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Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii

Yıl 2022, , 213 - 218, 30.12.2022
https://doi.org/10.25308/aduziraat.1103450

Öz

Sulfate is an essential macroelement for all living organisms. However, sulfate can be limited in agricultural settings. Microorganisms change their gene expression to acclimate to sulfate deficient conditions. Green microalga Chlamydomonas reinhardtii expresses and secretes extracellular arylsulfatase (ARS) under sulfate deficient conditions. Our results show that C. reinhardtii ARS can hydrolyze both sulfate monoester (5-bromo-4-chloro-3 indolyl sulfate; X-SO42-) and phosphate monoester (5-bromo-4-chloro-3 indolyl phosphate; X-PO43-) providing evidence that ARS enzyme has promiscuous activity. C. reinhardtii is found in soil and fresh water habitats in nature. This promiscuous activity can be beneficial in making both sulfate and phosphate bioavailable for uptake by soil organisms and plant roots.

Destekleyen Kurum

Akdeniz University BAP Commission

Proje Numarası

FBA-2018-4156

Kaynakça

  • Aksoy M, Pootakham W, Pollock SV, Moseley JL, González-Ballester D, Grossman AR (2013) Tiered Regulation of Sulfur Deprivation Responses in Chlamydomonas reinhardtii and Identification of an Associated Regulatory Factor. Plant Physiology 162: 195–211.
  • Aksoy M, Pootakham W, Grossman AR (2014) Critical Function of a Chlamydomonas reinhardtii Putative Polyphosphate Polymerase Subunit during Nutrient Deprivation. The Plant Cell 26: 4214–4229.
  • Boltes I, Czapinska H, Kahnert A, von Bülow R, Dierks T, Schmidt B, von Figura K, Kertesz MA, Usón I (2001) 1.3 Å Structure of Arylsulfatase from Pseudomonas aeruginosa Establishes the Catalytic Mechanism of Sulfate Ester Cleavage in the Sulfatase Family. Structure 9: 483–491.
  • Bouranis DL, Malagoli M, Avice JC, Bloem E (2020) Advances in Plant Sulfur Research. Plants 9, 256.
  • Chruszcz M, Laidler P, Monkiewicz M, Ortlund E, Lebioda L, Lewinski K (2003) Crystal structure of a covalent intermediate of endogenous human arylsulfatase A. Journal of Inorganic Biochemistry 96: 386–392.
  • Cloves JM, Dodgson KS, Games DE, Shaw DJ, White GF (1977) The Mechanism of Action of Primary Alkylsulphohydrolase and Arylsulphohydrolase from a Detergent-degrading Microorganism. Biochemistry Journal 167: 843–846.
  • Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas with Aberrant Responses to Sulfur Deprivation. The Plant Cell 6: 53–63.
  • De Hostos EL, Togasaki RK, Grossman A (1988) Purification and Biosynthesis of a Derepressible Periplasmic Arylsulfatase from Chlamydomonas reinhardtii. Journal of Cell Biology 106: 29–37.
  • De Hostos EL, Schilling J, Grossman AR (1989) Structure and Expression of the Gene Encoding the Periplasmic Arylsulfatase of Chlamydomonas reinhardtii. MGG Molecular & General Genetics, 218: 229–239.
  • Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K (1999) Sequence Determinants Directing Conversion of Cysteine to Formylglycine in Eukaryotic Sulfatases. EMBO Journal 18: 2084–2091.
  • Gorman DS, Levine RP (1965) Cytochrome f and Plastocyanin: Their Sequence in the Photosynthetic Electron Transport Chain of Chlamydomonas reinhardi. Proceedings of the National Academy of Sciences of the United States of America 54(6): 1665–1669.
  • Günal S, Hardman R, Kopriva S, Mueller JW (2019) Sulfation Pathways From Red to Green. Journal of Biological Chemistry 294(33): 12293–12312.
  • Jonas S, van Loo B, Hyvonen M, Hollfelder F (2008) A New Member of the Alkaline Phosphatase Superfamily with a Formylglycine Nucleophile: Structural and Kinetic Characterisation of a Phosphonate Monoester Hydrolase/Phosphodiesterase from Rhizobium leguminosarum. Journal of Molecular Biology 384: 120–36.
  • Kagiwada S, Nakamae I, Kayukawa M, Kato S (2004) Cytoskeleton-dependent Polarized Secretion of Arylsulfatase in the Unicellular Green Alga, Chlamydomonas reinhardtii. Plant Science 166: 1515–1524.
  • Kertesz MA (2000) Riding the sulfur cycle - Metabolism of Sulfonates and Sulfate Esters in Gram-negative Bacteria. FEMS Microbiology Reviews 24: 135–175.
  • Knauff U, Schulz M, Scherer HW (2003) Arylsufatase Activity in the Rhizosphere and Roots of Different Crop Species. European Journal of Agronomy 19: 215–223.
  • Liang C, Wang J, Zhao J, Tian J, Liao H (2014) Control of Phosphate Homeostasis Through Gene Regulation in Crops. Current Opinion in Plant Biology 21: 59–66.
  • López-Arredondo D, Leyva-González M, González-Morales S, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: Improving low-phosphate tolerance in crops. Annual Review of Plant Biology 65: 95–123.
  • Marino T, Russo N, Toscano M (2013) Catalytic Mechanism of the Arylsulfatase Promiscuous Enzyme from Pseudomonas aeruginosa. Chemistry A European Journal 19: 2185–2192.
  • Marquordt C, Fang Q, Will E, Peng J, von Figura K, Dierks T (2003) Posttranslational Modification of Serine to Formylglycine in Bacterial Sulfatases: Recognition of the Modification Motif by the Iron-sulfur Protein AtsB. Journal of Biological Chemistry 278: 2212–2218.
  • Moseley JL, Gonzalez-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic Interactions Between Regulators of Chlamydomonas Phosphorus and Sulfur Deprivation Responses. Genetics 181: 889–905.
  • Murooka Y, Ishibashi K, Yasumoto M, Sasaki M, Sugino H, Azakami H, Yamashita M (1990) A sulfur- and Tyramine Regulated Klebsiella aerogenes Operon Containing the Arylsulfatase (atsA) Gene and the atsB Gene. Journal of Bacteriology 172: 2131–2140.
  • Olguin LF, Askew SE, O’Donoghue AMC, Hollfelder F (2008) Efficient Catalytic Promiscuity in an Enzyme Superfamily: An Arylsulfatase Shows a Rate Acceleration of 1013 for Phosphate Monoester Hydrolysis. Journal of American Chemical Society 130: 16547–16555.
  • Sasso S, Stibor H, Mittag M, Grossman AR (2018) The Natural History of Model Organisms from Molecular Manipulation of Domesticated Chlamydomonas reinhardtii to Survival in Nature. Elife 7:e39233.
  • Salarvan, F (2021) Determınation of Expressıon Levels of Chlamydomonas reinhardtii Arylsulfatase Genes by Semi-quantitative PCR and qPCR Methods. MSc Thesis, Akdeniz University.
  • Schmidt B, Selmer T, Ingendoh A, von Figurat K (1995) ANovel Amino Acid Modification in Sulfatases That is Defective in Multiple Sulfatase Deficiency. Cell 82: 271–278.
  • Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate Solubilizing Microbes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils. SpringerPlus 2: 587.
  • Shimogawara K, Wykoff DD, Usuda H, Grossman AR (1999) Chlamydomonas reinhardtii Mutants Abnormal in Their Responses to Phosphorus Deprivation. Plant Physiology 120: 1–10.
  • Toesch M, Schober M, Faber K (2014) Microbial Alkyl- and Aryl-sulfatases: Mechanism, Occurrence, Screening and Stereoselectivities. Applied Microbiology and Biotechnology 98: 1485–1496.
  • Van Loo B, Bayer CD, Fischer G, Jonas S, Valkov E, Mohamed MF, Vorobieva A, Dutruel C, Hyvönen M, Hollfelder F (2019) Balancing Specificity and Promiscuity in Enzyme Evolution: Multidimensional Activity Transitions in the Alkaline Phosphatase Superfamily. Journal of the American Chemical Society 141: 370–387.

Chlamydomonas reinhardtii'de Seçici Olmayan Arilsülfataz Aktivitesi

Yıl 2022, , 213 - 218, 30.12.2022
https://doi.org/10.25308/aduziraat.1103450

Öz

Sülfat canlılar için zorunlu bir makroelementtir. Buna rağmen, sülfat tarımsal alanlarda eksik olabilir. Mikroorganizmalar gen ekspresyonlarını değistirerek sülfat eksikliğine aklimasyon gösterirler. Yeşil mikroalg Chlamydomonas reinhardtii sülfat eksikliği altında arilsülfataz (ARS) sentezler ve hücre dışına salgılar. Bu çalışmadaki sonuçlarımız, C. reinhardtii ARS’ın hem sülfat monoesterlerini (5-bromo-4-chloro-3 indolyl sulfate; X-SO42-) hem de fosfat monoesterlerini (5-bromo-4-chloro-3 indolyl phosphate; X-PO43-) hidrolize ettiğini göstermiştir. Bu da ARS’ın seçici olmayan aktiviteye sahip olduğuna kanıt sunmaktadır. C. reinhardtii toprak ve taze su ortamlarında yaşamaktadır. Sahip olduğu seçici olmayan ARS aktivitesi hem sülfatın hem de fosfatın bitki tarafından kullanılabilir forma getirilmesine katkı sağlayabilir.

Proje Numarası

FBA-2018-4156

Kaynakça

  • Aksoy M, Pootakham W, Pollock SV, Moseley JL, González-Ballester D, Grossman AR (2013) Tiered Regulation of Sulfur Deprivation Responses in Chlamydomonas reinhardtii and Identification of an Associated Regulatory Factor. Plant Physiology 162: 195–211.
  • Aksoy M, Pootakham W, Grossman AR (2014) Critical Function of a Chlamydomonas reinhardtii Putative Polyphosphate Polymerase Subunit during Nutrient Deprivation. The Plant Cell 26: 4214–4229.
  • Boltes I, Czapinska H, Kahnert A, von Bülow R, Dierks T, Schmidt B, von Figura K, Kertesz MA, Usón I (2001) 1.3 Å Structure of Arylsulfatase from Pseudomonas aeruginosa Establishes the Catalytic Mechanism of Sulfate Ester Cleavage in the Sulfatase Family. Structure 9: 483–491.
  • Bouranis DL, Malagoli M, Avice JC, Bloem E (2020) Advances in Plant Sulfur Research. Plants 9, 256.
  • Chruszcz M, Laidler P, Monkiewicz M, Ortlund E, Lebioda L, Lewinski K (2003) Crystal structure of a covalent intermediate of endogenous human arylsulfatase A. Journal of Inorganic Biochemistry 96: 386–392.
  • Cloves JM, Dodgson KS, Games DE, Shaw DJ, White GF (1977) The Mechanism of Action of Primary Alkylsulphohydrolase and Arylsulphohydrolase from a Detergent-degrading Microorganism. Biochemistry Journal 167: 843–846.
  • Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas with Aberrant Responses to Sulfur Deprivation. The Plant Cell 6: 53–63.
  • De Hostos EL, Togasaki RK, Grossman A (1988) Purification and Biosynthesis of a Derepressible Periplasmic Arylsulfatase from Chlamydomonas reinhardtii. Journal of Cell Biology 106: 29–37.
  • De Hostos EL, Schilling J, Grossman AR (1989) Structure and Expression of the Gene Encoding the Periplasmic Arylsulfatase of Chlamydomonas reinhardtii. MGG Molecular & General Genetics, 218: 229–239.
  • Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K (1999) Sequence Determinants Directing Conversion of Cysteine to Formylglycine in Eukaryotic Sulfatases. EMBO Journal 18: 2084–2091.
  • Gorman DS, Levine RP (1965) Cytochrome f and Plastocyanin: Their Sequence in the Photosynthetic Electron Transport Chain of Chlamydomonas reinhardi. Proceedings of the National Academy of Sciences of the United States of America 54(6): 1665–1669.
  • Günal S, Hardman R, Kopriva S, Mueller JW (2019) Sulfation Pathways From Red to Green. Journal of Biological Chemistry 294(33): 12293–12312.
  • Jonas S, van Loo B, Hyvonen M, Hollfelder F (2008) A New Member of the Alkaline Phosphatase Superfamily with a Formylglycine Nucleophile: Structural and Kinetic Characterisation of a Phosphonate Monoester Hydrolase/Phosphodiesterase from Rhizobium leguminosarum. Journal of Molecular Biology 384: 120–36.
  • Kagiwada S, Nakamae I, Kayukawa M, Kato S (2004) Cytoskeleton-dependent Polarized Secretion of Arylsulfatase in the Unicellular Green Alga, Chlamydomonas reinhardtii. Plant Science 166: 1515–1524.
  • Kertesz MA (2000) Riding the sulfur cycle - Metabolism of Sulfonates and Sulfate Esters in Gram-negative Bacteria. FEMS Microbiology Reviews 24: 135–175.
  • Knauff U, Schulz M, Scherer HW (2003) Arylsufatase Activity in the Rhizosphere and Roots of Different Crop Species. European Journal of Agronomy 19: 215–223.
  • Liang C, Wang J, Zhao J, Tian J, Liao H (2014) Control of Phosphate Homeostasis Through Gene Regulation in Crops. Current Opinion in Plant Biology 21: 59–66.
  • López-Arredondo D, Leyva-González M, González-Morales S, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: Improving low-phosphate tolerance in crops. Annual Review of Plant Biology 65: 95–123.
  • Marino T, Russo N, Toscano M (2013) Catalytic Mechanism of the Arylsulfatase Promiscuous Enzyme from Pseudomonas aeruginosa. Chemistry A European Journal 19: 2185–2192.
  • Marquordt C, Fang Q, Will E, Peng J, von Figura K, Dierks T (2003) Posttranslational Modification of Serine to Formylglycine in Bacterial Sulfatases: Recognition of the Modification Motif by the Iron-sulfur Protein AtsB. Journal of Biological Chemistry 278: 2212–2218.
  • Moseley JL, Gonzalez-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic Interactions Between Regulators of Chlamydomonas Phosphorus and Sulfur Deprivation Responses. Genetics 181: 889–905.
  • Murooka Y, Ishibashi K, Yasumoto M, Sasaki M, Sugino H, Azakami H, Yamashita M (1990) A sulfur- and Tyramine Regulated Klebsiella aerogenes Operon Containing the Arylsulfatase (atsA) Gene and the atsB Gene. Journal of Bacteriology 172: 2131–2140.
  • Olguin LF, Askew SE, O’Donoghue AMC, Hollfelder F (2008) Efficient Catalytic Promiscuity in an Enzyme Superfamily: An Arylsulfatase Shows a Rate Acceleration of 1013 for Phosphate Monoester Hydrolysis. Journal of American Chemical Society 130: 16547–16555.
  • Sasso S, Stibor H, Mittag M, Grossman AR (2018) The Natural History of Model Organisms from Molecular Manipulation of Domesticated Chlamydomonas reinhardtii to Survival in Nature. Elife 7:e39233.
  • Salarvan, F (2021) Determınation of Expressıon Levels of Chlamydomonas reinhardtii Arylsulfatase Genes by Semi-quantitative PCR and qPCR Methods. MSc Thesis, Akdeniz University.
  • Schmidt B, Selmer T, Ingendoh A, von Figurat K (1995) ANovel Amino Acid Modification in Sulfatases That is Defective in Multiple Sulfatase Deficiency. Cell 82: 271–278.
  • Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate Solubilizing Microbes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils. SpringerPlus 2: 587.
  • Shimogawara K, Wykoff DD, Usuda H, Grossman AR (1999) Chlamydomonas reinhardtii Mutants Abnormal in Their Responses to Phosphorus Deprivation. Plant Physiology 120: 1–10.
  • Toesch M, Schober M, Faber K (2014) Microbial Alkyl- and Aryl-sulfatases: Mechanism, Occurrence, Screening and Stereoselectivities. Applied Microbiology and Biotechnology 98: 1485–1496.
  • Van Loo B, Bayer CD, Fischer G, Jonas S, Valkov E, Mohamed MF, Vorobieva A, Dutruel C, Hyvönen M, Hollfelder F (2019) Balancing Specificity and Promiscuity in Enzyme Evolution: Multidimensional Activity Transitions in the Alkaline Phosphatase Superfamily. Journal of the American Chemical Society 141: 370–387.
Toplam 30 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Endüstriyel Biyoteknoloji
Bölüm Araştırma
Yazarlar

Münevver Aksoy 0000-0002-0798-5805

Proje Numarası FBA-2018-4156
Yayımlanma Tarihi 30 Aralık 2022
Yayımlandığı Sayı Yıl 2022

Kaynak Göster

APA Aksoy, M. (2022). Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi, 19(2), 213-218. https://doi.org/10.25308/aduziraat.1103450
AMA Aksoy M. Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii. ADÜ ZİRAAT DERG. Aralık 2022;19(2):213-218. doi:10.25308/aduziraat.1103450
Chicago Aksoy, Münevver. “Promiscuous Arylsulfatase Activity in Chlamydomonas Reinhardtii”. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi 19, sy. 2 (Aralık 2022): 213-18. https://doi.org/10.25308/aduziraat.1103450.
EndNote Aksoy M (01 Aralık 2022) Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi 19 2 213–218.
IEEE M. Aksoy, “Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii”, ADÜ ZİRAAT DERG, c. 19, sy. 2, ss. 213–218, 2022, doi: 10.25308/aduziraat.1103450.
ISNAD Aksoy, Münevver. “Promiscuous Arylsulfatase Activity in Chlamydomonas Reinhardtii”. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi 19/2 (Aralık 2022), 213-218. https://doi.org/10.25308/aduziraat.1103450.
JAMA Aksoy M. Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii. ADÜ ZİRAAT DERG. 2022;19:213–218.
MLA Aksoy, Münevver. “Promiscuous Arylsulfatase Activity in Chlamydomonas Reinhardtii”. Adnan Menderes Üniversitesi Ziraat Fakültesi Dergisi, c. 19, sy. 2, 2022, ss. 213-8, doi:10.25308/aduziraat.1103450.
Vancouver Aksoy M. Promiscuous Arylsulfatase Activity in Chlamydomonas reinhardtii. ADÜ ZİRAAT DERG. 2022;19(2):213-8.