Jean Houmard

[34] Complementary chromatic adaptation: Physiological conditions and action spectra

Publisher Summary This chapter focuses on the physiological conditions and action spectra of complementary chromatic adaptation. Photosynthetic organisms can modulate their relative pigment content in response to changes in either light intensity or light wavelength. Generally, one observes an inverse correlation between light intensity and pigment content—the less light energy available, the more photosynthetic pigments are synthesized by the cells. The effect of light wavelength on the pigment content of the cells, termed complementary chromatic adaptation, appears to be restricted to some cyanobacteria. In this type of adaptation, changes in cell pigmentation in response to specific spectral illuminations result from modifications of the relative amounts of the red-colored phycoerythrin (PE) and the blue-colored phycocyanin (PC), with a predominance of PE in green-light-grown cells and of PC in red-light-grown cells. The regulatory processes involved in complementary chromatic adaptation are controlled by a photoreceptor pigment system which presumably acts at the transcriptional level. The property of photoreversibility of the cyanobacterial photoreceptor resembles that of the phytochrome present in higher plants and algae, although its action maxima are situated at shorter wavelengths in the visible spectrum.

Cyanobacterial Two-Component Proteins: Structure, Diversity, Distribution, and Evolution

SUMMARY A survey of the already characterized and potential two-component protein sequences that exist in the nine complete and seven partially annotated cyanobacterial genome sequences available (as of May 2005) showed that the cyanobacteria possess a much larger repertoire of such proteins than most other bacteria. By analysis of the domain structure of the 1,171 potential histidine kinases, response regulators, and hybrid kinases, many various arrangements of about thirty different modules could be distinguished. The number of two-component proteins is related in part to genome size but also to the variety of physiological properties and ecophysiologies of the different strains. Groups of orthologues were defined, only a few of which have representatives with known physiological functions. Based on comparisons with the proposed phylogenetic relationships between the strains, the orthology groups show that (i) a few genes, some of them clustered on the genome, have been conserved by all species, suggesting their very ancient origin and an essential role for the corresponding proteins, and (ii) duplications, fusions, gene losses, insertions, and deletions, as well as domain shuffling, occurred during evolution, leading to the extant repertoire. These mechanisms are put in perspective with the different genetic properties that cyanobacteria have to achieve genome plasticity. This review is designed to serve as a basis for orienting further research aimed at defining the most ancient regulatory mechanisms and understanding how evolution worked to select and keep the most appropriate systems for cyanobacteria to develop in the quite different environments that they have successfully colonized.

Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov. strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria).

The formal description of Prochlorococcus marinus Chisholm et al. 1992, 299 was based on the non-axenic nomenclatural type, strain CCMP 1375T. The purification and properties of the axenic strain PCC 9511, derived from the same primary culture (SARG) as the type species, are reported here. Prochlorococcus PCC 9511 differs from the latter in possessing horseshoe-shaped thylakoids, exhibiting a low chlorophyll b2 content and lacking phycoerythrin, but shares these phenotypic properties with Prochlorococcus strain CCMP 1378. This relationship was confirmed by 16S rRNA sequence analyses, which clearly demonstrated that the axenic isolate is not co-identic with the nomenclatural type. Strain PCC 9511 has a low mean DNA base composition (32 mol% G+C) and harbours the smallest genome of all known oxyphotobacteria (genome complexity 1.3 GDa = 2 Mbp). Urea and ammonia are the preferred sources of nitrogen for growth, whereas nitrate is not utilized. Several different organic phosphorus compounds efficiently replace phosphate in the culture medium, indicative of ecto-phosphohydrolase activity. In order to distinguish strain PCC 9511 from the nomenclatural type, a new subspecies is proposed, Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov.

A role for the signal transduction protein PII in the control of nitrate/nitrite uptake in a cyanobacterium

In the cyanobacterium Synechococcus sp. strain PCC 7942, ammonium exerts a rapid and reversible inhibition of the nitrate and nitrite uptake, and the PII protein (GlnB) is differentially phosphorylated depending on the intracellular N/C balance. RNA/DNA hybridizations, as well as nitrate and nitrite uptake experiments, were carried out with the wild‐type strain and a PII‐null mutant. The transcriptional control by ammonium of the expression of the nir‐nrtABCD‐narB operon remained operative in the mutant but, in contrast to the wild‐type strain, the mutant took up nitrate and nitrite even in the presence of ammonium. Moreover, the wild‐type phenotype was restored by insertion of a copy of the wild‐type glnB gene in the genome of the PII‐null mutant. These results indicate that the unphosphorylated form of PII is involved in the short‐term inhibition by ammonium of the nitrate and nitrite uptake in Synechococcus sp. strain PCC 7942.

A developmentally regulated gvpABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601.

In the filamentous cyanobacterium Calothrix PCC7601, gas-vesicle (GV) formation is restricted to specialized filaments, called hormogonia. The differentiation of these cells is controlled by environmental factors, such as light intensity and/or wavelength. The structural gene (gvpA) encoding a GV protein in this cyanobacterium has been previously cloned and sequenced. Two other genes, gvpB and gvpC have been found in the sequence downstream from gvpA. The gvpB gene corresponds to a second copy of gvpA, encoding an identical protein. Unlike the GV protein, the product of the gvpC gene is predominantly hydrophilic, as deduced from nucleotide sequence. Interestingly, the internal part of the gvpC gene is composed of four contiguous repeats, each containing 99 bp, forming highly homologous repeats in the deduced amino acid sequence. Another kind of periodicity has been detected inside the 99-bp repeats, suggesting that the gvpC gene might have evolved by amplification of a 33-bp-long primordial building block. The function of this gene remains to be elucidated. Finally, we have shown that the three genes, gvpA, gvpB, and gvpC, are organized in an operon that is exclusively expressed during GV formation in hormogonia.

Hormogonium Differentiation in the Cyanobacterium Calothrix: A Photoregulated Developmental Process.

Hormogonium differentiation is part of the developmental cycle in many heterocystous cyanobacteria. Hormogonia are involved in the dispersal and survival of the species in its natural habitat. The formation of these differentiated filaments has been shown to depend on several environmental conditions, including spectral light quality. We report here morphological and ultrastructural changes associated with the formation of hormogonia, as well as optimal light conditions required for their differentiation in the cyanobacterium Calothrix sp PCC 7601. The action spectrum for hormogonium differentiation is similar to that which triggers complementary chromatic adaptation because red and green radiation display antagonistic effects in both cases. However, these two photoregulated processes also show major differences. Transcription analyses of genes that are specifically expressed during hormogonium differentiation, as well as of genes encoding phycobiliproteins, suggest that two different photoregulatory pathways may exist in this cyanobacterium.

Photoregulation of gene expression in the filamentous cyanobacterium Calothrix sp. PCC 7601: light-harvesting complexes and cell differentiation

Light plays a major role in many physiological processes in cyanobacteria. In Calothrix sp. PCC 7601, these include the biosynthesis of the components of the light-harvesting antenna (phycobilisomes) and the differentiation of the vegetative trichomes into hormogonia (short chains of smaller cells). In order to study the molecular basis for the photoregulation of gene expression, physiological studies have been coupled with the characterization of genes involved either in the formation of phycobilisomes or in the synthesis of gas vesicles, which are only present at the hormogonial stage.In each system, a number of genes have been isolated and sequenced. This demonstrated the existence of multigene families, as well as of gene products which have not yet been identified biochemically. Further studies have also established the occurrence of both transcriptional and post-transcriptional regulation. The transcription of genes encoding components of the phycobilisome rods is light-wavelength dependent, while translation of the phycocyanin genes may require the synthesis of another gene product irrespective of the light regime. In this report, we propose two hypothetical models which might be part of the complex regulatory mechanisms involved in the formation of functional phycobilisomes. On the other hand, transcription of genes involved in the gas vesicles formation (gvp genes) is turned on during hormogonia differentiation, while that of phycobiliprotein genes is simultaneously turned off. In addition, and antisense RNA which might modulate the translation of the gvp mRNAs is synthezised.

A multigene family in Calothrix sp. PCC 7601 encodes phycocyanin, the major component of the cyanobacterial light-harvesting antenna

SummaryIn cyanobacteria, light is harvested by phycobilisomes which are essentially made up of chromophoric proteins called phycobiliproteins. We have characterized two gene clusters (cpcB1, cpcA1 and cpcB3, cpcA3) each encoding the two subunits of phycocyanin (βPC and αPC, respectively), one of the major phycobiliproteins in Calothrix 7601. Downstream from the gene encoding the PCα subunit in cluster 1, an open reading frame was found, cpcE1. These genes are organized in two transcriptional units, namely: cpcB3 A3 and cpcB1 A1 E1. All these genes are transcribed whatever the chromatic light received during cell growth. Consequently, although only one type of “constitutive” PC has been biochemically characterized, we have demonstrated that there are two cpc operons “constitutively” transcribed in this strain. With the previously described red light “inducible” cpcB2 A2 operon, there are three copies of the PC encoding genes in Calothrix 7601. The significance of this newly described multigene family in cyanobacteria is discussed. We have also mapped the 5′ and 3′ termini of the major transcript from the cpc1 operon. Analysis of the 5′ untranslated region of this transcript has revealed alternative secondary structures which are proposed to play a role in the regulation of the expression of this operon.

Convergence of two global transcriptional regulators on nitrogen induction of the stress-acclimation gene nblA in the cyanobacterium Synechococcus sp. PCC 7942

Cyanobacteria respond to environmental stress conditions by degrading their phycobilisomes, the light harvesting complexes for photosynthesis. The expression of nblA, a key gene in this process, is controlled by the response regulator NblR in Synechococcus sp. PCC 7942. Here we show that, under nitrogen stress, nblA is also regulated by NtcA, the global regulator for nitrogen control. NtcA activation of nblA was found to be nitrogen‐specific and did not take place under sulphur stress. Transcripts from the two major transcription start points (tsp) for the nblA gene were induced in response to nitrogen and sulphur starvation. The most active one (tspII) required both NblR and NtcA to induce full nblA expression under nitrogen starvation. NblR and NtcA bound in vitro to a DNA fragment from the nblA promoter region, suggesting that, under nitrogen stress, both NblR and NtcA activate the main regulated promoter (PnblA‐2) by direct DNA‐binding. The structure of PnblA‐2 differs from that of the canonical NtcA‐activated promoter and it is therefore proposed to represent a novel type of NtcA‐dependent promoter. We analysed expression patterns from ntcA and selected NtcA targets in NtcA–, NblR– and wild‐type strains, and discuss data suggesting further interrelations between phycobilisome degradation and nitrogen assimilation regulatory pathways.

Synechocystis Strain PCC 6803 cya2, a Prokaryotic Gene That Encodes a Guanylyl Cyclase

Synechocystis strain PCC 6803 exhibits similar levels of cyclic AMP (cAMP) and cyclic GMP (cGMP). A thorough analysis of its genome showed that Cya2 (Sll0646) has all the sequence determinants required in terms of activity and purine specificity for being a guanylyl cyclase. Insertional mutagenesis of cya2 caused a marked reduction in cGMP content without altering the cAMP content. Thus, Cya2 represents the first example of a prokaryotic guanylyl cyclase.