Identification and Characterization of an Extracellular Alkaline Phosphatase in the Marine Diatom Phaeodactylum tricornutum

Marine Biotechnology

Volumn 15, Issue 4, 2013, Pages 425-436

  Lin, Hung Yun ^a   Shih, Chi Yu ^a   Liu, Hung Chun ^a   Chang, Jeng ^a   Chen, Ying Lan ^b,c   Chen, Yet Ran ^a,c   Lin, Han Tso ^d   Chang, Yu Yung ^b   Hsu, Chun Hua ^b   Lin, Han Jia ^a  

^a NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

^d MING CHUAN UNIVERSITY   (Taiwan)

Author keywords

Alkaline phosphatase; Diatom; Glycoprotein; Metal ion; PhoA

Indexed keywords

ALKALINE PHOSPHATASE; DIATOM; ENZYMATIC ACTIVITIES; GEL-FILTRATION CHROMATOGRAPHY; PHAEODACTYLUM TRICORNUTUM; PHOA; PHYLOGENETIC ANALYSIS; PHYSIOLOGICAL CONDITION;

AMINO ACIDS; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; GLYCOPROTEINS; METAL IONS; PHOSPHATASES; PHOSPHORUS; PHYTOPLANKTON; POLYMERASE CHAIN REACTION; POPULATION STATISTICS; SEARCH ENGINES; ZINC;

ENZYME ACTIVITY;

ALKALINE PHOSPHATASE; HEAVY METAL; PHOSPHORUS; PRIMER DNA;

AMINO ACID; BACTERIUM; BIOMONITORING; BIOREACTOR; DATABASE; DIATOM; ENZYME ACTIVITY; HEAVY METAL; IDENTIFICATION METHOD; INHIBITION; MARINE ENVIRONMENT; NUCLEIC ACID; PHOSPHORUS; PHYLOGENETICS; POLYMERASE CHAIN REACTION; POPULATION GROWTH;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGICAL MODEL; BIOLOGY; CLUSTER ANALYSIS; DIATOM; DIMERIZATION; ENZYMOLOGY; EXTRACELLULAR FLUID; GEL CHROMATOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POPULATION DYNAMICS; PROTEOMICS; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE;

ALKALINE PHOSPHATASE; AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMATOGRAPHY, GEL; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DIATOMS; DIMERIZATION; DNA PRIMERS; EXTRACELLULAR FLUID; GENE EXPRESSION REGULATION; METALS, HEAVY; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHOSPHORUS; PHYLOGENY; POPULATION DYNAMICS; PROTEOMICS; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY;

BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); COBETIA MARINA; ESCHERICHIA COLI; NITZSCHIA ALBA; PHAEODACTYLUM TRICORNUTUM;

EID: 84879784162     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-013-9494-3     Document Type: Article

References (51)

1. Adl SMS, Simpson AGBA, Farmer MAM, Andersen RAR, Anderson ORO, Barta JRJ, Bowser SSS, Brugerolle GG, Fensome RAR, Fredericq SS, James TYT, Karpov SS, Kugrens PP, Krug JJ, Lane CEC, Lewis LAL, Lodge JJ, Lynn DHD, Mann DGD, Mccourt RMR, Mendoza LL, Moestrup OO, Mozley-Standridge SES, Nerad TAT, Shearer CAC, Smirnov AVA, Spiegel FWF, Taylor MFJRM (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52: 399-451.
2. Armbrust EV (2009) The life of diatoms in the world's oceans. Nature 459: 185-192.
3. Baiet B, Burel C, Saint-Jean B, Louvet R, Menu-Bouaouiche L, Kiefer-Meyer MC, Mathieu-Rivet E, Lefebvre T, Castel H, Carlier A, Cadoret JP, Lerouge P, Bardor M (2011) N-glycans of Phaeodactylum tricornutum diatom and functional characterization of its N-acetylglucosaminyltransferase I enzyme. J Biol Chem 286: 6152-6164.
4. Bailleul B, Rogato A, De Martino A, Coesel S, Cardol P, Bowler C, Falciatore A, Finazzi G (2010) An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci U S A 107: 18214-18219.
5. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18: 298-305.
6. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret J-P, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jézéquel V, Lopez PJ, Lucas S, Mangogna M, Mcginnis K, Medlin LK, Montsant A, Oudot-Le Secq M-P, Napoli C, Obornik M, Parker MS, Petit J-L, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, Von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, van De Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239-244.
7. Bozarth A, Maier U-G, Zauner S (2009) Diatoms in biotechnology: modern tools and applications. Appl Microbiol Biotechnol 82: 195-201.
8. Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol R 62: 667-683.
9. Chen C-J, Tseng M-C, Lin T-W, Chen Y-R (2010) Visual indicator for surfactant abundance in MS-based membrane and general proteomics applications. Anal Chem 82: 8283-8290.
10. Chen C-J, Chen W-Y, Tseng M-C, Chen Y-R (2012) Tunnel frit: a nonmetallic in-capillary frit for nanoflow ultra high-performance liquid chromatography-mass spectrometry applications. Anal Chem 84: 297-303.
11. Chung C-C, Hwang S-PL, Chang J (2005) Cooccurrence of ScDSP gene expression, cell death, and DNA fragmentation in a marine diatom, Skeletonema costatum. Appl Environ Microb 71: 8744-8751.
12. Chung C-C, Chang J, Gong G-C, Hsu S-C, Chiang K-P, Liao C-W (2011) Effects of Asian dust storms on synechococcus populations in the subtropical Kuroshio current. Mar Biotechnol 13: 751-763.
13. Coleman JE (1992) Structure and mechanism of alkaline phosphatase. Annu Rev Biophys Biomol Struct 21: 441-483.
14. Dyhrman ST, Palenik B (1999) Phosphate stress in cultures and field populations of the dinoflagellate Prorocentrum minimum detected by a single-cell alkaline phosphatase assay. Appl Environ Microb 65: 3205-3212.
15. Dyhrman ST, Ruttenberg KC (2006) Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnol Oceanogr 51: 1381-1390.
16. Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML, Alexander H, Whitney LP, Drzewianowski A, Bulygin VV, Bertrand EM, Wu Z, Benitez-Nelson C, Heithoff A (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7: e33768.
17. Eder S, Shi L, Jensen K, Yamane K, Hulett FM (1996) A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology 142(Pt 8): 2041-2047.
18. Falkowski P, Katz M, Knoll A, Quigg A, Raven J, Schofield O, Taylor F (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354-360.
19. Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3. 2). Cladistics 5: 164-166.
20. Giovannoni SJ, Stingl U (2005) Molecular diversity and ecology of microbial plankton. Nature 437: 343-348.
21. Guillard RRL, Ryther J (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 8: 229-239.
22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 14: 95-98.
23. Hallmann AA (1999) Enzymes in the extracellular matrix of Volvox: an inducible, calcium-dependent phosphatase with a modular composition. J Biol Chem 274: 1691-1697.
24. Huang B, Ou L, Hong H, Luo H, Wang D (2005) Bioavailability of dissolved organic phosphorus compounds to typical harmful dinoflagellate Prorocentrum donghaiense Lu. Mar Pollut Bull 51: 838-844.
25. Kang LK, Wang HF, Chang J (2010) Diversity of phytoplankton nitrate transporter sequences from isolated single cells and mixed samples from the East China Sea and mRNA quantification. Appl Environ Microb 77: 122-130.
26. Kang LK, Tsui FH, Chang J (2012) Quantification of diatom gene expression in the sea by selecting uniformly transcribed mRNA as the basis for normalization. Appl Environ Microb 78: 6051-6058.
27. Karl DM, Bjorkman KM, Dore JE, Fujieki L, Hebel DV, Houlihan T, Letelier RM, Tupas LM (2001) Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep-Sea Res II Top Stud Oceanogr 48: 1529-1566.
28. Katz M, Wright J, Miller K, Cramer B, Fennel K, Falkowski P (2005) Biological overprint of the geological carbon cycle. Mar Geol 217: 323-338.
29. Kim E, Wyckoff HW (1991) Reaction-mechanism of alkaline-phosphatase based on crystal structures. J Mol Biol 218: 449-464.
30. Lin X, Zhang H, Huang B (2011) Alkaline phosphatase gene sequence and transcriptional regulation by phosphate limitation in Amphidinium carterae (Dinophyceae). J Phycol 47(5): 1110-1120.
31. Lin X, Zhang H, Cui Y, Lin S (2012a) High sequence variability, diverse subcellular localizations, and ecological implications of alkaline phosphatase in dinoflagellates and other eukaryotic phytoplankton. Front Microbio 3: 235.
32. Lin X, Zhang H, Huang B, Lin S (2012b) Alkaline phosphatase gene sequence characteristics and transcriptional regulation by phosphate limitation in Karenia brevis (Dinophyceae). Harmful Algae 17: 14-24.
33. Liu HC, Gong GC, Chang J (2010) Lateral water exchange between shelf-margin upwelling and Kuroshio waters influences phosphorus stress in microphytoplankton. Mar Ecol Prog Ser 409: 121-130.
34. Lohan M, Statham P, Crawford D (2002) Total dissolved zinc in the upper water column of the subarctic North East Pacific. Deep-Sea Res Pt II 49: 5793-5808.
35. Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proc Natl Acad Sci USA 106: 21219-21223.
36. Luo M, Guo Y, Deng J, Wei H, Zhang Z, Leng Y, Men D, Song L, Zhang X, Zhou Y (2010) Characterization of a monomeric heat-labile classical alkaline phosphatase from Anabaena sp. PCC7120. Biochem Mosc 75: 655-664.
37. Majumdar A, Ghatak A, Ghosh RK (2005) Identification of the gene for the monomeric alkaline phosphatase of Vibrio cholerae serogroup O1 strain. Gene 344: 251-258.
38. Nelson D, Tréguer P, Brzezinski M, Leynaert A, Quéguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cy 9: 359-372.
39. Ottesen EA, Marin R, Preston CM, Young CR, Ryan JP, Scholin CA, Delong EF (2011) Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton. ISME J 5: 1881-1895.
40. Perry M (1976) Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in the oligotrophic waters of the central North Pacific. Limnol Oceanogr 21: 88-107.
41. Quisel JD, Wykoff DD, Grossman AR (1996) Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. Plant Physiol 111: 839-848.
42. Riegman R, Stolte W, Noordeloos A, Slezak D (2000) Nutrient uptake, and alkaline phosphate (EC 3: 1: 3: 1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. J Phycol 36: 87-96.
43. Ruttenberg K, Dyhrman S (2005) Temporal and spatial variability of dissolved organic and inorganic phosphorus, and metrics of phosphorus bioavailability in an upwelling-dominated coastal system. J Geophys Res-Oceans 110(10): C10S13.
44. Saade A, Bowler C (2009) Molecular tools for discovering the secrets of diatoms. Bioscience 59: 757-765.
45. Sebastian M, Ammerman JW (2009) The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J 3: 563-572.
46. Siaut M, Heijde M, Mangogna M, Montsant A, Coesel S, Allen A, Manfredonia A, Falciatore A, Bowler C (2007) Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene 406: 23-35.
47. Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45: 361-402.
48. Sorhannus U (2007) A nuclear-encoded small-subunit ribosomal RNA timescale for diatom evolution. Mar Micropaleontol 65: 1-12.
49. 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.
50. Xu Y, Wahlund TM, Feng L, Shaked Y, Morel FMM (2006) A novel alkaline phosphatase in the coccolithophore Emiliania huxleyi (Prymnesiophyceae) and its regulation by phosphorus. J Phycol 42: 835-844.
51. Yu Plisova E, Balabanova L, Ivanova E, Kozhemyako V, Mikhailov V, Agafonova E, Rasskazov V (2005) A highly active alkaline phosphatase from the marine bacterium Cobetia. Mar Biotechnol 7: 173-178.