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Beta-propeller phytases in the aquatic environment

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Abstract

Phytate, which is one of the dominant organic phosphorus compounds in nature, is very stable in soils. Although a substantial amount of phytate is carried from terrestrial to aquatic systems, it is a minor component of organic phosphorus in coastal sediments. The ephemeral nature of phytate implies the rapid hydrolysis of phytate under aquatic conditions. Among the four classes of known phytases that have been identified in terrestrial organisms, only β-propeller phytase-like sequences have been identified in the aquatic environment. A novel β-propeller phytase gene (phyS), cloned from Shewanella oneidensis MR-1, was found to encode a protein with two beta-propeller phytase domains. The characterization of recombinant full-length PhyS and its domains demonstrated that Domain II was the catalytic domain responsible for phytate hydrolysis. The full-length PhyS displayed a Km of 83 μM with a kcat of 175.9 min−1 and the Domain II displayed a Km of 474 μM with a kcat of 10.6 min−1. These results confirm that the phyS gene encodes a functional β-propeller phytase, which is expressed in S. oneidensis under phosphorus deficienct condition. The presence of multiple sequences with a high similarity to phyS in aquatic environmental samples and the widespread occurrence of the Shewanella species in nature suggest that the β-propeller phytase family is the major class of phytases in the aquatic environment, and that it may play an important role in the recycling of phosphorus.

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References

  • Bendtsen JD, Nielsen H, von HG, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  PubMed  CAS  Google Scholar 

  • Brettar I, Christen R, Hofle MG (2002) Shewanella denitrificans sp. nov., a vigorously denitrifying bacterium isolated from the oxic-anoxic interface of the Gotland Deep in the central Baltic Sea. Int J Syst Evol Microbiol 52:2211–2217

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Sankaranarayanan R, Sonti RV (2003) PhyA, a secreted protein of Xanthomonas oryzae pv. oryzae, is required for optimum virulence and growth on phytic acid as a sole phosphate source. Mol Plant Microbe Interact 16:973–982

    Article  PubMed  CAS  Google Scholar 

  • Chu HM, Guo RT, Lin TW, Chou CC, Shr HL, Lai HL, Tang TY, Cheng KJ, Selinger BL, Wang AH (2004) Structures of Selenomonas ruminantium phytase in complex with persulfated phytate: DSP phytase fold and mechanism for sequential substrate hydrolysis. Structure (Camb) 12:2015–2024

    Article  CAS  Google Scholar 

  • Gonin M, Quardokus EM, O’Donnol D, Maddock J, Brun YV (2000) Regulation of stalk elongation by phosphate in Caulobacter crescentus. J Bacteriol 182:337–347

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez JM, Weiner RM (2000) Phylogenetic characterization of marine bacterium strain 2–40, a degrader of complex polysaccharides. Int J Syst Evol Microbiol 50(Pt 2):831–834

    PubMed  Google Scholar 

  • Ha NC, Oh BC, Shin S, Kim HJ, Oh TK, Kim YO, Choi KY, Oh BH (2000) Crystal structures of a novel, thermostable phytase in partially and fully calcium-loaded states. Nat Struct Biol 7:147–153

    Article  PubMed  CAS  Google Scholar 

  • Hegeman CE, Grabau EA (2001) A novel phytase with sequence similarity to purple acid phosphatases is expressed in cotyledons of germinating soybean seedlings. Plant Physiol 126:1598–1608

    Article  PubMed  CAS  Google Scholar 

  • Ireland MM, Karty JA, Quardokus EM, Reilly JP, Brun YV (2002) Proteomic analysis of the Caulobacter crescentus stalk indicates competence for nutrient uptake. Mol Microbiol 45:1029–1041

    Article  PubMed  CAS  Google Scholar 

  • Ivanova EP, Sawabe T, Hayashi K, Gorshkova NM, Zhukova NV, Nedashkovskaya OI, Mikhailov VV, Nicolau DV, Christen R (2003a) Shewanella fidelis sp. nov., isolated from sediments and sea water. Int J Syst Evol Microbiol 53:577–582

    Article  CAS  Google Scholar 

  • Ivanova EP, Sawabe T, Zhukova NV, Gorshkova NM, Nedashkovskaya OI, Hayashi K, Frolova GM, Sergeev AF, Pavel KG, Mikhailov VV, Nicolau DV (2003b) Occurrence and diversity of mesophilic Shewanella strains isolated from the North-West Pacific Ocean. Syst Appl Microbiol 26:293–301

    Article  CAS  Google Scholar 

  • Kelley LA, MacCallum RM, Sternberg MJ (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 299:499–520

    Article  PubMed  CAS  Google Scholar 

  • Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998) Cloning of the thermostable phytase gene (phy) from Bacillus sp. DS11 and its overexpression in Escherichia coli. FEMS Microbiol Lett 162:185–191

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lott JNA, Ockenden I, Raboy V, Batten GD (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci Res 10:11–33. 2003

    Google Scholar 

  • Martin CJ, Evans WJ (1986) Phytic acid-metal ion interactions. II. The effect of pH on Ca(II) binding. J Inorg Biochem 27:17–30

    Article  PubMed  CAS  Google Scholar 

  • Mullaney EJ, Daly CB, Ullah AH (2000) Advances in phytase research. Adv Appl Microbiol 47:157–199

    PubMed  CAS  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Oh BC, Chang BS, Park KH, Ha NC, Kim HK, Oh BH, Oh TK (2001) Calcium-dependent catalytic activity of a novel phytase from Bacillus amyloliquefaciens DS11. Biochemistry 40:9669–9676

    Article  PubMed  CAS  Google Scholar 

  • Satomi M, Oikawa H, Yano Y (2003) Shewanella marinintestina sp. nov., Shewanella schlegeliana sp. nov. and Shewanella sairae sp. nov., novel eicosapentaenoic-acid- producing marine bacteria isolated from sea-animal intestines. Int J Syst Evol Microbiol 53:491–499

    Article  PubMed  CAS  Google Scholar 

  • Schenk G, Guddat LW, Ge Y, Carrington LE, Hume DA, Hamilton S, de Jersey J (2000) Identification of mammalian-like purple acid phosphatases in a wide range of plants. Gene 250:117–125

    Article  PubMed  CAS  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  • Sly LI, Cox TL, Beckenham TB (1999) The phylogenetic relationships of Caulobacter, Asticcacaulis and Brevundimonas species and their taxonomic implications. Int J Syst Bacteriol 49(Pt 2):483–488

    PubMed  Google Scholar 

  • Spizizen J (1958) Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA 44:1072–1078

    Article  PubMed  CAS  Google Scholar 

  • Suzumura M, Kamatani A (1993) Isolation and determination of inositol hexaphosphate in sediments from Tokyo Bay. Geochim Cosmochim Acta 57:2197–2202

    Article  CAS  Google Scholar 

  • Suzumura M, Kamatani A (1995a) Origin and distribution of inositol hexaphosphate in estuarine and coastal sediments. Limnol Oceanogr 40:1254–1261

    Article  CAS  Google Scholar 

  • Suzumura M, Kamatani A (1995b) Mineralization of inositol hexaphosphate in aerobic and anaerobic marine sediments: implications for the phosphorus cycle. Geochim Cosmochim Acta 59:1021–1026

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Turner BL, Paphazy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos Trans R Soc Lond B Biol Sci 357:449–469

    Article  PubMed  CAS  Google Scholar 

  • Tye AJ, Siu F-KY, Leung T-YC, Lim BL (2002) Molecular cloning and the biochemical characterization of two novel phytases from B. subtilis 168 and B. licheniformis. Appl Microbiol Biotechnol 59:190–197

    Article  PubMed  CAS  Google Scholar 

  • Ullah AH, Mullaney EJ (1996) Disulfide bonds are necessary for structure and activity in Aspergillus ficuum phytase. Biochem Biophys Res Commun 227:311–317

    Article  PubMed  CAS  Google Scholar 

  • Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49(Pt 2):705–724

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  CAS  Google Scholar 

  • Wang XY, Meng FG, Zhou HM (2004) The role of disulfide bonds in the conformational stability and catalytic activity of phytase. Biochem Cell Biol 82:329–334

    Article  PubMed  CAS  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552

    PubMed  CAS  Google Scholar 

  • Yanke LJ, Bae HD, Selinger LB, Cheng KJ (1998) Phytase activity of anaerobic ruminal bacteria. Microbiology 144(Pt 6):1565–1573

    Article  PubMed  CAS  Google Scholar 

  • Yip W, Wang L, Cheng C, Wu W, Lung S, Lim BL (2003) The introduction of a phytase gene from Bacillus subtilis improved the growth performance of transgenic tobacco. Biochem Biophys Res Commun 310:1148–1154

    Google Scholar 

Download references

Acknowledgements

We thank Mr. Chung Chau Hon for his advice on homology modeling and phylogenetic tree analyses. This work was supported by the Research Grants Council of the Hong Kong Special Administrative Region Government, China (project HKU 7335/04M) and the University Research Committee (No. 10205120).

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  1. Department of Zoology, the University of Hong Kong, Pokfulam Road, Hong Kong, China

    Chiwai Cheng & Boon L. Lim

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  1. Chiwai Cheng
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  2. Boon L. Lim
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Correspondence to Boon L. Lim.

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Cheng, C., Lim, B.L. Beta-propeller phytases in the aquatic environment. Arch Microbiol 185, 1–13 (2006). https://doi.org/10.1007/s00203-005-0080-6

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