Abstract
Understanding of sulfur metabolism has reached a new dimension with comprehension of its molecular regulation; however, knowledge underlining the evolutionary perspective and dynamics of this metabolism in cyanobacteria is still limited. In this review, we provided a comprehensive overview of sulfur metabolism with special emphasis on cyanobacteria and discussed the biosynthesis of cysteine and its downstream sulfur containing metabolites. Here, we invested efforts to understand the possible regulatory mechanisms of cyanobacterial sulfur assimilation process by comparing with that of other bacteria and plants. The impact of sulfur limitation on the morpho-physiological, biochemical, and molecular responses in cyanobacteria was also elucidated. The present work reflected that the cyanobacterial sulfur assimilatory pathway is identical to that of bacteria and plants since all of them employ similar enzymes in the process; however, the regulatory mechanism may vary in cyanobacteria. This communication comprehends the recent progresses made in the field of cyanobacterial sulfur metabolism research along with a comparative account of sulfur metabolism in some related organisms. Therefore, this review not only gives a broad overview on cyanobacterial sulfur metabolism but also increases our understanding of the importance and evolutionary perspective of this crucial metabolism.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABC:
-
ATP- binding cassette
- APS :
-
Adenosine-5′-phosphosulfate
- ATPS:
-
ATP sulfurylase
- CSC:
-
Cysteine synthase complex
- SAM:
-
S-adenosylmethionine
- STAS :
-
Sulphate Transporter and Anti-Sigma factor antagonist.
References
Aguilar-Barajas E, Díaz-Pérez C, Ramírez-Díaz MI, Riveros-Rosas H, Cervantes C (2011) Bacterial transport of sulfate, molybdate, and related oxyanions. Biometals 24:687–707. https://doi.org/10.1007/s10534-011-9421-x
Allen MM (1984) Cyanobacterial cell inclusions. Ann Rev Microbiol 38:1–25. https://doi.org/10.1146/annurev.mi.38.100184.000245
Antal TK, Lindblad P (2005) Production of H2 by sulfur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98:114–120. https://doi.org/10.1111/j.1365-2672.2004.02431.x
Ariño X, Ortega-Calvo JJ, Hernandez-Marine M, Saiz-Jimenez C (1995) Effect of sulfur starvation on the morphology and ultrastructure of the cyanobacterium Gloeothece sp. PCC 6909. Arch Microbiol 163:447–453. https://doi.org/10.1007/BF00272134
Awazuhara M, Fujiwara T, Hayashi H (2005) The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Physiol Plant 125:95–105. https://doi.org/10.1111/j.1399-3054.2005.00543.x
Bácsi I, Vasas G, Surányi G, M-Hamvas M, Máthé C, Tóth E, Grigorszky I, Gáspár A, Tóth S, Borbely G (2006) Alteration of cylindrospermopsin production in sulfate-or phosphate-starved cyanobacterium Aphanizomenon ovalisporum. FEMS Microbiol Lett 259:303–310. https://doi.org/10.1111/j.1574-6968.2006.00282.x
Baebprasert W, Lindblad P, Incharoensakdi A (2010) Response of H2 production and Hox-hydrogenase activity to external factors in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrogen Energy 35:6611–6616. https://doi.org/10.1016/j.ijhydene.2010.04.047
Barber J, Gounaris K (1986) What role does sulfolipid play within the thylakoid membrane? Photosyn Res 9:239–249. https://doi.org/10.1007/BF00029747
Barberon M, Berthomieu P, Clairotte M, Shibagaki N, Davidian JC, Gosti F (2008) Unequal functional redundancy between the two Arabidopsis thaliana high‐affinity sulphate transporters SULTR1; 1 and SULTR1; 2. New Phytol 180:608–619. https://doi.org/10.1111/j.1469-8137.2008.02604.x
Bhati R, Samantaray S, Sharma L, Mallick N (2010) Poly-β-hydroxybutyrate accumulation in cyanobacteria under photoautotrophy. Biotechnol J 5:1181–1185. https://doi.org/10.1002/biot.201000252
Biedlingmaier S, Schmidt A (1987) Uptake and utilization of sulfonic acids in the cyanobacterial strains Anabaena variabilis and Plectonema 73110. Z Naturforsch 42:891–896. https://doi.org/10.1515/znc-1987-7-827
Bochenek M, Etherington GJ, Koprivova A, Mugford ST, Bell TG, Malin G, Kopriva S (2013) Transcriptome analysis of the sulfate deficiency response in the marine microalga Emiliania huxleyi. New Phytol 199:650–662. https://doi.org/10.1111/nph.12303
Brunold C, Suter M (1984) Regulation of sulfate assimilation by nitrogen nutrition in the duckweed Lemna minor L. Plant Physiol 76:579–583. https://doi.org/10.1104/pp.76.3.579
Bryant DA, Liu ZF (2013) Green bacteria: insights into green bacterial evolution through genomic analyses. In: Beatty JT (ed) Genome evolution of photosynthetic bacteria. Advances in botanical research. Academic Press, San Diego, pp 99–150
Bykowski T, Ploeg JR, Iwanicka-Nowicka R, Hryniewicz MM (2002) The switch from inorganic to organic Sulphur assimilation in Escherichia coli: adenosine 5′-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol Microbiol 43:1347–1358. https://doi.org/10.1046/j.1365-2958.2002.02846.x
Byrne CR, Monroe RS, Ward KA, Kredich NM (1988) DNA sequences of the cysK regions of Salmonella typhimurium and Escherichia coli and linkage of the cysK regions to ptsH. J Bacteriol 170:3150–3157. https://doi.org/10.1128/jb.170.7.3150-3157.1988
Callow ME, Evans LV (1979) Polyphosphate accumulation in Sulphur-starved cells of Rhodella maculata. Br Phycol J 14:27–37. https://doi.org/10.1080/00071617900650361
Churchill ME, Suzuki M (1989) 'SPKK' motifs prefer to bind to DNA at A/T-rich sites. EMBO J 8:4189–4195
Collier JL, Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174:4718–4726. https://doi.org/10.1002/j.1460-2075.1989.tb08604.x
Collier JL, Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047. https://doi.org/10.1002/j.1460-2075.1994.tb06352.x
Couturier J, Jacquot JP, Rouhier N (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell Mol Life Sci 66:2539–2557. https://doi.org/10.1007/s00018-009-0054-y
Couturier J, Ströher E, Albetel AN, Roret T, Muthuramalingam M, Tarrago L, Seidel T, Tsan P, Jacquot JP, Johnson MK, Dietz KJ (2011) Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J Biol Chem 286:27515–27527. https://doi.org/10.1074/jbc.M111.228726
Davidian JC, Kopriva S (2010) Regulation of sulfate uptake and assimilation - the same or not the same? Mol Plant 3:314–325. https://doi.org/10.1093/mp/ssq001
Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas reinhardtii with aberrant responses to sulfur deprivation. Plant Cell 6:53–63. https://doi.org/10.1105/tpc.6.1.53
Davies JP, Yildiz FH, Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150–2159. https://doi.org/10.1002/j.1460-2075.1996.tb00568.x
Davies JP, Grossman AR (1998) Responses to deficiencies in macronutrients. In: Rochaix J-D, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers p, Dordrecht, The Netherlands, pp 613–635
Davies JP, Yildiz FH, Grossman AR (1999) Sac3, an Snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11:1179–1190. https://doi.org/10.1105/tpc.11.6.1179
Di Cesare A, Cabello-Yeves PJ, Chrismas NA, Sánchez-Baracaldo P, Salcher MM, Callieri C (2018) Genome analysis of the freshwater planktonic Vulcanococcus limneticus sp. nov. reveals horizontal transfer of nitrogenase operon and alternative pathways of nitrogen utilization. BMC Genomics 19:259. https://doi.org/10.1186/s12864-018-4648-3
Diessner W, Schmidt A (1981) Isoenzymes of cysteine synthase in the cyanobacterium Synechococcus 6301. Z Pflanzenphysiol 102:57–68. https://doi.org/10.1016/S0044-328X(81)80217-6
El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian J (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241. https://doi.org/10.1104/pp.106.091462
Fernandez-Gonzalez N, Sierra-Alvarez R, Field JA, Amils R, Sanz JL (2019) Adaptation of granular sludge microbial communities to nitrate, sulfide, and/or p-cresol removal. Int Microbiol 22:305–316. https://doi.org/10.1007/s10123-018-00050-4
Gekeler W, Grill E, Winnacker EL, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol 150:197–202. https://doi.org/10.1007/BF00425162
Giddings TH Jr, Wolk CP, Shomer-Ilan A (1981) Metabolism of sulfur compounds by whole filaments and heterocysts of Anabaena variabilis. J Bacteriol 146:1067–1074. https://doi.org/10.1128/JB.146.3.1067-1074.1981
Gill BC, Lyons TW, Saltzman MR (2007) Parallel, high-resolution carbon and sulfur isotope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeogr Palaeoclimatol Palaeoecol 256:156–173. https://doi.org/10.1016/j.palaeo.2007.02.030
Gill BC, Lyons TW, Young S, Kump L, Knoll AH, Saltzman MR (2011) Geochemical evidence for widespread euxinia in the Later Cambrian ocean. Nature 469:80–83. https://doi.org/10.1038/nature09700
Giordano M, Pezzoni V, Hell R (2000) Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol 124:857–864. https://doi.org/10.1104/pp.124.2.857
Giordano M, Raven JA (2014) Nitrogen and sulfur assimilation in plants and algae. Aqua Bot 118:45–61. https://doi.org/10.1016/j.aquabot.2014.06.012
Giordano M, Norici A, Hell R (2005) Tansley review. Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–382. https://doi.org/10.1111/j.1469-8137.2005.01335.x
Giordano M, Norici A, Ratti S, Raven JA (2008) Role of sulfur for algae: acquisition, metabolism, ecology and evolution. In: Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, pp 397–415. https://doi.org/10.1007/978-1-4020-6863-8_20
Giordano M, Pezzoni V, Hell R (2013) Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol 124:857–864. https://doi.org/10.1104/pp.124.2.857
Gleason FK (1994) Thioredoxins in cyanobacteria: structure and redox regulation of enzyme activity. In The Molecular Biology of Cyanobacteria (pp. 715–729). Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0227-8_24
Green LS, Grossman AR (1988) Changes in sulfate transport characteristics and protein composition of Anacystis nidulans R2 during sulfate deprivation. J Bacteriol 170:583–587. https://doi.org/10.1128/jb.170.2.583-587.1988
Green LS, Laudenbach DE, Grossman AR (1989) A region of a cyanobacterial genome required for sulfate transport. Proc Natl Acad Sci 86:1949–1953. https://doi.org/10.1073/pnas.86.6.1949
Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Nat Acad Sci 86:6838–6842. https://doi.org/10.1073/pnas.86.18.6838
Guédon E, Martin-Verstraete I (2006) Cysteine metabolism and its regulation in Bacteria. Microbiol Monogr:1–24. https://doi.org/10.1007/7171_2006_060
Günal S, Hardman R, Kopriva S, Mueller JW (2019) Sulfation pathways from red to green. J Biol Chem 294:12293–12312. https://doi.org/10.1074/jbc.REV119.007422
Gutu A, Alvey RM, Bashour S, Zingg D, Kehoe DM (2011) Sulfate-driven elemental sparing is regulated at the transcriptional and posttranscriptional levels in a filamentous cyanobacterium. J Bacteriol 193:1449–1460. https://doi.org/10.1128/JB.00885-10
Habicht KS, Gade M, Thamdrup B, Berg P, Canfield DE (2002) Calibration of sulfate levels in the Archean ocean. Science 298:2372–2374. https://doi.org/10.1126/science.1078265
Hai T, Hein S, Steinbüchel A (2001) Multiple evidence for widespread and general occurrence of type-III PHA synthases in cyanobacteria and molecular characterization of the PHA synthases from two thermophilic cyanobacteria: Chlorogloeopsis fritschii PCC 6912 and Synechococcus sp. strain MA19. Microbiology 147:3047–3060. https://doi.org/10.1099/00221287-147-11-3047
Harwood JL, Okanenko AA (2003) Sulphoquinovosyl diacylglycerol (SQDG)-the sulpholipid of higher plants. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Springer, Dordrecht, pp 189–219. https://doi.org/10.1007/978-94-017-0289-8_11
Hesse H, Nikiforova V, Gakière B, Hoefgen R (2004) Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. J Exp Bot 55:1283–1292. https://doi.org/10.1093/jxb/erh136
Hifney AF, Abdel-Basset R (2014) Induction of hydrogen evolution in Nostoc spp. by nitrogen and/or sulphur deficiency. Int J Curr Microbiol App Sci 3:1028–1044
Hirai MY, Saito K (2004) Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur deficiency. J Exp Bot 55:1871–1879. https://doi.org/10.1093/jxb/erh184
Hirai K, Nojo M, Sato Y, Tsuzuki M, Sato N (2019) Contribution of protein synthesis depression to poly-β-hydroxybutyrate accumulation in Synechocystis sp. PCC 6803 under nutrient-starved conditions. Sci Rep 9:1–0. https://doi.org/10.1038/s41598-019-56520-w
Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant132:190–198. https://doi.org/10.1111/j.1399-3054.2007.01012.x
Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw Biol 46:431–451. https://doi.org/10.1046/j.1365-2427.2001.00687.x
Hopkins L, Parmar S, Błaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433–440. https://doi.org/10.1104/pp.104.057521
Howarth JR, Parmar S, Barraclough PB, Hawkesford MJ (2009) A Sulphur deficiency-induced gene sdi1, involved in the utilization of stored sulphate pools under sulphur-limiting conditions has potential as a diagnostic indicator of sulphur nutritional status. Plant Biotechnol J 7:200–209. https://doi.org/10.1111/j.1467-7652.2008.00391.x
Howe G, Merchant S (1992) Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol 98:127–136. https://doi.org/10.1104/pp.98.1.127
Hryniewicz MM, Kredich NM (1991) The cysP promoter of Salmonella typhimurium: characterization of two binding sites for CysB protein, studies of in vivo transcription initiation, and demonstration of the anti-inducer effects of thiosulfate. J Bacteriol 173:5876–5886. https://doi.org/10.1128/jb.173.18.5876-5886.1991
Hughes AR, Sulesky A, Andersson B, Peers G (2018) Sulfate amendment improves the growth and bioremediation capacity of a cyanobacteria cultured on municipal wastewater centrate. Algal Res 32:30–37. https://doi.org/10.1016/j.algal.2018.03.004
Iwanicka-Nowicka R, Hryniewicz MM (1995) A new gene, cbl, encoding a member of the LysR family of transcriptional regulators belongs to Escherichia coli cys regulon. Gene 166:11–17. https://doi.org/10.1016/0378-1119(95)00606-8
Jeanjean R, Broda E (1977) Dependence of suifate uptake by Anacystis nidulanson energy, on osmotic shock and on sulfate starvation. Arch Microbiol 114:19–23. https://doi.org/10.1007/BF00429625
Jensen TE, Rachlin JW (1984) Effect of varying sulfur deficiency on structural components of a cyanobacterium Synechococcus leopoliensis: a morphometric study. Cytobios 42:35–46. https://doi.org/10.1007/BF00413264
Kah LC, Lyons TW, Frank TD (2004) Low marine sulphate and protracted oxygenation of the Proterozoic biosphere. Nature 431:834–838. https://doi.org/10.1038/nature02974
Kaneko T, Sato S, Kotani H, Tanaka A (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136. https://doi.org/10.1093/dnares/3.3.10
Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-to-shoot transport of sulfate in Arabidopsis: evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204. https://doi.org/10.1104/pp.104.045625
Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704. https://doi.org/10.1105/tpc.104.023960
Kaur G, Chandna R, Pandey R, Abrol YP, Iqbal M, Ahmad A (2011) Sulfur starvation and restoration affect nitrate uptake and assimilation in rapeseed. Protoplasma 248:299–311. https://doi.org/10.1007/s00709-010-0171-3
Kharwar S, Mishra AK (2020) Unraveling the complexities underlying sulfur deficiency and starvation in the cyanobacterium Anabaena sp. PCC 7120. Environ Exp Bot:103966. https://doi.org/10.1016/j.envexpbot.2019.103966
Kharwar S, Bhattacharjee S, Mishra AK (2021) Disentangling the impact of sulfur limitation on exopolysaccharide and functionality of Alr2882 by in silico approaches in Anabaena sp. PCC 7120. Appl Biochem Biotechnol:1–22. https://doi.org/10.1007/s12010-021-03501-3
Kiyota H, Ikeuchi M, Hirai MK (2012) Response of amino acid metabolism to sulfur starvation in Synechocystis sp. PCC 683. In: Sulfur metabolism in plants. Springer, Dordrecht, Netherlands pp 53-59. https://doi.org/10.1007/978-94-007-4450-9_6
Kiyota H, Hirai M, Ikeuchi M (2014) NblA1/A2-dependent homeostasis of amino acid pools during nitrogen starvation in Synechocystis sp. PCC 6803. Metabolites 4:517–531. https://doi.org/10.3390/metabo4030517
Klanchui A, Dulsawat S, Chaloemngam K, Cheevadhanarak S, Prommeenate P, Meechai A (2018) An improved genome-scale metabolic model of Arthrospira platensis C1 (iAK888) and its application in glycogen overproduction. Metabolites 8:84. https://doi.org/10.3390/metabo8040084
Kohn C, Schumann J (1993) Nucleotide sequence and homology comparison of two genes of the sulfate transport operon from the cyanobacterium Synechocystis sp. PCC6803. Plant Mol Biol 21:409–412. https://doi.org/10.1074/jbc.M112.392407
Kolesinski P, Rydzy M, Szczepaniak A (2017) Is RAF1 protein from Synechocystis sp. PCC 6803 really needed in the cyanobacterial Rubisco assembly process? Photosynth Res 132:135–148. https://doi.org/10.1007/s11120-017-0336-4
Kopriva S, Koprivova A (2004) Plant adenosine 5 phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783. https://doi.org/10.1093/jxb/erh18
Kopriva S, Büchert T, Fritz G, Suter M, Benda R, Schünemann V, Koprivova A, Schürmann P, Trautwein AX, Kroneck PM, Brunold C (2002) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation. J Biol Chem 277:21786–21791. https://doi.org/10.1074/jbc.M202152200
Krämer E, Schmidt A (1989) Nitrite accumulation by Synechococcus 6301 as a consequence of carbon or sulfur deficiency. FEMS Microbiol Lett 59:191–196. https://doi.org/10.1111/j.1574-6968.1989.tb03108.x
Kredich NM (1966) Biosynthesis of cysteine. Cellular and molecular biology. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB et al (eds) Escherichia coli and Salmonella typhimurium. Washington, DC, ASM Press, pp 514–27
Kredich NM, Becker MA, Tomkins GM (1969) Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 244:2428–2439. https://doi.org/10.1016/S0021-9258(19)78241-6
Ksionzek KB, Lechtenfeld OJ, McCallister SL, Schmitt-Kopplin P, Geuer JK, Geibert W, Koch BP (2016) Dissolved organic sulfur in the ocean: biogeochemistry of a petagram inventory. Science 354:456–459. https://doi.org/10.1126/science.aaf7796
Kumaresan V, Nizam F, Ravichandran G, Viswanathan K, Palanisamy R, Bhatt P, Arasu MV, Al-Dhabi NA, Mala K, Arockiaraj J (2017) Transcriptome changes of blue-green algae, Arthrospira sp. in response to sulfate stress. Algal Res 23:96–103. https://doi.org/10.1016/j.algal.2017.01.012
Kyndiah O, Rai AN (2006) Induction of sporulation by sulphate limitation in Nostoc ANTH, a symbiotic strain capable of colonizing roots of rice plants. Ind J Biotechnol 6:57–62
Lass B, Ullrich-Eberius CI (1984) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53–60. https://doi.org/10.1007/BF00951460
Laudenbach DE, Grossman AR (1991) Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport. J Bacteriol 173:2739–2750. https://doi.org/10.1128/jb.173.9.2739-2750.1991
Laudenbach DE, Ehrhardt D, Green L, Grossman A (1991) Isolation and characterization of a sulfur-regulated gene encoding a periplasmically localized protein with sequence similarity to rhodanese. J Bacteriol 173:2751–2760. https://doi.org/10.1128/jb.173.9.2751-2760.1991
Lawry NH, Jensen TE (1979) Deposition of condensed phosphate as an effect of varying sulfur deficiency in the cyanobacterium Synechococcus sp. (Anacystis nidulans). Arch Microbiol 120:1–7. https://doi.org/10.1007/BF00413264
Lawry NH, Jensen TE (1986) Condensed phosphate deposition, sulfur amino acid use, and unidirectional transsulfuration in Synechococcus leopoliensis. Arch Microbiol 144:317–323. https://doi.org/10.1007/BF00409879
Lawry NH, Simon RD (1982) The normal and induced occurrence of cyanophycin inclusion bodies in several blue-green algae. J Phycol 18:391–399. https://doi.org/10.1111/j.1529-8817.1982.tb03201.x
Li H, Outten CE (2012) Monothiol CGFS glutaredoxins and BolA-like proteins: [2Fe-2S] binding partners in iron homeostasis. Biochemistry 51:4377–4389. https://doi.org/10.1021/bi300393z
Lindberg P, Melis A (2008) The chloroplast sulfate transport system in the green alga Chlamydomonas reinhardtii. Planta 228:951–961. https://doi.org/10.1007/s00425-008-0795-0
Lindblad P (1999) Cyanobacterial H2 metabolism: knowledge and potential/strategies for a photobiotechnological production of H2. Biotechnol Appl 16:141–144. https://doi.org/10.1007/s00425-003-1113-5
Long BM (2010) Evidence that sulfur metabolism plays a role in microcystin production by Microcystis aeruginosa. Harmful Algae 9:74–81. https://doi.org/10.1016/j.hal.2009.08.003
Lowenstein TK, Hardie LA, Timofeeff MN, Demicco RV (2003) Secular variation in seawater chemistry and the origin of calcium chloride basinal brines. Geol 31:857–860. https://doi.org/10.1130/G19728R.1
Ludwig M, Bryant DA (2012) Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol 3:145. https://doi.org/10.3389/fmicb.2012.00145
Lyubetsky VA, Seliverstov AV, Zverkov OA (2013) Transcription regulation of plastid genes involved in sulfate transport in Viridiplantae. Bio Med Res Inter 2013:6. https://doi.org/10.1155/2013/413450
Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J. https://doi.org/10.1111/j.1365-313X.2005.02363.x
Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trend Plant Sci 4:130–135. https://doi.org/10.1016/S1360-1385(99)01387-4
Melis A, Chen HC (2005) Chloroplast sulfate transport in green algae - genes, proteins and effects. Photosynth Res 86:299–307. https://doi.org/10.1007/s11120-005-7382-z
Menon VKN, Varma AK (1978) Adenosine 5′-triphosphate sulphurilase from Spirulina platensis. Experientia 35:854–855. https://doi.org/10.1007/BF01955107
Meyer J (2008) Iron-sulfur protein folds, iron-sulfur chemistry, and evolution. J Biol Inorg Chem 13:157–170. https://doi.org/10.1007/s00775-007-0318-7
Migge A, Bork C, Hell R, Becker TW (2000) Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur deprived tobacco. Planta 211:587–595. https://doi.org/10.1007/s004250000322
Monshupanee T, Incharoensakdi A (2016) Enhanced accumulation of glycogen, lipids and polyhydroxybutyrate under optimal nutrients and light intensities in the cyanobacterium Synechocystis sp. PCC 6803. J Appl Microbiol 116:830–838. https://doi.org/10.1111/jam.12409
Müller S, Schmidt A (1986) Substrate-Dependent Arylsulfatase Activity in the Cyanobacterium Plectonema 73110. Z Naturforsch 41c:820–824. https://doi.org/10.1515/znc-1986-9-1004
Narainsamy K, Farci S, Braun E, Junot C, Cassier-Chauvat C, Chauvat F (2016) Oxidative-stress detoxification and signalling in cyanobacteria: the crucial glutathione synthesis pathway supports the production of ergothioneine and ophthalmate. Mol Microbiol 100:15–24. https://doi.org/10.1111/mmi.13296
Nicholson ML, Laudenbach DE (1995) Genes encoded on a cyanobacterial plasmid are transcriptionally regulated by sulfur availability and CysR. J Bacteriol 177:2143–2150. https://doi.org/10.1128/jb.177.8.2143-2150.1995
Nicholson ML, Gaasenbeek M, Laudenbach DE (1995) Two enzymes together capable of cysteine biosynthesis are encoded on a cyanobacterial plasmid. Mol Gen Genet 247:623–632. https://doi.org/10.1007/BF00290354
Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650
Nishihara A, Haruta S, McGlynn SE, Thiel V, Matsuura K (2018) Nitrogen fixation in thermophilic chemosynthetic microbial communities depending on hydrogen, sulfate, and carbon dioxide. Microbes Environ 33:10-18. https://doi.org/10.1264/jsme2.ME17134
Ortega-Calvo JJ, Stal LJ (1994) Sulphate-limited growth in the N2-fixing unicellular cyanobacterium Gloeothece (Nageli) sp. PCC 6909. New Phytol 128:273–281. https://doi.org/10.1111/j.1469-8137.1994.tb04011.x
Ostrowski J, Wu JY, Rueger DC, Miller BE, Siegel LM, Kredich NM (1989) Characterization of the cysJIH regions of Salmonella typhimurium and Escherichia coli B. DNA sequences of cysI and cysH and a model for the siroheme-Fe4S4 active center of sulfite reductase hemoprotein based on amino acid homology with spinach nitrite reductase. J Biol Chem 264:15726–15737
Pardee AB, Prestidge LS, Whipple MB (1966) A binding site for sulfate and its relation to sulfate transport into Salmonella typhimurium. J Biol Chem 241:3962–3969. https://doi.org/10.1016/S0021-9258(18)99799-1
Parra F, Britton P, Castle C, Jones-Mortimer MC, Kornberg HL (1983) Two separate genes involved in sulphate transport in Escherichia coli K12. Microbiol 129:357–358. https://doi.org/10.1099/00221287-129-2-357
Parry J, Clark DP (2002) Identification of a CysB-regulated gene involved in glutathione transport in Escherichia coli. FEMS Microbiol Lett 209:81–85. https://doi.org/10.1111/j.1574-6968.2002.tb11113.x
Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evolu Biol 8:1–4. https://doi.org/10.1186/1471-2148-8-39
Patzer SI, Hantke K (1999) SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J Bacteriol 181:3307–3309. https://doi.org/10.1128/JB.181.10.3307-3309.1999
Petrychenko OY, Peryt TMT, Chechel EI (2005) Early Cambrian seawater chemistry from fluid inclusions in halite from Siberian evaporites. Chem Geol 219:149–161. https://doi.org/10.1016/j.chemgeo.2005.02.003
Pootakham W, Gonzalez-Ballester D, Grossman AR (2010) Identification and regulation of plasma membrane sulfate transporters in Chlamydomonas. Plant Physiol 153:1653–1668. https://doi.org/10.1104/pp.110.157875
Prioretti L, Gontero B, Hell R, Giordano M (2014) Diversity and regulation of ATP sulfurylase in photosynthetic organisms. Front Plant Sci 5:597. https://doi.org/10.3389/fpls.2014.00597
Prosser IM, Schneider A, Hawkesford MJ, Clarkson DT (1997) Changes in nutrient composition, metabolite concentrations and enzyme activities in spinach in the early stages of S-deprivation. Sulphur metabolism in higher plants: molecular, ecophysiological and nutritional aspects. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulphur metabolism in higher plants. Backhuys Publishers, Leiden The Netherlands, pp 339–342
Prosser IM, Purves JV, Saker LR, Clarkson DT (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J Exp Bot 52:113–121. https://doi.org/10.1093/jxb/52.354.113
Ratti S, Knoll AH, Giordano M (2011) Did sulfate availability facilitate the evolutionary expansion of chlorophyll a+ c phytoplankton in the oceans? Geobiology 9:301–312. https://doi.org/10.1111/j.1472-4669.2011.00284.x
Ratti S, Knoll AH, Giordano M (2013) Grazers and phytoplankton growth in the oceans: an experimental and evolutionary perspective. PLoS One 8:e77349. https://doi.org/10.1371/journal.pone.0077349
Ravilious GE, Nguyen A, Francois JA, Jez JM (2012) Structural basis and evolution of redox regulation in plant adenosine-5′-phosphosulfate kinase. Proc Natl Acad Sci 109:309–314. https://doi.org/10.1073/pnas.1115772108
Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies JP (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and post trascriptional control of cysteine biosynthesis. Plant Physiol 130:2076–2084. https://doi.org/10.1104/pp.012484
Richaud C, Zabulon G, Joder A, Thomas JC (2001) Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. J Bacteriol 183:2989–2994. https://doi.org/10.1128/JB.183.10.2989-2994.2001
Riemenschneider A, Riedel K, Hoefgen R, Papenbrock J, Hesse H (2005) Impact of reduced O-acetylserine (thiol) lyase isoform contents on potato plant metabolism. Plant Physiol 137:892–900. https://doi.org/10.1104/pp.104.057125
Ritchie RJ (1996) Sulphate transport in the cyanobacterium Synechococcus R2 (Anacystis nidulens, S. leopolensis) PCC 7942. Plant Cell Environ 19:1307–1315. https://doi.org/10.1111/j.1365-3040.1996.tb00009.x
Rouhier N, Couturier J, Johnson MK, Jacquot JP (2010) Glutaredoxins: roles in iron homeostasis. Trends Biochem Sci 35:43–52. https://doi.org/10.1016/j.tibs.2009.08.005
Ruiz FA, Marchesini N, Seufferheld M, Docampo R (2001) The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 276:46196–46203. https://doi.org/10.1074/jbc.M105268200
Saito K (2004) Sulfur assimilatory metabolism. The Long and smelling road. Plant Cell Physiol 136:2443–2450. https://doi.org/10.1104/pp.104.046755
Samantaray S, Mallick N (2015) Impact of various stress conditions on poly-β-hydroxybutyrate (PHB) accumulation in Aulosira fertilissima CCC 444. Curr Biotechnol 4:366–372. https://doi.org/10.2174/2211550104666150806000642
Sato N (2004) Roles of the acidic lipids sulfoquinovosyldeacylglycerol and phosphotadylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505. https://doi.org/10.1007/s10265-004-0183-1
Sato N, Sonoike K, Tsuzuk M, Kawaguchi A (1995) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234:16–23. https://doi.org/10.1111/j.1432-1033.1995.016_c.x
Sato N, Aoki M, Maru Y, Sonoike K, Minoda A, Tsuzuki M (2003a) Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 217:245–251. https://doi.org/10.1007/s00425-003-0992-9
Sato N, Sugimoto K, Meguro A, Tsuzuki M (2003b) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phylogeny. DNA Res 10:229–237. https://doi.org/10.1093/dnares/10.6.229
Sato N, Suda K, Tsuzuki M (2004) Responsibility of phosphatidylglycerol for biogenesis of the PSI complex. Biochim Biophys Acta 1658:235–243. https://doi.org/10.1016/j.bbabio.2004.06.008
Sato N, Kamimura R, Kaneta K, Yoshikawa M, Tsuzuki M (2017) Species-specific roles of sulfolipid metabolism in acclimation of photosynthetic microbes to sulfur-starvation stress. PLoS One 12:e0186154. https://doi.org/10.1371/journal.pone.0186154
Schmidt A (1977a) Assimilatory sulfate reduction via 3′-phosphoadenosine-5′-phosphosulfate (PAPS) and adenosine-5′-phosphosulfate (APS) in blue-green algae. FEMS Microbiol Lett 1:137–140. https://doi.org/10.1111/j.1574-6968.1977.tb00599.x
Schmidt A (1977b) Exchange of cysteine-bound sulfide with free sulfide and cysteine synthase activity in Chlorella pyrenoidosa. Z Naturf C 84:435–446. https://doi.org/10.1016/S0044-328X(77)80235-3
Schmidt A (1979) Photosynthetic assimilation of sulfur compounds. In: Gibbs M, Latzko E (eds) Encyclopedia of plant physiology. Springer-Verlag, Berlin, pp 481–496. https://doi.org/10.1007/978-3-642-67242-2_37
Schmidt A (1988) [62] Sulfur metabolism in cyanobacteria. Methods in Enzymology.167:572–583. https://doi.org/10.1016/0076-6879(88)67065-0
Schmidt A, Christen U (1978) A factor-dependent sulfotransferase specific for 3′-phosphoadenosine-5′-phosphosulfate (PAPS) in the cyanobacterium Synechococcus 6301. Planta 140:239–244. https://doi.org/10.1007/BF00390254
Schmidt A, Jäger K (1992) Open questions about sulfur metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 43:325–349. https://doi.org/10.1146/annurev.pp.43.060192.001545
Schmidt A, Erdle I, Köst HP (1982) Changes of C-Phycocyanin in Synechococcus 6301 in relation to growth on various sulfur compounds materials and methods. Z Naturf 37:870–876. https://doi.org/10.1515/znc-1982-1004
Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514. https://doi.org/10.1099/mic.0.27883-0
Schwarz R, Grossman AR (1998) A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proc Natl Acad Sci 95:11008–11013. https://doi.org/10.1073/pnas.95.18.11008
Sekowska A, Kung HF, Danchin A (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2:145–177
Selstam E, Campbell D (1996) Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus sp. PCC 7421, which lacks sulfoquinovosyl diacylglycerol. Arch Microbiol 166:132–135. https://doi.org/10.1007/s002030050367
Shibagaki N, Grossman AR (2008) The state of sulfur metabolism in algae: from ecology to genomics. Hell R, Dahl C, Knaff D, Leustek T (eds) Advances in photosynthesis and respiration: sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 231-267. https://doi.org/10.1007/978-1-4020-6863-8_13
Siegel LM, Davis PS (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of Enterobacteria. IV The Escherichia coli hemoflavoprotein: subunit structure and dissociation into hemoprotein and flavoprotein components. J Biol Chem 249:1587–1598. https://doi.org/10.1016/S0021-9258(19)42922-0
Siegel LM, Murphy MJ, Kamin H (1973) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. I The Escherichia coli hemoflavoprotein: molecular parameters and prosthetic groups. J Biol Chem 248:251–261. https://doi.org/10.1016/S0021-9258(19)44469-4
Siegel LM, Davis PS, Kamin H (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of Enterobacteria. III The Escherichia coli hemoflavoprotein: catalytic parameters and the sequence of electron flow. J Biol Chem 249:1572–1586. https://doi.org/10.1016/S0021-9258(19)42921-9
Singh SP, Klisch M, Sinha RP, Häder DP (2010) Sulfur deficiency changes mycosporine-like amino acid (MAA) composition of Anabaena variabilis PCC 7937: a possible role of sulfur in MAA bioconversion. Photochem Photobiol 86:862–870. https://doi.org/10.1111/j.1751-1097.2010.00736.x
Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995a) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci 92:9373–9377. https://doi.org/10.1073/pnas.92.20.9373
Smith FW, Hawkesford MJ, Prosser IM, Clarkson DT (1995b) Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high-affinity sulfate transporter at the plasma-membrane. Mol Gen Genet 247:709–715. https://doi.org/10.1007/BF00290402
Suzuki M, Gerstein M, Johnson T (1993) An NMR study on the DNA-binding SPKK motif and a model for its interaction with DNA. Protein Eng:565–574. https://doi.org/10.1093/protein/6.6.565
Takahashi H (2010) Regulation of sulfate transport and assimilation in plants. Int Rev Cell Mol Biol 281:129–159. https://doi.org/10.1016/S1937-6448(10)81004-4
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, de Almeida EJ, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci 94:11102–11107. https://doi.org/10.1073/pnas.94.20.11102
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The role of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J 23:171–182. https://doi.org/10.1046/j.1365-313x.2000.00768.x
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184. https://doi.org/10.1146/annurev-arplant-042110-103921
Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu SH (2012) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:119. https://doi.org/10.3389/fpls.2011.00119
Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180
Thomas MD (1958) Assimilation of sulfur and physiology of essential S-compounds. Encyclopedia of Plant Physiology IX, pp37–63
Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci 104:18807–18812. https://doi.org/10.1073/pnas.0706373104
Tsang MLS, Schiff JA (1975) Studies of sulfate utilization by alage. 14. Distribution of adenosine 5′- phosphosulfate (APS) and adenosine 3′ phosphate 5′- phosphosulfate (PAPS) sulfotransferases in assimilatory sulfate reducers. Plant Sci Lett 4:301–307. https://doi.org/10.1016/0304-4211(75)90102-9
Utkilen HC (1982) Magnesium-limited growth of the cyanobacterium Anacystis nidulans. Microbiology 28:1849–1862. https://doi.org/10.1099/00221287-128-8-1849
Utkilen HC, Heldal M, Knutsen G (1976) Characterization of sulfate uptake in Anacystis nidulans. Plant Physiol 38:217–220. https://doi.org/10.1111/j.1399-3054.1976.tb03993.x
Van Der Ploeg JR, Barone M, Leisinger T (2001) Expression of the Bacillus subtilis sulphonate-sulphur utilization genes is regulated at the levels of transcription initiation and termination. Mol Microbiol 39:1356–1136. https://doi.org/10.1111/j.1365-2958.2001.02327.x
Vasilikiotis C, Melis A (1994) Photosystem II reaction center damage and repair cycle: chloroplast acclimation strategy to irradiance stress. Proc Natl Acad Sci 91:7222–7226. https://doi.org/10.1073/pnas.91.15.7222
Warshan D, Espinoza JL, Stuart RK, Richter RA, Kim SY, Shapiro N, Woyke T, Kyrpides NC, Barry K, Singan V, Lindquist E (2017) Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis. ISME J 11:2821–2833. https://doi.org/10.1038/ismej.2017.134
Warshan D, Liaimer A, Pederson E, Kim SY, Shapiro N, Woyke T, Altermark B, Pawlowski K, Weyman PD, Dupont CL, Rasmussen U (2018) Genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiont. Mol Biol Evol 35:1160–1175. https://doi.org/10.1093/molbev/msy029
Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139. https://doi.org/10.1104/pp.117.1.129
Yodsang P, Raksajit W, Aro EM, Mäenpää P, Incharoensakdi A (2018) Factors affecting photobiological hydrogen production in five filamentous cyanobacteria from Thailand. Photosynthetica 56:334–341. https://doi.org/10.1007/s11099-018-0789-5
Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378–388. https://doi.org/10.1104/pp.107.105742
Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561. https://doi.org/10.1007/s004250100660
Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348. https://doi.org/10.1128/EC.3.5.1331-1348.2004
Zhang Z, Pendse ND, Phillips KN, Cotner JB, Khodursky A (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 9:1–14. https://doi.org/10.1186/1471-2164-9-344
Zhang Y, Huang Z, Zheng H, Wang Q, Li A (2020) Growth, biochemical composition and photosynthetic performance of Scenedesmus acuminatus under different initial sulfur supplies. Algal Res 45:101728. https://doi.org/10.1016/j.algal.2019.101728
Zheng L, Cash VL, Flint DH, Dean DR (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273:13264–13272. https://doi.org/10.1074/jbc.273.21.13264
Acknowledgments
The Head of Department of Botany, Banaras Hindu University, Varanasi, India is gratefully acknowledged for providing laboratory facilities. Surbhi Kharwar and Samujjal Bhattacharjee are thankful to UGC and CSIR, New Delhi, India, for fellowship, respectively, and Sindhunath Chakraborty is thankful to ICAR-AMAAS for providing financial support. All content of the review article is fully acknowledged.
Funding
The Head of Department of Botany, Banaras Hindu University, Varanasi, India is gratefully acknowledged for providing laboratory facilities. Surbhi Kharwar and Samujjal Bhattacharjee are thankful to UGC and CSIR, New Delhi, India in form of fellowship and Sindhunath Chakraborty is thankful to ICAR-AMAAS for providing financial support.
Author information
Authors and Affiliations
Contributions
A.K.M and S.K. conceptualized the overall structure. S.K. and S.B. wrote the manuscript. S.K. and S.B. prepared illustrations, figures, tables, and references. S.K., S.B., and S.C. edited the manuscript. A.K.M contributed critical comments to the draft and approved the manuscript. All the authors reviewed the draft.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kharwar, S., Bhattacharjee, S., Chakraborty, S. et al. Regulation of sulfur metabolism, homeostasis and adaptive responses to sulfur limitation in cyanobacteria. Biologia 76, 2811–2835 (2021). https://doi.org/10.1007/s11756-021-00819-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00819-5