Research Article: Species-specific roles of sulfolipid metabolism in acclimation of photosynthetic microbes to sulfur-starvation stress

Date Published: October 12, 2017

Publisher: Public Library of Science

Author(s): Norihiro Sato, Ryohei Kamimura, Kodai Kaneta, Misato Yoshikawa, Mikio Tsuzuki, Franck Chauvat.


Photosynthetic organisms utilize sulfate for the synthesis of sulfur-compounds including proteins and a sulfolipid, sulfoquinovosyl diacylglycerol. Upon ambient deficiency in sulfate, cells of a green alga, Chlamydomonas reinhardtii, degrade the chloroplast membrane sulfolipid to ensure an intracellular-sulfur source for necessary protein synthesis. Here, the effects of sulfate-starvation on the sulfolipid stability were investigated in another green alga, Chlorella kessleri, and two cyanobacteria, Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. The results showed that sulfolipid degradation was induced only in C. kessleri, raising the possibility that this degradation ability was obtained not by cyanobacteria, but by eukaryotic algae during the evolution of photosynthetic organisms. Meanwhile, Synechococcus disruptants concerning sqdB and sqdX genes, which are involved in successive reactions in the sulfolipid synthesis pathway, were respectively characterized in cellular response to sulfate-starvation. Phycobilisome degradation intrinsic to Synechococcus, but not to Synechocystis, and cell growth under sulfate-starved conditions were repressed in the sqdB and sqdX disruptants, respectively, relative to in the wild type. Their distinct phenotypes, despite the common loss of the sulfolipid, inferred specific roles of sqdB and sqdX. This study demonstrated that sulfolipid metabolism might have been developed to enable species- or cyanobacterial-strain dependent processes for acclimation to sulfate-starvation.

Partial Text

Sulfoquinovosyl diacylglycerol (SQDG), which includes sulfoquinovose as a negatively charged head group, is conserved widely among oxygenic photosynthetic organisms (reviewed in e.g., [1]). This anionic lipid, which accounts for ca. 10–20 mole% of total cellular glycerolipids, contributes to construction of the membranes of chloroplasts in plants and their postulated ancestor, cyanobacteria, with predominant localization in their thylakoid membranes. The SQDG synthesis system in oxygenic photosynthetic organisms includes UDP-sulfoquinovose synthase (encoded by SQD1 in plants or sqdB in cyanobacteria) and SQDG synthase (encoded by SQD2 in plants or sqdX in cyanobacteria). These two enzymes catalyze successive reactions, i.e., the former combines sulfite and UDP-glucose for UDP-sulfoquinovose synthesis, and then the latter transfers the sulfoquinovose moiety of UDP-sulfoquinovose to diacylglycerol for SQDG synthesis. Interestingly, physiological characterization of SQDG-deficient mutants, including those disrupted in the above genes for SQDG synthesis, has thus far shown species-dependent roles of SQDG under normal growth conditions or even strain-dependent ones within species: e.g., SQDG is essential for cell growth in a cyanobacterium, Synechocystis sp. PCC 6803 (herein referred to as Synechocystis, [2]), but not in other oxygenic photoysnthetic organisms including cyanobacteria Synechococcus elongatus PCC 7942 (herein referred to as Synechococcus, [3]) and Synechococcus sp. PCC 7002 [4], a green alga, Chlamydomonas reinhardtii [5], and a seed plant, Arabidopsis thaliana [6]. Meanwhile, SQDG is required for the normal functionality of photosystem II in Synechocystis [2] and Chlamydomonas reinhardtii [7], but not in Synechococcus [3], Synechococcus sp. PCC 7002 [4] or Arabidopsis thaliana [6].

This study demonstrated that freshwater photosynthetic microbes, which might face S-deficiency, utilize the SQDG metabolism for acclimation to S-deficiency in species or even cyanobacterial-strain dependent manner. This situation, which is reminiscent of the species-dependent physiological significance of SQDG under S-replete conditions, is quite distinct from the universal role of SQDG to substitute for PG under P-deficient conditions. Our findings will be a foundation for a fuller understanding of the species-dependent mechanisms by which photosynthetic microbes acclimate to S-deficiency stress, and for consideration of their changes through evolution of photosynthetic organisms. In line, with our study as a starting point, it is expected that research on lipid role will change to include consideration of their dependency on the organism, and also on the respective genes for lipid synthesis in an organism.