1 Faculty of Life Sciences, Bar-Ilan University, 52900 Ramat-Gan, Israel
2 Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, 35392 Giessen, Germany
Correspondence
Rakefet Schwarz
schwarr2{at}mail.biu.ac.il
Karl Forchhammer
Karl.Forchhammer{at}mikro.bio.uni-giessen.de
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ABSTRACT |
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Introduction |
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Deprivation of essential nutrients is frequently the limiting factor in cyanobacterial cell growth, and the need to adapt to periods of nutrient limitation is a major source of selective pressure in diverse natural environments. Various bacteria respond to nutrient limitation by entering a morphogenetic programme resulting in spore formation. Although they do not sporulate, unicellular cyanobacteria undergo substantial changes in response to nutrient starvation and exhibit sophisticated strategies that allow survival for long periods under stress conditions. This survival strategy, employing a stand-by energy metabolism (see below), differs fundamentally from the dormant state of spores and akinetes (spore-like cells produced by some filamentous cyanobacteria) and requires a highly regulated switch of cellular activities. Research in the past decade has led to fundamental new insights into the molecular mechanisms of these responses.
Classically, acclimation responses to nutrient limitation are grouped into specific and general, or common, responses. The specific responses are the acclimation processes that occur as a result of limitation for a particular nutrient, whereas the general responses occur under any starvation condition. This review will mainly describe studies in the unicellular, non-nitrogen-fixing strains Synechococcus elongatus PCC 7942 and Synechocystis sp. PCC 6803 (hereafter, Synechococcus and Synechocystis, respectively). First, we will describe the general acclimation processes, with an emphasis on modifications of the photosynthetic apparatus, as a fundamental aspect of cyanobacterial acclimation. Next, we will review the specific responses to limitation of the macronutrients phosphorus and nitrogen. As little substantial progress has been made in understanding the molecular mechanisms underlying responses to sulfur limitation, the reader is referred to the existing literature. Inorganic carbon availability is a major environmental factor affecting growth of photosynthetic micro-organisms such as cyanobacteria; this subject is reviewed elsewhere (Kaplan & Reinhold, 1999; Badger & Price, 2003
).
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General acclimation responses |
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An important aspect of survival under stress conditions is the protection of the genetic material. A Synechococcus homologue of the Escherichia coli Dps protein, a non-specific DNA binding protein essential for protection of bacterial DNA under stress (Almiron et al., 1992; Martinez & Kolter, 1997
; Wolf et al., 1999
), was identified and shown to accumulate in nutrient-limited cells (Pena et al., 1995
; Pena & Bullerjahn, 1995
). The alternative sigma factor, SigE, of Synechococcus sp. strain PCC 7002 is involved in expression of Dps upon entry of this cyanobacterium into stationary phase (Gruber & Bryant, 1998
). Further studies are required to elucidate the detailed regulation of Dps expression and to find out whether additional DNA-binding proteins with protective functions are present. Additional proteins that strongly accumulate in Synechococcus under conditions of nitrogen and sulfur starvation include the outer-membrane porins SomA/SomB (Sauer et al., 2001
; K. Forchhammer, unpublished), which might enhance the ability of the organisms to scavenge nutrients from their surroundings. Moreover, striking changes in cell physiology are related to the modification of the photosynthetic apparatus, as will be outlined below.
Modification of the photosynthetic apparatus
All photosynthetic organisms must tune their energy input, or excitation rate, to cellular metabolic capacity. During growth under nutrient-sufficient conditions, the reducing potential produced by the photosynthetic electron-transport chain is used for anabolic reactions. Nutrient limitation slows down the reoxidation of the final electron acceptors, and therefore electron transfer activity must be down-regulated (Grossman et al., 1993; Schwarz & Grossman, 1998
). The adjustment of the photosynthetic apparatus to nutrient-limiting conditions is a process that causes apparent changes; when cyanobacteria are maintained under conditions of starvation for an essential nutrient, they turn yellow (Fig. 2
a). This process, termed chlorosis or bleaching, was described long ago (Allen & Smith, 1969
) and has attracted manifold research activities. The common scheme of chlorosis is the degradation of photosynthetic pigments, in particular, the phycobiliprotiens, which constitute the major light-harvesting antenna in cyanobacteria, as well as chlorophyll a, the pigment in the reaction centres and core antenna of photosystem (PS) I and PSII. The kinetics of pigment degradation is rather variable and depends on the specific nutrient that is absent as well as on other environmental conditions such as CO2 supply, temperature and light intensity (Barker-Astrom et al., 2005
; Collier & Grossman, 1992
; Görl et al., 1998
). Furthermore, different cyanobacterial strains may respond quite differently to various starvation conditions. For example, sulfur starvation causes rapid chlorosis in Synechococcus (Collier & Grossman, 1992
), while Synechocystis does not degrade its phycobilisome in response to sulfur deprivation (Richaud et al., 2001
).
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Physiological analysis of long-term-starved cells that were maintained for more than 2 months in nitrogen-depleted medium revealed that the cells retained residual activities of PSI as well as PSII, amounting to approximately 0·1 % of the activity observed in growing cells (Sauer et al., 2001). Net oxygen evolution and anabolic activities, however, were not detected under these conditions. Therefore, it was suggested that cells perform a pseudo-cyclic electron flow (water-to-water cycle) in which oxygen, generated by PSII activity, is directly reduced by PSI. Interestingly, Synechocystis was recently shown to possess type A flavoproteins, which may directly reduce oxygen to water using electrons from PSI, thus without producing the toxic superoxide radical and hydrogen peroxide associated with the previously known mechanisms for pseudo-cyclic electron flow (Helman et al., 2003
). This electron-transport chain may generate membrane potential to fuel residual cellular activities. In vivo protein labelling revealed that the apparently dormant cells slowly turn over a subset of their cellular proteins, in particular proteins involved in photosynthesis and redox homeostasis, whereas proteins participating in the translational machinery are hardly synthesized de novo (Sauer et al., 2001
). In summary, the cyanobacterial mode of survival appears to be based on constant low metabolism, in contrast to the fully dormant stage exhibited by bacterial spores.
Degradation of the phycobilisome
Modulation of the phycobilisome, the light-harvesting antenna typical of most cyanobacteria, upon nutrient depletion involves repression of synthesis of new pigments as well as active degradation. Starvation for phosphorus (Collier & Grossman, 1992), inorganic carbon (Barker-Astrom et al., 2005
) or iron (Singh & Sherman, 2000
) results in partial loss of pigment. Nitrogen and sulfur starvation, on the other hand, elicit substantial pigment loss in Synechococcus, with nitrogen depletion inducing rapid and complete phycobilisome degradation (Collier & Grossman, 1992
). The phycobilisome is an ultrastructure consisting of pigmented proteins (phycobiliproteins) as well as non-pigmented (linker) polypeptides (Glazer, 1985
; Grossman et al., 1993
; MacColl, 1998
). The rapid and complete degradation of this abundant complex, which may constitute up to 50 % of soluble cellular protein, indicates the existence of highly effective degradation machinery.
To address the molecular mechanisms underlying the degradation process and its regulation, mutants were isolated that do not degrade their light-harvesting pigments under nutrient starvation. This phenotype was termed non-bleaching (Nbl) since the mutants appear blue-green when starved, rather than yellowish or bleached as do the wild-type cultures. Molecular analysis of non-bleaching mutants uncovered several genes essential for phycobilisome degradation. The pioneering work using this approach led to identification of nblA, a small gene encoding a 59 amino acid polypeptide, which is induced upon starvation (Collier & Grossman, 1994). Subsequently, genes encoding NblA-like peptides were identified and characterized in various cyanobacterial species (Baier et al., 2001
; de Alda et al., 2004
; Delumeau et al., 2002
; Luque et al., 2003
; Richaud et al., 2001
; Li & Sherman, 2002
). In fact, examination of the available complete genomic sequences indicated the existence of at least one nblA homologue in all organisms that possess a phycobilisome (cyanobacteria and red algae). NblA does not exhibit homology to any other proteins of known function, and its specific role in phycobilisome degradation is subject to speculation. Recent studies have suggested association of NblA with specific components of the phycobilisome (Luque et al., 2003
), but the functional significance of this association is yet to be established.
Under nitrogen starvation, certain filamentous cyanobacteria differentiate heterocysts, cells that have a specialized nitrogen fixation function. To enable the nitrogenase activity of heterocysts, oxygen evolution is depressed and the phycobilisomes are degraded as part of the down-regulation of their photosynthetic apparatus. NblA is essential for the specific phycobilisome degradation that occurs in these cells. The Anabaena nblA mutant, however, develops functional heterocysts, indicating that phycobilisome degradation is not essential for heterocyst development or nitrogen fixation (Baier et al., 2004). An additional component required for the degradation process is NblB (Dolganov & Grossman, 1999
). This protein exhibits homology to the chromophore-interacting region of phycocyanin lyases, enzymes that covalently attach a chromophore to the proteinaceous component of the pigment. Possibly, interaction of NblB with the chromophore is required for the disassembly of the phycobilisome, rendering it susceptible to protease action.
Pigment degradation must be tightly controlled either by environmental cues or by their physiological or biochemical consequences. Several regulatory components required for degradation have been identified. NblS (van Waasbergen et al., 2002) and NblR (Schwarz & Grossman, 1998
), are homologues of histidine kinase sensors and response regulators of two-component signal transduction pathways, respectively. Mutation in nblS or nblR results in severe impairment of phycobilisome degradation; however, the proposed function of the components encoded by these genes as a sensorregulator pair still awaits proof. NblC, a recently identified component of the nbl pathway, is a homologue of eubacterial anti-sigma factors (R. Schwarz, unpublished). These three regulatory components are required for efficient transcription induction of nblA. Previous analysis of a Synechococcus nblS mutant (van Waasbergen et al., 2002
) as well as recent studies of a nblS homologue (also termed dspA or hik33) mutant in Synechocystis (Hsiao et al., 2004
; Tu et al., 2004
) indicated that the nbl pathway, which modulates pigment degradation during nutrient stress, interacts with a signal transduction chain critical for transcription regulation under high-light conditions (Fig. 2
). This suggestion is supported by the pleiotropic effect of nblR mutations on cell survival during high light and nutrient stress (Schwarz & Grossman, 1998
) (see legend of Fig. 2
for details). The signal that triggers the nbl pathway is yet to be identified. The presence of a PAS domain in NblS suggests that light or redox changes may serve as a trigger for this pathway (van Waasbergen et al., 2002
). An additional modulator of general acclimation responses may be the protein encoded by slr2031, a homologue of eubacterial regulators of
B; cultures of an slr2031 mutant exhibit a lower proportion of cells capable of resuming growth following nitrogen or sulfur starvation (Huckauf et al., 2000
).
In summary, isolation and characterization of non-bleaching mutants has revealed several components of the phycobilisome degradation pathway. A novel screen employing fluorescence-activated cell sorting is expected to greatly facilitate the isolation of additional mutants and consequently genes involved in the pathway (Perelman et al., 2004). Characterization of the available and newly isolated mutants will help to delineate the mechanism of disintegration and degradation of the light-harvesting antennae as well as the details of the signal transduction cascade.
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Nutrient-specific molecular responses |
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Acclimation to phosphorus limitation
When starved for phosphorus, Synechococcus cells significantly induce phosphate uptake: a 50-fold increase in Vmax for phosphate transport is observed upon phosphorus starvation (Grillo & Gibson, 1979). Furthermore, periplasmic alkaline phosphatases, for example PhoA (Ray et al., 1991
) and PhoV (Wagner et al., 1995
), release phosphate from various compounds, making it available for the transport systems. PhoA, an atypically large alkaline phosphatase, is strongly induced upon starvation (Ray et al., 1991
). This enzyme may provide the ability to scavenge phosphate from a large variety of substrates, as suggested by its in vitro activity. The responses to phosphorus limitation are governed by a sensor kinase and a response regulator comprising a two-component signal transduction pathway. Genome-wide transcription analysis of Synechocystis revealed a phosphate regulon (Pho regulon), three clusters of genes exhibiting substantial induction upon phosphate starvation (Suzuki et al., 2004
). These include two sets of genes encoding putative phosphate-specific transport systems (pst1 and pst2), and phoA and nucH, which encode alkaline phosphatase and extracellular nuclease, respectively. An additional single gene encoding a periplasmic protein of unknown function, urtA, was found to be highly repressed upon phosphorus starvation. Importantly, the Pho regulon may extend beyond the genes described above (ppa and ppx may be included; see below); definition of the Pho regulon by Suzuki et al. (2004)
is currently based on genes which exhibit more than sevenfold induction or repression following phosphorus starvation. Transcription analysis of Synechocystis sensor (SphS) and regulator (SphR) mutants indicated exclusive regulation of the currently defined Pho regulon by these components. Examination of the promoter sequences of Synechocystis Pho regulon genes as well as gel mobility shift experiments identified a Pho box, a promoter sequence required for transcription activation by SphR (Suzuki et al., 2004
). The molecular mechanism underlying activation of SphS by phosphorus starvation and signal transduction to SphR is yet to be elucidated. The presence of a PAS domain in the C-terminal region of SphS suggests involvement of light or changes in redox state as possible signals (Suzuki et al., 2004
).
A study showing that complete genomic sequences may provide insight into ecological features came from analysis of the genomic region of phoR and phoB, encoding the sensor kinase and response regulators involved in acclimation to phosphorus limitation in two Prochlorococcus species (MED4 and MIT9313) (Scanlan & West, 2002). Prochlorococcus MIT9313, an ecotype acclimated to the low light intensity present in deep waters, carries a mutation introducing a stop codon into the coding region of phoR. Furthermore, this species possesses aberrant ptrA, a putative transcription regulator of phosphorus utilization. In contrast, the high-light-acclimated ecotype Prochlorococcus MED4 contains intact copies of phoR and ptrA. The mutations found in the Prochlorococcus MIT9313 may reflect the relatively high phosphorus concentrations found in deep waters, and therefore the dispensability of the components regulating the response to phosphate starvation.
Micro-organisms are able to accumulate inorganic phosphate in excess of their immediate requirements. Polyphosphates, linear polymers of tens to hundreds of phosphate units linked by high-energy phosphoanhydride bonds, serve as a phosphate reservoir (Kornberg et al., 1999). Polyphosphate synthesis is dependent on Ppk (ATP-polyP phosphotransferase), whereas degradation of the polymer is achieved through the activity of Ppx (exophosphatase) and Ppa (inorganic pyrophosphorylase). The latter two enzymes are induced upon phosphorus starvation of Synechocystis (Gomez-Garcia et al., 2003
) and may be included in the Pho regulon. Ppa activity appears to be essential for survival: no fully segregated mutant in this gene has been isolated. ppx mutant strains exhibit aberrant growth as compared to the wild-type under phosphorus depletion but interestingly, during growth in replete medium as well. Aside from being a phosphate reservoir, polyphosphates have been assigned an elaborate series of functions including a regulatory role, and may function as an ATP substitute and divalent metal chelator (Kornberg et al., 1999
). Based on these multiple roles, the growth impairment of the ppx mutant of Synechocystis during phosphate-replete growth is not surprising. PolyP accumulation has been documented in a wide range of organisms under both favourable and stress conditions (Kornberg et al., 1999
). Interestingly, the Ppa homologue of Synechococcus is depressed during either nitrogen or sulfur starvation (Aldehni et al., 2003
). Accumulation of polyP is consistent with this repression of its degrading enzyme, Ppa; however, the cellular function of polyP as a general stress effector is unknown.
A recent study indicated substantial changes in the lipid composition of photosynthetic membranes upon phosphorus limitation in cyanobacteria as well as in green algae and higher plants. This is reflected in substitution of some of the phosphatidylglycerol with sulfoquinovosyldiacylglycerol (SQDG). Interestingly, a Synechococcus mutant impaired in SQDG synthesis becomes starved for phosphate sooner than the wild-type strain. This suggests that while maintaining the essential anionic composition of the photosynthetic membranes, the change in lipid composition allows some phosphate to be used for other cellular functions (Frentzen, 2004).
Acclimation to nitrogen deprivation
The global nitrogen control system.
Generally, ammonium is the preferred nitrogen source of cyanobacteria; its utilization prevents the use of alternative nitrogen sources via a regulatory system referred to as global nitrogen control (reviewed by Flores & Herrero, 1994; Herrero et al., 2001
). In the absence of usable combined nitrogen sources, diazotrophic strains are able to fix atmospheric N2 and thereby circumvent nitrogen depletion. In contrast, non-diazotrophic strains face nitrogen starvation, a situation which ultimately blocks anabolic metabolism and causes nitrogen chlorosis. Recently, it became evident that the global nitrogen control system shares common components with the specific responses of cyanobacteria to combined-nitrogen depletion. Various aspects of global nitrogen control have been reviewed recently (Herrero et al., 2001
, 2004
; Forchhammer 2004
), and therefore will only be outlined as regards their relevance to the specific responses of non-diazotrophic cyanobacteria to nitrogen starvation. The various nitrogen compounds that serve as nutrients are first converted to ammonium intracellularly. Ammonium is then assimilated via the glutamine synthetaseglutamate synthase (GS-GOGAT) pathway by incorporation into the carbon skeleton of 2-oxoglutarate, resulting in the synthesis of glutamate. 2-Oxoglutarate synthesis by isocitrate dehydrogenase is the final step of the oxidative branch of the TCA cycle in cyanobacteria (Tandeau de Marsac & Lee, 1999
), and its consumption via GOGAT is directly coupled to ammonium assimilation. Consequently, limitation of the GS-GOGAT cycle by ammonium depletion leads to accumulation of 2-oxoglutarate, which serves as an indicator of the cellular nitrogen status (Irmler et al., 1997
; Forchhammer, 1999
; Muro-Pastor et al., 2001
). Two 2-oxoglutarate-responsive elements, PII and NtcA, have been recognized so far in cyanobacteria. Although these proteins are generally present in cyanobacteria, they seem to affect gene expression differently in freshwater and marine cyanobacterial strains. The marine strains are adapted to very low ambient combined nitrogen concentrations and do not exhibit the tight repression in response to ammonium as described for the freshwater Synechococcus or Synechocystis strains. Thus, the regulatory role of these proteins in the marine strains remains to be further elucidated and we refer the reader to recent publications concerning marine Synechococcus and Prochlorococcus strains (Lindell et al., 2002
; Zubkov et al., 2003
; Bird & Wyman, 2003
).
The PII signalling protein.
The cyanobacterial PII protein is a member of the large family of PII signal transduction proteins, which have widespread roles in nitrogen control in bacteria, plants, and some archaea (for recent reviews see Arcondeguy et al., 2001; Forchhammer, 2004
). Similar to the PII signalling protein in E. coli (Kamberov et al., 1995
), Synechococcus PII binds ATP and 2-oxoglutarate in a cooperative manner (Forchhammer & Hedler, 1997
) and was the first 2-oxoglutarate-responsive factor recognized in cyanobacteria. In the presence of increased 2-oxoglutarate levels, corresponding to nitrogen-limited conditions, PII is phosphorylated at a seryl residue (Ser-49) (Forchhammer & Tandeau de Marsac, 1995a
). PII-P is dephosphorylated in vitro at low 2-oxoglutarate levels (Ruppert et al., 2002
), which correspond in vivo to conditions of nitrogen excess (ammonium supplementation) or limiting inorganic carbon supply (see Fig. 3
). In general, PII signal transduction is based on proteinprotein interactions with receptor proteins, in which PII modulates the activities of the target proteins. The proteinprotein interactions are sensitive to the signal input state of PII proteins, including their binding of effector molecules and, if applicable, their state of covalent modification. Recently, the key enzyme of the arginine synthesis pathway, N-acetylglutamate kinase (NAGK), was identified as the first receptor for PII in a cyanobacterium (Heinrich et al., 2004
; Burillo et al., 2004
). Complex formation and catalytic activation by PII of NAGK was shown to depend both on the phosphorylation state of PII and on its binding of effector molecules (Heinrich et al., 2004
; Maheswaran et al., 2004
). Earlier studies suggested that PII plays only a subordinate role in the regulation of nitrogen assimilation via global nitrogen control, since the response of several ammonium-depressed genes to the absence or presence of ammonium was not significantly altered in PII mutants (Lee et al., 2000
). The contribution of PII to global nitrogen control appeared to be limited to the regulation of ammonium/CO2-dependent nitrate/nitrite uptake (Forchhammer & Tandeau de Marsac, 1995b
; Lee et al., 1998
, Hisbergues et al., 1999
). However, recent results suggest that PII is intimately involved in the response of cyanobacteria to nitrogen limitation (see below).
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Functional interaction of PII and NtcA during nitrogen deprivation.
Synthesis of GlnN following nitrogen deprivation is impaired not only in an NtcA-deficient mutant but also in a mutant deficient in PII (Sauer et al., 2000), suggesting a link between PII and NtcA under conditions of nitrogen deprivation. To investigate this potential relationship, protein synthesis patterns of Synechococcus wild-type, PII- and NtcA-deficient mutants were compared (Aldehni et al., 2003
). All proteins whose synthesis responded specifically to nitrogen deprivation (and did not respond to sulfur starvation), were shown to be under NtcA control, demonstrating the universal role of NtcA as the master-regulator of nitrogen-controlled gene expression. Surprisingly, however, the PII-deficient mutant exhibits a similar phenotype. It is also unable to specifically respond to combined-nitrogen deprivation at the level of altered protein expression patterns, confirming a functional relationship between PII and NtcA.
Another class of proteins respond to both nitrogen and sulfur deprivation. Most of these are not affected in NtcA or PII mutants; some, however, are indeed affected in the NtcA or PII mutant background, but only during nitrogen deprivation. One of the NtcA/PII-dependent so-called general starvation-repressed proteins' was identified as a subunit of RubisCO. Northern blot analysis revealed that the RubisCO (rbcSL) genes are in fact rapidly down-regulated following nitrogen deprivation in an NtcA/PII-dependent manner. This suggests that some genes which respond to different kinds of nutrient stresses, such as rbcLS, are controlled by separate mechanisms under the various conditions, e.g. by NtcA during nitrogen depletion and by an as-yet-unidentified factor during sulfur starvation. In no case do the NtcA- and PII-deficient mutants show an impaired response during sulfur deprivation, demonstrating their nitrogen specificity. The PII requirement in activating NtcA-dependent gene expression following nitrogen deprivation was studied independently by Northern blot analysis on four different NtcA-dependent transcripts (Paz-Yepes et al., 2003). Whereas in the wild-type, these transcripts accumulate rapidly after shifting cells from nitrate-supplemented to combined nitrogen-depleted medium, this transcriptional response is strongly impaired in a PII-deficient mutant. A PII Ser49Ala mutant, which cannot be phosphorylated (Lee et al., 2000
), also shows impaired activation of NtcA (Paz-Yepes et al., 2003
), suggesting that the phosphorylated form of PII preferentially stimulates NtcA-dependent transcription following nitrogen step-down.
The fine-tuning of NtcA activity by PII was investigated by using luxAB reporter fusions to the glnB promoter, which is regulated by NtcA (Aldehni et al., 2003). In a truncated version of the glnB promoter, in which the constitutive,
70-dependent start site 1 was deleted, retaining only the NtcA-dependent start site (tsp2), differential PII dependency of reporter gene (luciferase) activity could be detected. In the presence of ammonium, luxAB expression was repressed to very low levels in both the wild-type and the PII-deficient mutant. In the presence of nitrate, luxAB was moderately expressed in the wild-type, but considerably derepressed in the PII-null mutant. When cells were shifted to nitrogen-depleted conditions, promoter activity increased rapidly to very high levels in the wild-type, whereas the PII mutant failed to increase reporter activity further. Together, these observations suggest the following functional relationships between PII and NtcA. (i) In the presence of nitrate, the PII-deficient mutant exhibits significantly higher NtcA-dependent reporter gene activity than the wild-type, suggesting that PII is inhibitory for NtcA under those conditions. This confirms older studies showing a partial derepression of nitrogen-regulated enzymes in the PII-deficient background in the presence of nitrate (Forchhammer & Tandeau de Marsac, 1995b
). (ii) The high activation of NtcA following nitrogen step-down requires PII. In addition, activation of NtcA by phosphorylated PII occurs only in the absence of nitrate, suggesting that an additional factor is needed to distinguish between the presence of nitrate and the absence of any nitrogen source. To clarify these points, the mechanism of functional interaction between NtcA and PII must be determined.
Reciprocally to the effect of PII on NtcA activation, NtcA affects PII under nitrogen-limited conditions. In the NtcA-deficient mutant, phosphorylation of the PII protein is drastically affected: almost no phosphorylation occurs after nitrogen step-down (Lee et al., 1999; Sauer et al., 1999
), suggesting that PII kinase might be under NtcA control. Furthermore, transcription of the PII-encoding glnB gene is strongly enhanced by activated NtcA under conditions of nitrogen deprivation (see above). These mutual interactions result in a positive feedback loop: phosphorylated PII activates NtcA; in turn, activated NtcA augments the levels of the NtcA and PII proteins as well as stimulating PII phosphorylation (see Fig. 3
).
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Cross-talk between signalling pathways |
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Future prospects |
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Studies of heterotrophic eubacteria have highlighted phenomena related to stress physiology, which, although not yet documented for cyanobacteria, may be relevant to their acclimation strategy. Bacterial cultures at the so-called stationary phase of growth were shown to be highly dynamic; clones having a growth advantage at the stationary phase (GASP) tend to take over the population (Finkel & Kolter, 1999). Another example is quorum sensing, the expression of genes under density-dependent control, mediated by bacterial pheromones and crucial for numerous stress-related bacterial responses (Bassler, 2002
). Although quorum sensing has not been documented for cyanobacteria, this mechanism may present a novel aspect of their acclimation responses based on intra-species interaction and communal behaviour.
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ACKNOWLEDGEMENTS |
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