reduction of nitrate, which are catalyzed by products of the nirrA-nrtABCD-narB sequence. Both are required for heterocyst formation. Because the hanA gene is preceded by an NtcA-binding site, its transcription may depend upon activity of NtcA. There is suggestive evidence that HanA participates, direcdy or indirectly, in the transcriptional regulation of hetR and that nlcA acts also later in heterocyst differentiation. A hetR mutation prevents both heterocyst formation and (in N. ellipsosporum) akinete formation. The similar phenotypes of hetC and hetP mutants (the two genes map close together) are suggestive of a blockage in a very early step in the differentiation of cells that have been chosen to become heterocysts but, in N. ellipsosponum, no blockage in the formation of akinetes. Beyond the hetC-hetP step, formation of the two layers of the heterocyst envelope and development of the protoplast of the heterocyst appear to proceed independently, except that a combination of completion of the glycolipid layer and enhanced respiration may lead to microaerobic conditions in the protoplast, and microaerobiosis is required for such late biochemical changes as the appearance of nitrogenase activity, hep genes may also be active during formation of the akinete envelope (Leganés, 1994; Wolk et al, 1994). Where patS falls in this scheme is unclear. Thin curved arrows marked a to d refer to regulation that is probable (a), demonstrated (b), and possible (c and d). Temporal relationships, e.g., that in any particular region of the heterocyst envelope, glycolipid deposition follows polysaccharide deposition and that nitrogenase activity follows excisase activity, are not direcdy illustrated (for references, see the text). An earlier version of this model has appeared (Wolk et al., 1999).

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 3
FIGURE 3

Localization of expression of helR, visualized as hetR:: luxAB transcriptional fusions in the presence (A to D) and absence (E and F) of intact helR after 0 (A and E), 3.5 (B), 6, (C), and 24 (D and F) h of deprivation of fixed nitrogen in Anabaena sp. strain PCC 7120. In panel D, the arrows indicate mature heterocysts that appear nonluminescent due, at least in part, to a decrease in the concentration of O. a substrate of luciferase, within the heterocyst ( ). In each panel, the upper image is a bright-field micrograph with an instrumentally generated honeycomb background and the lower image represents luminescence integrated for 20 min. Bar. 10 µm. (Reproduced from , with permission.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 4
FIGURE 4

Heterocyst envelope glycolipids of Anabaena sp. strain PCC 7120.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 5
FIGURE 5

Composite structure of the probable repeating element of heterocyst envelope polysaccharides from A. cylindrica (a), A. variabilis (b), and Cylindrospermum sp. (c). The anomeric configurations of the linkages and the locations of particular side branches have been determined only for A. cylindrica. The dashes correspond to linkages that are present in only some of the positions indicated.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 6
FIGURE 6

Electron micrographs of the wild type (A and B) and hep A mutant DR1069 (C and D) of Anabaena sp. strain PCC 7120. (A and B) In a heterocyst (H) of wild-type Anabaena sp. strain PCC 7120, the laminated layer of glycolipids (GL) is enveloped by a layer of polysaccharide (PS). In contrast, the only envelope layer seen in heterocysts of the hepA mutant (C) is the laminated layer of glycolipids. (D) Enlargement of box in panel C. V, vegetative cell. (Panels A and B are reproduced from Zhu et al., 1998, with permission.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Tables

Generic image for table
TABLE 1

Classes of genes activated upon nitrogen stepdown and/or required for aerobic N fixation

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4

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