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Department of Microbiology, University of Hawaii, Honolulu, HI 96822, USA
Correspondence
Sean M. Callahan
scallaha{at}hawaii.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Heterocysts produced by Anabaena sp. strain PCC 7120 can be distinguished from vegetative cells microscopically by their larger size and thicker cell envelope. In order to create microaerophilic conditions for the activity of nitrogenase, they have two additional layers of envelope made of polysaccharides and glycolipids (Murry & Wolk, 1989
). The glycolipid layer, which is the innermost of the two, is thought to act as a barrier against the entry of oxygen (Walsby, 1985; Winkenbach et al., 1972). The exterior polysaccharide layer is thought to preserve the integrity of the glycolipid layer. Genes necessary for the production and localization of both layers have been found, and pathways for their synthesis have been proposed (Fan et al., 2005; Huang et al., 2005). Once a micro-oxic environment has been created inside the heterocysts, they fix atmospheric nitrogen, and transport it to vegetative cells, and in return they receive a source of reductant required for fixation from vegetative cells (Thomas et al., 1977).
The pattern of heterocysts along a filament is determined by the interplay of positive- and negative-acting regulatory factors, and approximately 12 h after the removal of fixed nitrogen, selected cells have committed to terminal differentiation into heterocysts (Meeks & Elhai, 2002; Wolk, 2000; Zhang et al., 2006). PatS and HetR appear to be the two central factors that control differentiation and pattern formation. HetR is the master regulator and has both DNA-binding and protease activity (Buikema & Haselkorn, 1991b; Huang et al., 2004; Zhou et al., 1998). It displays positive autoregulation, and expression of hetR is induced in proheterocysts prior to commitment to differentiation (Black et al., 1993).
In order to identify the genes involved in diazotrophic growth and differentiation of heterocysts by Anabaena sp. strain PCC 7120, a genetic screen was conducted to isolate mutants incapable of growth in the absence of fixed nitrogen. Interruption of the coding region of fraG, the gene upstream of hetR, by a transposon resulted in a fragmentation mutant that was unable to grow in the absence of a fixed source of nitrogen. The predicted protein is similar to permeases and is necessary for filament integrity and maturation of heterocysts to the point of glycolipid layer formation.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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describes the Anabaena strains, plasmids and oligonucleotides used in this study. The wild-type strain Anabaena sp. strain PCC 7120, and its derivatives, were grown in BG-11 medium, and for induction of heterocysts they were transferred to BG-110 medium as described previously (Borthakur et al., 2005). Transposon mutagenesis, screening for mutants unable to grow diazotrophically and recovery of the transposon insertion site were performed as described by Wolk et al. (1991), except that spectinomycin and streptomycin, each at a concentration of 2.5 µg ml–1, were used to select for cells in which the transposon had transposed into the genome of Anabaena sp. strain PCC 7120. To determine mean filament lengths, the number of cells in 125 filaments was determined microscopically and averaged. Growth of Escherichia coli, and concentrations of antibiotics were as previously described (Borthakur et al., 2005).
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. pRL1058, which bears the original transposon on a suicide plasmid, was digested with MslI to remove genes conferring resistance to kanamycin, bleomycin and streptomycin. An 
cassette conferring resistance to streptomycin and spectinomycin was inserted as a SmaI fragment from pDW9 (Golden & Wiest, 1988) to create pRR106, which was used to mutagenize Anabaena sp. strain PCC 7120.
pAN120 is the suicide plasmid that was used to replace a 592 bp internal fragment of fraG with an cassette conferring resistance to streptomycin and spectinomycin. A region of DNA corresponding to nucleotides +12 to +817, relative to the start of fraG, was amplified using the primers alr2338 UF and alr2338 UR, and a downstream region of fraG corresponding to nucleotides +1409 to +2213 was amplified using the primers alr2338 DF and alr2338 DR. The two fragments were cloned into pGEM-T (Promega) and then moved into pHY101, which consists of pBluescript SK(+) (Stratagene) with an cassette conferring resistance to streptomycin and spectinomycin (Fellay et al., 1987) in the HindIII site, on either side of the cassette. A fragment consisting of the upstream and downstream regions of fraG flanking the cassette was moved into pRL278 (Black et al., 1993) using XhoI and SpeI. The fraG mutant UHM127 was created using plasmid pAN120, as previously described (Orozco et al., 2006).
Two GFP transcriptional fusions were made, resulting in plasmid pAN116, which contains nucleotides located at –352 to –19 relative to the translational start site of fraG, and pAN129, which contains nucleotides located at –760 to –19. Plasmid pAN116 was constructed by amplifying the promoter region of fraG using the primers alr2338promoterUp and alr2338promoterDown, and cloning into pGEM-T. The fragment was then moved to pAM1956 (Yoon & Golden, 2001) using SacI and KpnI. For plasmid pAN129, a larger region upstream of fraG was amplified using primers UpPalr2338SacIA and Rev 2338. This region was cloned directly into pAM1956 by using SacI and KpnI. Results with both plasmids were identical. To complement the 
fraG mutant, pAN130 was constructed. Plasmid pAN130 contains the promoter and coding region of fraG. This region was amplified using UpPalr2338SacIA and alr2338 end KpnI, and was moved into pAM505 (Wei et al., 1994) by using the restriction sites introduced by the primers.
Plasmid pDR138 was used to express hetR from the native hetR promoter. A 846 bp fragment upstream of the hetR coding region was amplified via PCR using primers PhetR-KpnI-F and PhetR-NdeI-R, and cloned into pGEM-T. PhetR was subsequently cloned into pBluescript as an ApaI–PstI fragment to create pDR133. hetR was amplified from genomic DNA using primers hetRcf-NdeI and hetR6H-r, cloned into pGEM-T and then moved to pDR133 as an NdeI–PstI fragment by using an NdeI site introduced by one of the primers. The subsequent PhetR–hetR fragment was cloned into pAM504 to create pDR138.
Acetylene reduction, glycolipid and exopolysaccharide assays.
For acetylene reduction assays, strains were grown in BG-11 medium to exponential phase. The cultures were then induced by transferring to BG-110 and grown under standard conditions for 120 h. Reduction of acetylene was measured immediately after nitrogen step-down, and every 24 h thereafter, using a gas chromatograph, as previously described (Borthakur et al., 2005). Reported values of acetylene reduction are means of measurements from three independent cultures. TLC and staining of exopolysaccharides were performed as previously described (Callahan & Buikema, 2001; Nichols & Wood, 1968).
Microscopy.
Cells were viewed through a Nikon Diaphot 300 inverted microscope, using either a x60 oil or a x40 objective, and images were captured with an Olympus DP70 digital camera. For fluorescent images, a Chroma Technologies 41001 filter set, with an excitation of 480±20 nm and an emission of 535±25 nm, was used to monitor fluorescence specific to the GFP. Images were processed in Adobe Photoshop version 7.0.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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), and named fraG (fragmentation, glycolipid) by ourselves, was interrupted at nucleotide positions +124, +158, +176 and +1770 relative to the predicted translational start site. To confirm a cause-and-effect relationship between the insertions and the mutants' inability to grow diazotrophically, an internal region of fraG in the wild-type strain Anabaena sp. strain PCC 7120 was replaced by an cassette. The resulting strain UHM127 was unable to grow diazotrophically. Because fraG is located immediately upstream of hetR, which is the master regulator for heterocyst differentiation, hetR and its promoter region were introduced into the mutant on a shuttle vector to see if the phenotype was the result of a polar effect on hetR. The wild-type phenotype was not restored to the mutant by the addition of hetR, whereas addition of a wild-type copy of fraG restored the wild-type phenotype, indicating that the phenotype of UHM127 was caused by inactivation of fraG.
The gene fraG encodes a putative protein of 751 aa. One complete and one partial DUF6 domain were detected at the carboxy-terminal end of the protein. DUF6 domains are indicative of integral membrane proteins and it is common for proteins to contain two of these domains. The carboxy-terminal half of the protein is predicted to contain 10 
-helical transmembrane domains (Marchler-Bauer et al., 2003).
The rate of growth of the mutant strain UHM127 was similar to that of the wild-type in medium containing nitrate as a fixed nitrogen source. However, mean filament length was substantially reduced to about 50 cells, compared with more than 200 cells for the wild-type. Unlike the wild-type, which forms a pattern of single heterocysts along the filament (Fig. 1a), UHM127 fragmented when deprived of fixed nitrogen. Fragmentation started between 16 and 18 h after nitrogen deprivation, and at 24 h, single cells and filaments with a mean filament length of about nine cells were present together (Fig. 1b), compared with intact filaments with a mean length of 150 cells for the wild-type. The single cells in the mutant culture were less pigmented than the cells in the filaments, reminiscent of the reduced pigmentation in heterocysts caused by the degradation of phycobilisomes. After 48 h nitrogen deprivation, the mean number of cells for the mutant was five, and for the wild-type it was 145. At 72 h and thereafter, the mutant culture was mostly unicellular (Fig. 1c). No mature heterocysts were observed in the mutant culture at any time.
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), was used as a control for anaerobic conditions and could only fix in the absence of oxygen as expected; UHM127 could not fix under either condition. At 48 h post-induction, rates of acetylene reduction for the wild-type under aerobic and anaerobic conditions, and for the pbp6 mutant, were 91, 392 and 86 nmol ethylene h–1 ml–1 (OD750 unit)–1, respectively. UHM127 was therefore categorized as a Fix– mutant with developmental defects.
Fragmentation can be elicited by differentiation alone
Deprivation of a fixed source of nitrogen induces a developmental programme in Anabaena sp. strain PCC 7120 that culminates in the formation of a pattern of heterocysts along a filament. To examine whether deprivation of fixed nitrogen, or induction of differentiation, was the more direct cause of fragmentation of the mutant strain UHM127, differentiation was induced in medium containing fixed nitrogen and the phenotype of the mutant was observed. Extra copies of hetR under the control of the copper-inducible petE promoter on plasmid pPetHetR cause differentiation of heterocysts in the wild-type strain in the presence of nitrate or ammonia when copper is present in the medium (Buikema & Haselkorn, 2001). UHM127 carrying pPetHetR, in the presence of nitrate and absence of copper, had filaments similar to the same strain without the plasmid. However, when copper was included in the medium to induce expression of hetR and heterocyst formation, the strain fragmented in a manner similar to the mutant strain in a medium lacking fixed nitrogen at 24 h post-induction (Fig. 1d
). Fragmentation in the presence of fixed nitrogen when differentiation was induced by overexpression of hetR suggested that differentiation, and not a lack of fixed nitrogen in the medium, was the more direct cause of fragmentation by the mutant.
fraG is not necessary for pattern formation
The absence of mature heterocysts in strain UHM127 indicated that fraG was necessary for complete differentiation of heterocysts. To determine whether inactivation of fraG affects the formation of the heterocyst pattern, a hetR–gfp transcriptional fusion on plasmid pSMC127 (Callahan & Buikema, 2001) was introduced on a shuttle vector into both the mutant and the wild-type. In the wild-type, a pattern of expression of hetR in single cells that predicted the pattern of cells that differentiated into heterocysts could be visualized with the GFP fusion between approximately 8 and 24 h after removal of combined nitrogen. In UHM127, a pattern of GFP fluorescence was seen in proheterocysts 12 h after induction, before fragmentation started in the mutant (Fig. 2a, b). A pattern of induction of the hetR promoter in single cells separated by approximately 10 cells with lower fluorescence, and similar to that in the wild-type, was seen in the mutant, and this suggested that fraG was not necessary for proper pattern formation.
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). From the time of removal of fixed nitrogen from the culture, to the appearance of mature heterocysts, the same low uniform level of fluorescence was observed as seen with filaments grown in medium containing nitrate. Therefore, transcription of fraG appeared to be enhanced in heterocysts, or perhaps in proheterocysts just prior to maturation.
fraG is necessary for synthesis of heterocyst glycolipids
Although cells with larger size and thickened cell envelopes, two of the attributes of mature heterocysts, were not seen in the fraG mutant, single cells with reduced pigmentation appeared to break off and fragment filaments between 16 and 18 h post-induction. These cells appeared to be proheterocysts that were arrested at a certain stage of development. To determine if heterocyst-specific exopolysaccharides and glycolipids, which are involved in the late stages of heterocyst maturation and necessary for creation of a microaerophilic environment in functioning heterocysts, were produced in the fraG mutant, UHM127 was checked for their presence. Alcian Blue, which binds specifically to heterocyst envelope polysaccharides, stained the cells with reduced pigmentation that broke from the filaments between 16 and 18 h post-induction, confirming that they were proheterocysts and indicating that fraG was not necessary for exopolysaccharide synthesis or deposition (Fig. 3).
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). UHM127 complemented with a wild-type copy of fraG on a plasmid produced similar types and quantities of glycolipids as the wild-type. The absence of heterocyst glycolipids in the mutant implied that either fraG performs a function that may be directly required for glycolipid synthesis or, alternatively, fragmentation arrests development before glycolipid synthesis begins in the wild-type, and their absence in the mutant is an indirect consequence of mutation of fraG. To distinguish between these two possibilities, glycolipids from the mutant and the wild-type were visualized at 15 h post-induction, before fragmentation of the mutant. One of the two heterocyst glycolipids was clearly visible in samples from the wild-type 15 h post-induction, indicating that glycolipid synthesis began before the time of fragmentation of UHM127 (Fig. 4). The mutant, however, had not produced heterocyst glycolipid at this time when filaments were still intact; this indicated that fragmentation most likely did not arrest development prior to synthesis of glycolipid to stop its production. Instead, it appeared that fraG was necessary for both glycolipid synthesis and maintenance of filament integrity during differentiation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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described the isolation of four mutants with Fox– fragmentation phenotypes in a study that also led to the identification of hetR. For one mutant, the mutation necessary for the phenotype was found to disrupt the fraC gene, which encodes a phenylalanine-rich peptide with four potential transmembrane domains (Bauer et al., 1995). In contrast to the fraG mutant UHM127 described here, a fraC mutant can fix nitrogen in the absence of molecular oxygen, mature heterocysts are occasionally observed and can be induced by introducing extra copies of hetR on a plasmid, and the fragmentation phenotype is more severe in the presence of fixed nitrogen. Similarly, mutation of fraH, which encodes a proline-rich peptide, causes fragmentation of filaments, but mature heterocysts are common in the mutant. The genetically uncharacterized fragmentation mutant N5 described by Wolk and coworkers, on the other hand, shows no signs of differentiation (Ernst et al., 1992), unlike UHM127, which develops a normal pattern of proheterocysts. Finally, Golden and coworkers inactivated some group 2 sigma factors from Anabaena sp. strain PCC 7120 and found that a sigE sigD double mutant fragmented upon removal of fixed nitrogen, but mature heterocysts were formed (Khudyakov & Golden, 2001), suggesting that these two sigma factors are more likely to be involved in transcription of fraC or fraH, than transcription of fraG. The increased fragility of the majority of fragmentation mutants in both nitrogen-replete and nitrogen-free media suggests that the integrity of heterocyst–vegetative cell junctions may rely on proteins that are also necessary for vegetative cell junctions, rather than being dependent solely on a separate set of proteins specific to heterocyst junctions. A low level of expression of fraG in vegetative cells, followed by induction in heterocysts, is consistent with this idea.
The somewhat pleiotropic effect of mutation of fraG, which resulted in Fix– Hgl– (lacking correctly localized heterocyst glycolipids) Fra phenotypes, suggests that mutation of fraG affects both structural and regulatory aspects of heterocyst development, with a defect in one affecting the other. In particular, FraG may have a structural role only, and its effect on glycolipid synthesis and regulation of differentiation could be indirect. Disruption of glycolipid formation, or the accumulation of a glycolipid intermediate, may affect filament integrity. Conversely, as an integral membrane protein, FraG may have primarily a structural role that is necessary for the advancement beyond a certain point in the developmental programme. In this case, regulation of differentiation would involve sensing of membrane or cell-junction structure. The formation of heterocyst-specific glycolipid by the wild-type at a time before fragmentation of the mutant, coupled with the absence of glycolipid synthesis in the mutant, suggests that fragmentation is not the structural change that prevents differentiation in the absence of fraG. Finally, the primary function of fraG may be in transport or signal transduction that is necessary for development, and disruption of development initiates a genetically programmed response that leads to fragmentation. Fragmentation of the wild-type strain under some environmental conditions, and after the death of heterocysts when filaments are returned to nitrogen-replete conditions, may confer a selective advantage under certain conditions, presumably by facilitating cell dispersion.
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ACKNOWLEDGEMENTS |
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Edited by: D. J. Scanlan
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 15 September 2006;
revised 18 October 2006;
accepted 20 October 2006.
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