A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1756, 2013, Pages

  Marron, Alan O ^a   Alston, Mark J ^b   Heavens, Darren ^b   Akam, Michael ^a   Caccamo, Mario ^b   Holland, Peter W H ^c   Walker, Giselle ^d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b EARLHAM INSTITUTE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Biomineralization; Choanoflagellate; Diatom; Lateral gene transfer; Silicon transporter; Sit transport model

Indexed keywords

BIOCHEMICAL COMPOSITION; BIOMINERALIZATION; DIATOM; FLAGELLATE; GENE TRANSFER; GENOME; PHYLOGENETICS; PROTEIN; SILICON;

BACILLARIOPHYTA; CHOANOFLAGELLIDA; DIAPHANOECA GRANDIS; EUKARYOTA; STEPHANOECA DIPLOCOSTATA; STRAMENOPILES;

EID: 84878367070     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2543     Document Type: Article

References (74)

1. Simkiss K, Wilbur KM. 1989 Biomineralization: cell biology and mineral deposition. San Diego, CA: Academic Press Inc.
2. Gröger C, Lutz K, Brunner E. 2008 Biomolecular self-assembly and its relevance in silica biomineralization. Cell Biochem. Biophys. 50, 23-39. (doi:10.1007/s12013-007-9003-2)
3. Maldonado M, Carmona MC, Cruzado A. 1999 Decline in Mesozoic reef-building in sponges explained by silicon limitation. Nature 401, 785-788. (doi:10.1038/44560).
4. Hildebrand M, Higgins DR, Busser K, Volcani BE. 1993 Silicon-responsive cDNA clones isolated from the marine diatom Cylindrotheca fusiformis. Gene 132, 213-218. (doi:10.1016/0378- 1119(93)90198-C)
5. Jugdaohsingh R. 2009 Silicon and bone health. J. Nutr. Health Aging 11, 99-110.
6. Hildebrand M, Volcani BE, Gassman W, Schroeder J. 1997 A gene family of silicon transporters. Nature 385, 688-689. (doi:10.1038/385688b0)
7. Thamatrakoln K, Hildebrand M. 2007 Analysis of Thalassiosira pseudonana silicon transporters indicates distinct regulatory levels and transport activity through the cell cycle. Eukaryot. Cell 6, 271-279. (doi:10.1128/EC.00235-06)
8. Likhoshway YV, Masyukova YA, Sherbakova TA, Petrova DP, Grachev AMA. 2006 Detection of the gene responsible for silicic acid transport in chrysophycean algae. Dokl. Biol. Sci. 408, 256-260. (doi:10.1134/S001249660603015X)
9. Yamaji N, Ma JF. 2009 A transporter at the node responsible for intervascular transfer of silicon in rice. Plant Cell 21, 2878-2883. (doi:10.1105/tpc. 109.069831)
10. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M. 2006 A silicon transporter in rice. Nature 440, 688-691. (doi:10.1038/nature04590)
11. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M. 2007 An efflux transporter of silicon in rice. Nature 448, 209-213. (doi:10.1038/nature05964)
12. Schröder H-C, Perović-Ottstadt S, Rothenberger M, Wiens M, Schwertner H, Batel R, Korzhev M, Müller IM, Müller WEG. 2004 Silica transport in the demosponge Suberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter. Biochem. J. 381, 665-673. (doi:10.1042/BJ20040463)
13. Thamatrakoln K, Alverson AJ, Hildebrand M. 2006 Comparative sequence analysis of diatom silicon transporters: toward a mechanistic model of silicon transport. J. Phycol. 42, 822-834. (doi:10.1111/j. 1529-8817.2006.00233.x)
14. Mitani-Ueno N, Yamaji N, Zhao F-J, Ma JF. 2011 The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J. Exp. Bot. 62, 4391-4398. (doi:10.1093/jxb/err158)
15. King N et al. 2008 The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788. (doi:10.1038/ nature06617)
16. Torruella G, Derelle R, Jordi P, Lang BF, Andrew R, Shalchian-Tabrizi K, Iñaki R-T. 2012 Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains. Mol. Biol. Evol. 29, 531-544. (doi:10.1093/molbev/msr185).
17. Nitsche F, Carr M, Arndt H, Leadbeater BSC. 2011 Higher level taxonomy and molecular phylogenetics of the choanoflagellatea. J. Eukaryot. Microbiol. 58, 452-462. (doi:10.1111/j.1550-7408.2011.00572.x)
18. Mann S, Williams RJP. 1982 High resolution electron microscopy studies of the silica lorica in the choanoflagellate Stephanoeca diplocostata Ellis. Proc. R. Soc. Lond. B 216, 137-146. (doi:10.1098/ rspb.1982.0066)
19. Leadbeater BSC. 1979 Developmental studies on the loricate choanoflagellate Stephanoeca diplocostata Ellis. I. Ultrastructure of the non-dividing cell and costal strip production. Protoplasma 262, 241-262. (doi:10.1007/BF01281442)
20. Leadbeater BSC, Yu Q, Kent J, Stekel DJ. 2009 Three-dimensional images of choanoflagellate loricae. Proc. R. Soc. B 276, 3-11. (doi:10.1098/ rspb.2008.0844)
21. Leadbeater BSC. 1985 Developmental studies on the loricate choanoflagellate Stephanoeca diplocostata Ellis. IV. Effects of silica deprivation on growth and loricate production. Protoplasma 127, 171-179. (doi:10.1007/BF01276261)
22. Leadbeater BSC, Cheng R. 2010 Costal strip production and lorica assembly in the large tectiform choanoflagellate Diaphanoeca grandis Ellis. Eur. J. Protistol. 46, 96-110. (doi:10.1016/j. ejop.2009.12.003)
23. Leadbeater BSC. 1989 Developmental studies on the loricate choanoflagellate Stephanoeca diplocostata Ellis. VI. Effects of silica replenishment on silica impoverished cells. Protoplasma 153, 71-84. (doi:10.1007/BF01322467)
24. Leadbeater BSC. 1987 Developmental studies on the loricate choanoflagellate Stephanoeca diplocostata Ellis. V. The cytoskeleton and the effects of microtubule poisons. Protoplasma 136, 1-15. (doi:10.1007/BF01276313)
25. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (doi:10.1093/nar/25.17.3389)
26. Doyle J, Doyle J. 1987 A rapid DNA isolation method for small quantities of fresh tissues. Phytochem. Bull. 19, 11-15.
27. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007 WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587. (doi:10.1093/nar/gkm259)
28. Hoffman K, Stoffel W. 1993 TMbase: a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 374, 166.
29. Tusnády GE, Simon I. 2001 The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850. (doi:10.1093/ bioinformatics/17.9.849)
30. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001 Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580. (doi:10.1006/jmbi.2000.4315)
31. Sapriel G, Quinet M, Heijde M, Jourdren L, Crom L, Lopez PJ. 2009 Genome-wide transcriptome analyses of silicon metabolism in Phaeodactylum tricornutum reveal the multilevel regulation of silicic acid transporters. PLoS ONE 4, e7458. (doi:10.1371/ journal.pone.0007458)
32. Abascal F, Zardoya R, Posada D. 2005 ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105. (doi:10.1093/ bioinformatics/bti263)
33. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010 New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. (doi:10.1093/ sysbio/syq010)
34. Stamatakis A, Hoover P, Rougemont J. 2008 A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57, 758-771. (doi:10.1080/ 10635150802429642)
35. Huelsenbeck JP, Ronquist F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. (doi:10.1093/ bioinformatics/17.8.754)
36. Sherbakova TA et al. 2005 Conserved motif CMLD in silicic acid transport proteins of diatoms. Mol. Biol. 39, 269-280. (doi:10.1007/s11008-005-0038-4)
37. Walker G, Dorrell RG, Schlacht A, Dacks JB. 2011 Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology 138, 1638-1663. (doi:10.1017/S0031182010001708)
38. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N. 2011 Cell differentiation and morphogenesis in the colonyforming choanoflagellate Salpingoeca rosetta. Dev. Biol. 357, 73-82. (doi:10.1016/j.ydbio.2011. 06.003)
39. Snell EA, Brooke NM, Taylor WR, Casane D, Philippe H, Holland PWH. 2006 An unusual choanoflagellate protein released by Hedgehog autocatalytic processing. Proc. R. Soc. B 273, 401-407. (doi:10. 1098/rspb.2005.3263)
40. Hildebrand M, Dahlin K, Volcani BE. 1998 Characterization of a silicon transporter gene family in Cylindrotheca fusiformis: sequences, expression analysis, and identification of homologs in other diatoms. Mol. Gen. Genet. 260, 480-486. (doi:10. 1007/s004380050920)
41. Alverson AJ. 2007 Strong purifying selection in the silicon transporters of marine and freshwater diatoms. Plant Biol. 52, 1420-1429.
42. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016. (doi:10.1006/jmbi. 2000.3903)
43. Martin-Jézéquel V, Hildebrand M, Brzezinski MA. 2000 Silicon metabolism in diatoms: implications for growth. J. Phycol. 36, 821-840. (doi:10.1046/j. 1529-8817.2000.00019.x)
44. Finkel ZV, Kotrc B. 2010 Silica use through time: macroevolutionary change in the morphology of the diatom fustule. Geomicrobiol. J. 27, 596-608. (doi:10.1080/01490451003702941)
45. Abramson J, Wright EM. 2009 Structure and function of Na{thorn}-symporters with inverted repeats. Curr. Opin. Struct. Biol. 19, 425-432. (doi:10.1016/ j.sbi.2009.06.002)
46. Boudker O, Verdon G. 2010 Structural perspectives on secondary active transporters. Trends Pharmacol. Sci. 31, 418-426. (doi:10.1016/j.tips.2010.06.004)
47. Khafizov K, Staritzbichler R, Stamm M, Forrest LR. 2010 A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49, 10702-10713. (doi:10.1021/ bi101256x)
48. Thamatrakoln K, Hildebrand M. 2008 Silicon uptake in diatoms revisited: a model for saturable and nonsaturable uptake kinetics and the role of silicon transporters. Plant Physiol. 146, 1397-1407. (doi:10.1104/pp.107.107094)
49. Krishnamurthy H, Piscitelli CL, Gouaux E. 2009 Unlocking the molecular secrets of sodium-coupled transporters. Nature 459, 347-355. (doi:10.1038/ nature08143)
50. Screpanti E, Hunte C. 2007 Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261-267. (doi:10.1016/j.jsb.2007.01.011)
51. Bhattacharyya PEB, Volcani BE. 1980 Sodiumdependent silicate transport in the apochlorotic marine diatom Nitzschia alba. Proc. Natl Acad. Sci. USA 77, 6386-6390. (doi:10.1073/pnas.77. 11.6386)
52. Curnow P, Senior L, Knight MJ, Thamatrakoln K, Hildebrand M, Booth PJ. 2012 Expression, purification, and reconstitution of a diatom silicon transporter. Biochemistry 51, 3776-3785. (doi:10. 1021/bi3000484)
53. Leadbeater BSC. 2008 Choanoflagellate evolution: the morphological perspective. Protistology 5, 256-267.
54. Paul M. 2012 Acanthocorbis mongolica nov. spec.-description of the first freshwater loricate choanoflagellate (Acanthoecida) from a Mongolian lake. Eur. J. Protistol. 48, 1-8. (doi:10.1016/j.ejop. 2011.07.001)
55. Ruiz-Trillo I, Burger G, Holland PWH, King N, Lang BF, Roger AJ, Gray MW. 2007 The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 23, 113-118. (doi:10.1016/j.tig.2007. 01.005)
56. Gobler CJ et al. 2011 Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc. Natl Acad. Sci. USA 108, 4352-4357. (doi:10.1073/pnas.1016106108)
57. Sun G, Yang Z, Ishwar A, Huang J. 2010 Algal genes in the closest relatives of animals. Mol. Biol. Evol. 27, 2879-2889. (doi:10.1093/molbev/msq175)
58. Bowler C et al. 2008 The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244. (doi:10.1038/nature07410)
59. Keeling PJ, Palmer JD. 2008 Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618. (doi:10.1038/nrg2386)
60. Nedelcu AM, Blakney JC, Logue KD. 2009 Functional replacement of a primary metabolic pathway via multiple independent eukaryote-to-eukaryote gene transfers and selective retention. J. Evol. Biol. 22, 1882-1894. (doi:10.1111/j.1420-9101.2009.01797.x)
61. Tucker RP, Beckmann J, Leachman NT, Schöler J. 2012 Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol. Biol. Evol. 29, 1019-1029. (doi:10.1093/ molbev/msr271).
62. Michael AJ. 2011 Molecular machines encoded by bacterially-derived multi-domain gene fusions that potentially synthesize, N-methylate and transfer long chain polyamines in diatoms. FEBS Lett. 585, 2627-2634. (doi:10.1016/j.febslet.2011.07.038)
63. Mock T et al. 2008 Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc. Natl Acad. Sci. USA 105, 1579-1584. (doi:10.1073/pnas.0707946105)
64. Macdonald FA, Cohen PA, Dudas F, Schrag DP. 2010 Early Neoproterozoic scale microfossils in the Lower Tindir Group of Alaska and the Yukon Territory. Geology 38, 143-146. (doi:10.1130/G25637.1)
65. Parfrey LW, Lahr DJG, Knoll AH, Katz L. 2011 Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624-13629. (doi:10.1073/pnas.1110633108)
66. Poulsen N, Sumper M, Kroger N. 2003 Biosilica formation in diatoms: characterization of native silaffin-2 and its role in silica morphogenesis. Proc. Natl Acad. Sci. USA 100, 12075-12080. (doi:10. 1073/pnas.2035131100)
67. Wenzl S, Hett R, Richthammer P, Sumper M. 2008 Silacidins: highly acidic phosphopeptides from diatom shells assist in silica precipitation in vitro. Angew. Chem. 47, 1729-1732. (doi:10.1002/ anie.200704994)
68. Shimizu K, Cha J, Stucky GD, Morse DE. 1998 Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc. Natl Acad. Sci. USA 95, 6234-6238. (doi:10.1073/pnas.95.11.6234)
69. Gong N, Wiens M, Schröder HC, Mugnaioli E, Kolb U, Müller WEG. 2010 Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata. J. Exp. Biol. 213, 3575-3585. (doi:10. 1242/jeb.048496)
70. Zardoya R, Ding X, Kitagawa Y, Chrispeels MJ. 2002 Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc. Natl Acad. Sci. USA 99, 14893-14896. (doi:10.1073/ pnas.192573799)
71. Kinrade SD. 1999 Stable five- and six-coordinated silicate anions in aqueous solution. Science 285, 1542-1545. (doi:10.1126/science.285. 5433.1542)
72. Hamm CE, Merkel R, Springer O, Jurkojc P. 2003 Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421, 841-843. (doi:10.1038/ nature01416).
73. Ehrlich H et al. 2010 Mineralization of the metrelong biosilica structures of glass sponges is templated on hydroxylated collagen. Nat. Chem. 2, 1084-1088. (doi:10.1038/nchem.899)
74. Coradin T, Livage J. 2003 Interactions of bovine serum albumin and lysozyme with sodium silicate solutions. Colloids Surf. 29, 189-196. (doi:10.1016/ S0927-7765(02)00208-4)