Photosynthesis is a function of highly organized pigment protein complexes that are embedded in the polar lipid matrix of thylakoid membranes. Some of the lipids found in this membrane are generally absent from nonphotosynthetic membranes. A typical example is the sulfolipid sulfoquinovosyl diacylglycerol, which occurs in almost all photosynthetic organisms (1) with the exception of a few photosynthetic bacteria (2) and Rhizobium meliloti 2011, a nonphotosynthetic but plant-associated bacterium (3) with sulfolipid in its membranes. Although in higher plants and cyanobacteria two photoactive pigment-containing complexes exist, photosystems I and II, only one is present in purple bacteria. The photosynthetic reaction center of purple bacteria shows high structural and functional homology to that of photosystem II of cyanobacteria and plants (for a review see (4) ), but only photosystem II catalyzes the light-induced reduction of plastoquinone with electrons from water, thereby releasing oxygen (for a review see (5) ). The water splitting system is absent from purple bacteria, which use hydrogen donors with relatively low redox potential and evolve no oxygen. Because of the similar organization of the photosynthetic apparatus in cyanobacteria and higher plants, cyanobacteria have been used as model systems to genetically dissect the protein complexes of the thylakoid membrane (for reviews see Refs. 6 and 7). Because some cyanobacterial strains can grow heterotrophically, genes encoding individual protein components of the two photosystems can be inactivated by gene replacement, and the analysis of the resulting null mutants can reveal the function of the affected proteins. This genetic approach can also be applied to investigate the role of polar lipids for the formation and maintenance of protein lipid complexes required for oxygenic photosynthesis. However, no cyanobacterial mutants have been available that completely lack a class of polar lipids of the thylakoid membrane. But it should be noted that heterocyst mutants deficient in the biosynthesis of glycolipids specifically associated with this specialized, nitrogen-fixing cell type are known(8) . Furthermore, the fatty acid composition of cyanobacterial polar lipids has been altered by genetic engineering in order to study the influence of fatty acid composition on thermal tolerance of the organism(9) .

The almost exclusive occurrence of sulfolipid in photosynthetic membranes and its unusual sulfoquinovosyl head group (10) has stimulated debate over a specific role for this lipid in photosynthesis (11) . Sulfolipid has been identified as integral component of photosystem II protein complexes(12, 13) . Furthermore, in reconstitution experiments with chloroplast ATP synthase, sulfolipid was found to be required in stoichiometric amounts with other lipids for successful restoration of enzymatic activity(14) . These results led to the conclusion that sulfolipid functions as essential boundary lipid. Based on a more recent analysis of a sulfolipid-null mutant of the purple bacterium Rhodobacter sphaeroides, it can be assumed that sulfolipid plays no specific role in anoxygenic photosynthesis(15) , because photosynthetic electron transport rates were not altered and growth under optimal conditions was not reduced. However, upon transfer to phosphate-limiting conditions, growth of the mutant ceased earlier than that of wild type cells. In addition, a strong reduction in phospholipid content and a concomitant increase in novel lipids as well as sulfolipid was observed in the phosphate-stressed cells of R. sphaeroides(16) . Taken together, these observations led to the conclusion that sulfolipid may play a role as substitute for anionic phospholipids under phosphate-limiting growth conditions in purple bacteria and possibly other photosynthetic organisms.

Recently, a sulfolipid-deficient mutant of Chlamydomonas reinhardtii, which was induced by exposure to UV light, has been isolated based on its abnormal chlorophyll fluorescence(17) . The chlorophyll fluorescence phenotype is an indication that photosynthesis is affected in this mutant. However, it has not clearly been demonstrated that the fluorescence phenotype and the sulfolipid deficiency are due to the same genetic defect, leaving the causal relation between the two phenotypes open.

To further address the question of whether sulfolipid plays an essential role for oxygenic photosynthesis, we isolated and inactivated a gene involved in sulfolipid biosynthesis from the cyanobacterium Synechococcus sp. PCC7942. The only previously known genes encoding sulfolipid biosynthetic enzymes were the sqd genes from R. sphaeroides(18, 19) , of which one served as a molecular probe to isolate the homologous gene from the cyanobacterium. The resulting sulfolipid null mutant was analyzed with regard to its photosynthetic characteristics and growth under different conditions. Possible modifications of the photosystem II reaction kinetics due to the lack of sulfoquinovosyl diacylglycerol were investigated by measuring the oxygen yield in response to a regime of short flashes.

MATERIALS AND METHODS

Bacterial Strains, Plasmids, Media, and Growth Conditions

For routine cloning experiments, the Escherichia coli strains XL-1 Blue, XL-1 Blue MRF`, and XLOLR, as well as the plasmids pBluescript II-SK and pBK-CMV and the phage -ZAP-Express and ExAssist helper phage were used (Stratagene). The inactivation cassette carrying a neomycin phosphotransferase gene was derived from pUC4K(21, 22) . The origin of plasmids pSY2, pSY3, and pSYB (see Fig. 1) is described in the results section. Cultures of E. coli were grown in Luria broth. Kanamycin was usually added as required at 50 µg ml, and ampicillin was added at 100 µg ml.

Figure 1: Plasmids used for the characterization and inactivation of the sqdB gene from Synechococcus sp. PCC7942. Plasmids were constructed as described in the text. Small solid arrows, directions of sequence reactions; gray arrow, sqdB open reading frame; open arrow, neomycin phosphotransferase gene; cross-hatched box, fragment used for Southern hybridization. Restriction sites: A, BamHI; E, SpeI; H, HindIII; O, XhoI; P, PstI; S, SalI. The asterisks indicate a Sau3A/BamHI ligation site.

Recombinant DNA Techniques

Insertional Inactivation of sqdB and Transformation of Synechococcus sp. PCC7942

Lipid Analysis

Preparation of Radiolabeled Lipids

Oxygen Evolution Measurements

Absorption, 77 K, and Room Temperature Fluorescence Emission Measurements

Nucleotide Sequence

RESULTS

Isolation and Characterization of a Cyanobacterial Gene with Sequence Similarity to sqdB of R. sphaeroides

Figure 2: DNA and deduced amino acid sequence of the Synechococcus sp. PCC7942 sqdB gene. The nucleotide sequence is shown from the KpnI site to the XhoI site of pSYB. The protein sequence is given below the DNA sequence. The underlining indicates a putative ribosome binding site.

Construction of a Sulfolipid-deficient Null Mutant

Figure 3: Southern hybridization of wild type (WT) and SY-SQDB mutant. Genomic DNA was cut with HindIII and probed with a 1470-base pair SpeI/XhoI fragment from sqdB containing the open reading frame and adjacent sequences. The approximate length of DNA fragments is indicated (kilobase pairs).

Figure 4: Separation of S-labeled lipids of wild type (WT) and SY-SQDB mutant by thin layer chromatography. Approximately equal amounts of total lipids were spotted in case of undiluted extracts (undil.). In addition, 10-, 100-, and 1000-fold dilutions of the wild type extracts were loaded for estimation of the reduction of sulfolipid in the mutant extract. Radiolabeled lipids were visualized by autoradiography. F, solvent front; O, origin; SQD, sulfoquinovosyl diacylglycerol; U, unidentified compound.

The Effects of Phosphate-limiting Conditions on Growth and Lipid Composition of Mutant and Wild Type

Figure 5: Growth of Synechococcus sp. PCC7942 wild type (closed circles) and SY-SQDB mutant (open circles) under optimal (A) and under phosphate limiting conditions (B). Each value represents the mean of three measurements using independent cultures. Error bars were smaller than symbols.

Under phosphate-limiting growth conditions the relative amount of the major phospholipid phosphatidyl glycerol was reduced in wild type cells to 7.2 mol % compared with cells grown under optimal conditions (16.6 mol %, Table 1). Concomitantly, an increase in the relative amount of sulfolipid and digalactosyl diacylglycerol was observed for the wild type, whereas the relative amount of monogalactosyl diacylglycerol was slightly decreased. In the mutant, the relative amount of phosphatidylglycerol (28.4 mol %) was increased under optimal growth conditions and did not decrease as dramatically under phosphate-limiting conditions (23.2 mol %, Table 1). The relative amounts of the galactolipids were comparable with those found in wild type cells under both growth regimes.

Photosynthetic Characteristics of the Sulfolipid-deficient Mutant

Figure 6: Rate of oxygen evolution as function of photon flux density by Synechococcus sp. PCC7942 wild type (closed circles) and SY-SQDB mutant (open circles). Each value represents the mean of three independent measurements. The standard error was less than 6% of each value.

To examine the possibility of subtle changes in the reaction kinetics of photosystem II, the characteristic period four oscillation pattern of flash-induced oxygen evolution was compared in dark adapted wild type and mutant cells. The maximum oxygen yield is generated by the fourth flash (Fig. 7). This feature is typical for thoroughly dark-adapted cyanobacteria(31) . With regard to the active site tyrosine (Y) of the D2 protein, this pattern is indicative of an apparent population of redox states below SY (see (32) and references therein). Within the frame work of an extended Kok model, in which a cyclic sequence of redox states adopted by the water oxidase during catalysis is postulated(33) , the data can be satisfactorily described by the probability of misses ( = 0.23) and double hits ( = 0.01) and apparent S-state dark populations of [S] = 0.47, [S] = 0.39, and [S] = 0.12. Preillumination with a short saturating flash and subsequent dark incubation for 3 min leads to a shift of oxygen yield maximum to the third flash. This observation shows that the apparent high population of S is mainly due to the presence of Y in its reduced form(32) . Both oscillatory patterns exhibited virtually the same features (Fig. 7, A and B) except for the pronounced oxygen uptake in the mutant sample after the first two flashes of the sequence (Fig. 7B). In an attempt to test whether this phenomenon was restricted to the first two flashes, the measurements were repeated in the presence of hydrazine. Under these conditions the redox state S is highly populated, and the maximum of oxygen yield is shifted toward the sixth flash(32) . Likewise, virtually no oxygen is evolved during the first four flashes. Contrary to the wild type, the oxygen yield pattern of hydrazine-treated mutant cells revealed a marked oxygen uptake during the first four flashes in the SY-SQDB mutant (data not shown).

Figure 7: Flash-induced changes of oxygen evolution or uptake by Synechococcus sp. PCC7942 wild type (A) and SY-SQDB mutant (B). The polarographic signals (arbitrary units) were detected by a Joliot-type electrode. Positive peaks indicate oxygen evolution, and negative peaks indicate uptake.

Comparing room temperature chlorophyll fluorescence in the wild type and the mutant (Table 2), a similar dark level fluorescence yield (F) was observed for both strains. Because state 2-state 1 transitions can be important for the determination of the maximum fluorescence yield (F; (28) ), cells were first illuminated with low intensity white light to induce state 1 prior to the addition of the electron transfer inhibitor 3,4-(dichlorophenyl)-1,1-dimethylurea to close photosystem II reaction centers. Under these conditions, the mutant showed a higher F value and hence a higher variable fluorescence yield (F). Consequently, the ratio of F/F, which is a measure of the photochemical efficiency of photosystem II, was slightly increased in the mutant (Table 2). Based on statistical analysis, this increase was significant. In search for further alterations in the antenna system of the mutant, low temperature fluorescence spectra were recorded. The 77 K fluorescence spectra of wild type and mutant strains obtained after chlorophyll a excitation at 440 nm are shown in Fig. 8A. The large emission peak at 717 nm is predominantly derived from photosystem I, whereas the two peaks at 685 nm and approximately 695 nm emanate from photosystem II. The latter two can be mainly attributed to the core antenna proteins CP43 (34) and CP47(35) , respectively. No difference in the relative amplitudes of the emission maxima were observed between both strains. When excited at a wavelength of 590 nm, which corresponds to the maximum for the excitation of phycobilins, the intensity of the emission at approximately 655 nm was considerably reduced in the mutant (Fig. 8B). This peak presumably represents overlapping emissions for phycocyanin and allophycocyanin with maxima at 645 and 665 nm, respectively. Because no difference in the phycocyanin/chlorophyll ratio was observed (data not shown), this result can be taken as an indication for a higher efficiency of excitation energy transfer from phycobilins to the photosystem II reaction center chlorophyll a in the mutant.

Figure 8: 77 K fluorescence emission spectra of Synechococcus sp. PCC7942 wild type (solid lines) or SY-SQDB mutant (broken lines) after excitation at 440 nm (A) or 590 nm (B). Spectra in A were normalized to the emission maximum at 717 nm, and spectra in B were normalized to 683 nm. The spectra in A were set off to facilitate comparison. In each case, chlorophyll concentrations were adjusted to 2.5 µg ml.

DISCUSSION

To study the possible role of sulfolipid in oxygenic photosynthesis in a definitive way, we created a sulfolipid-deficient null mutant of Synechococcus sp. PCC7942. During the course of this work, we isolated for the first time and disrupted a gene involved in sulfolipid biosynthesis in an organism with oxygenic photosynthesis. This gene of Synechococcus sp. PCC7942 shares considerable sequence identity with the sqdB gene of R. sphaeroides and is therefore also designated sqdB. However, further experiments will be required to demonstrate functional homology between the two genes in R. sphaeroides and Synechococcus sp. PCC7942. Our current inability to detect cross-hybridization between other sqd genes of the two bacterial strains suggests that these are less conserved. Unfortunately, we still do not know the function of the sqdB gene product, and further experiments to elucidate its biochemical role may also allow us to solve the long standing mystery of sulfolipid biosynthesis.

Inactivation of the putative sqdB gene of Synechococcus sp. PCC7942 wild type gives rise to an otherwise isogenic null mutant, which was designated SY-SQDB and completely lacks sulfolipid, one of the four polar lipids found in this bacterium. This deficiency has no lethal consequences. It does not even lead to reduced growth under optimal conditions for photoautotrophic growth (Fig. 5), suggesting that sulfolipid is not essential for oxygenic photosynthesis. Apparently, the loss of the anionic sulfolipid is mainly compensated by an increased relative amount of phosphatidylglycerol (Table 1), which is the second anionic lipid found in the membranes of Synechococcus sp. PCC7942. Maintaining a certain level of anionic lipids in the membranes seems to be crucial for the organism, because the reduction in phosphatidylglycerol under phosphate limitation in the wild type is compensated by an increased level of sulfolipid. The sulfolipid-deficient mutant SY-SQDB cannot respond in the same way to phosphate limitation and has to maintain a higher level of phosphatidylglycerol. Because it cannot replace lipid-bound phosphor by sulfur under conditions of phosphate limitation, it becomes phosphate-depleted and enters the stationary growth phase at an earlier time point than the wild type (Fig. 5). The same phenomenon has been previously observed for R. sphaeroides(15) . In addition, both bacteria accumulate dihexosyl lipids under phosphate limitation. Although Synechococcus sp. PCC7942 does not accumulate glucosylgalactosyl diacylglycerol, as was observed for phosphate-limited R. sphaeroides(16) , the relative amount of digalactosyl diacylglycerol is increased (Table 1).

Normal growth of the SY-SQDB mutant under optimal laboratory conditions does not exclude the possibility of a more subtle role of sulfolipid in oxygenic photosynthesis relevant under natural conditions, e.g. high photon flux densities. However, the light response curves for oxygen evolution by wild type and mutant cells were nearly identical (Fig. 6).

This finding indicates that the lack of sulfolipid neither affects the overall electron transport rate nor the optical cross-section of oxygen evolution. More subtle changes in the reaction kinetics of photosystem II were expected to become apparent by monitoring the characteristic period four oscillation pattern of flash-induced oxygen evolution in dark-adapted wild type and mutant cells. A comparison of oscillatory patterns revealed that both strains exhibit virtually the same features except for the pronounced oxygen uptake in the mutant sample after the first two flashes (Fig. 7B). Because hydrazine-treated mutant cells showed also a marked increase in oxygen uptake during the first four flashes, it seems most likely that the enhancement of oxygen uptake in the SY-SQDB mutant is not necessarily directly related to the water splitting activity of photosystem II. Instead, increased oxygen uptake could be either due to the reduction of O by components of the electron transport chain or increased respiratory activity. Nevertheless, the data presented in this study clearly show that sulfolipid is not an essential constituent of a functionally competent water oxidase.

Low temperature fluorescence measurements suggest that the lack of sulfolipid in the null mutant most likely has no effect on the structural organization of the reaction center/core antenna complex of photosystem II. The similarity of the emission spectra following chlorophyll a excitation at 440 nm (Fig. 8A) indicates that neither the binding environment of the chlorophyll a emitting from the core antenna proteins CP43 and CP47, nor the excitation energy transfer to the reaction center is affected in the mutant. Moreover, based on the 77 K fluorescence emission spectra following the excitation at 590 nm (Fig. 8B), it appears that excitation energy transfer from phycobilins to chlorophyll a of photosystem II reaction centers is increased. This finding can be explained in terms of structural modifications within the phycobilisome complex or an altered coupling between phycobilisomes and thylakoids. An increase in energy transfer from phycobilins to chlorophyll a may explain the increased variable chlorophyll fluorescence yield in the mutant observed during measurements of room temperature fluorescence (Table 2). Generally, the increase in the variable chlorophyll fluorescence yield in the mutant could arise from either an increased activity of photosystem II reaction centers or an increased number of photosystem II (26) as well as a decreased number of photosystem I reaction centers(36) . An altered number of reaction centers seems rather unlikely because neither differences in the pigment content nor in the low temperature chlorophyll fluorescence ratio of photosystem II to photosystem I were observed (Fig. 8A). Thus, photosystem II activity should be increased, and an elevated oxygen evolution rate under saturating light in the mutant would be expected. However, the maximal rate of oxygen evolution seems to be not increased in the mutant (Fig. 6). The enhanced light-induced oxygen uptake in the mutant observed during polarographic measurements with the Joliot-type electrode (Fig. 7) may be a reasonable explanation for this apparent discrepancy.

The subtle alterations in photosynthesis observed for the SY-SQDB mutant would not have been sufficient to isolate this mutant from a randomly mutagenized population. On the contrary, a leaky sulfolipid-deficient mutant of C. reinhardtii has been isolated based on its high fluorescence phenotype following random mutagenesis(17) . However, a detailed analysis of the photosynthetic characteristics of this mutant is not available for comparison. Furthermore, it has not clearly been demonstrated that the fluorescence phenotype and the lipid phenotype are indeed caused by the same genetic defect. Therefore further experiments will be required to test whether sulfolipid may play a different role in chloroplasts as compared with cyanobacterial cells.

In summary, the extensive examination of a sulfolipid-deficient null mutant of Synechococcus sp. PCC7942, suggests that sulfolipid does not play a specific role for oxygenic photosynthesis. A similar conclusion was drawn for nonoxygenic photosynthesis of R. sphaeroides(15) . However, subtle changes in the biochemistry of O and an increased variable room temperature chlorophyll fluorescence yield were observed for the cyanobacterial mutant. As was concluded for R. sphaeroides, the biosynthesis of sulfolipid may have evolved and been maintained during evolution, primarily not to provide an essential component for photosynthetic processes but to provide a surrogate anionic lipid for conditions of phosphate limitation. Further experiments with higher plants and algae will be required to answer the question of whether this concept is ubiquitous.

FOOTNOTES

*

This work was supported in part by Grant BMBF 0316301 A, Project 2, from the Genzentrum Berlin. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore by hereby marked ``advertisement'' in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank(TM)/EMBL Data Bank with accession number(s) U45308[GenBank].

§

To whom reprint requests should be addressed. Fax: 49-30-830007-36; benning{at}mpimg-berlin-dahlem.mpg.de.

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				J. E. Froehlich, C. Benning, and P. Dormann The Digalactosyldiacylglycerol (DGDG) Synthase DGD1 Is Inserted into the Outer Envelope Membrane of Chloroplasts in a Manner Independent of the General Import Pathway and Does Not Depend on Direct Interaction with Monogalactosyldiacylglycerol Synthase for DGDG Biosynthesis J. Biol. Chem., August 17, 2001; 276(34): 31806 - 31812. [Abstract] [Full Text] [PDF]

				R. M. Klug and C. Benning Two enzymes of diacylglyceryl-O-4'-(N,N,N,-trimethyl)homoserine biosynthesis are encoded by btaA and btaB in the purple bacterium Rhodobacter sphaeroides PNAS, May 8, 2001; 98(10): 5910 - 5915. [Abstract] [Full Text] [PDF]

				H. Hartel, P. Dormann, and C. Benning DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis PNAS, September 12, 2000; 97(19): 10649 - 10654. [Abstract] [Full Text] [PDF]

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