全部 标题 作者
关键词 摘要

Marine Drugs  2013 

Evolution and Distribution of Saxitoxin Biosynthesis in Dinoflagellates

DOI: 10.3390/md11082814

Keywords: cyanobacteria, dinoflagellates, harmful algal blooms (HABs), horizontal gene transfer (HGT), phylogeny, paralytic shellfish poisoning (PSP), paralytic shellfish toxin (PST), saxitoxin, STX

Full-Text   Cite this paper   Add to My Lib

Abstract:

Numerous species of marine dinoflagellates synthesize the potent environmental neurotoxic alkaloid, saxitoxin, the agent of the human illness, paralytic shellfish poisoning. In addition, certain freshwater species of cyanobacteria also synthesize the same toxic compound, with the biosynthetic pathway and genes responsible being recently reported. Three theories have been postulated to explain the origin of saxitoxin in dinoflagellates: The production of saxitoxin by co-cultured bacteria rather than the dinoflagellates themselves, convergent evolution within both dinoflagellates and bacteria and horizontal gene transfer between dinoflagellates and bacteria. The discovery of cyanobacterial saxitoxin homologs in dinoflagellates has enabled us for the first time to evaluate these theories. Here, we review the distribution of saxitoxin within the dinoflagellates and our knowledge of its genetic basis to determine the likely evolutionary origins of this potent neurotoxin.

References

[1]  Taylor, F.J.R.; Hoppenrath, M.; Saldarriaga, J.F. Dinoflagellate diversity and distribution. Biodivers. Conserv. 2008, 17, 407–418, doi:10.1007/s10531-007-9258-3.
[2]  Hallegraeff, G.M. A review of harmful algal blooms and their apparent global increase. Phycologia 1993, 32, 79–99, doi:10.2216/i0031-8884-32-2-79.1.
[3]  Wiese, M.; D’Agostino, P.M.; Mihali, T.K.; Moffitt, M.C.; Neilan, B.A. Neurotoxic alkaloids: Saxitoxin and its analogs. Mar. Drugs 2010, 8, 2185–2211, doi:10.3390/md8072185.
[4]  Catterall, W.A.; Morrow, C.S.; Hartshorne, R.P. Neurotoxin binding to receptor sites associated with voltage sensitive sodium channels in intact, lysed, and detergent solubilized brain membranes. J. Biol. Chem. 1979, 254, 1379–1387.
[5]  Llewellyn, L.E. Saxitoxin, a toxic marine natural product that targets a multitude of receptors. Nat. Prod. Rep. 2006, 23, 200–222, doi:10.1039/b501296c.
[6]  Hallegraeff, G.M. Harmful Algal Blooms: A Global Overview. In Manual of Harmful Marine Microalgae; Hallegraeff, G.M., Anderson, D.M., Cembella, A.D., Eds.; International Oceanographic Commission (IOC) Manual and Guides UNESCO: Paris, France, 1995; pp. 1–22.
[7]  Hoagland, P.; Scatasta, S. The Economic Effects of Harmful Algal Blooms. In Ecology of Harmful Algae; Graneli, E., Turner, T., Eds.; Springer-Verlag: Dordrecht, The Netherlands, 2006; pp. 391–402.
[8]  Adl, S.M.; Simpson, A.G.B.; Lane, C.E.; Lukes, J.; Bass, D.; Bowser, S.S.; Brown, M.W.; Burki, F.; Dunthorn, M.; Hampl, V.; et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012, 59, 429–493, doi:10.1111/j.1550-7408.2012.00644.x.
[9]  Wu, D.Y.; Hugenholtz, P.; Mavromatis, K.; Pukall, R.; Dalin, E.; Ivanova, N.N.; Kunin, V.; Goodwin, L.; Wu, M.; Tindall, B.J.; et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 2009, 462, 1056–1060, doi:10.1038/nature08656.
[10]  Usup, G.; Ahmad, A.; Matsuoka, K.; Lim, P.T.; Leaw, C.P. Biology, ecology and bloom dynamics of the toxic marine dinoflagellate Pyrodinium bahamense. Harmful Algae 2012, 14, 301–312, doi:10.1016/j.hal.2011.10.026.
[11]  Gárate-Lizárraga, I.; Bustillos-Guzmán, J.J.; Morquecho, L.; Band-Schmidt, C.J.; Alonso-Rodriguez, R.; Erler, K.; Luckas, B.; Reyes-Salinas, A.; Góngora-González, D.T. Comparative paralytic shellfish toxin profiles in the strains of Gymnodinium catenatum Graham from the Gulf of California, Mexico. Mar. Pollut. Bull. 2005, 50, 211–217, doi:10.1016/j.marpolbul.2004.11.034.
[12]  Hallegraeff, G.M. Harmful Algal Blooms: A Global Overview. In Manual on Harmful Marine Microalgae; Hallegraeff, G.M., Anderson, D.M., Cembella, A.D., Eds.; Imprimerie Landais: Paris, France, 2005; pp. 25–49.
[13]  Cembella, A.D. Ecophysiology and Metabolism of Paralytic Shellfish Toxins in Marine Microalgae. In Physiological Ecology of Harmful Algal Blooms; Anderson, D.M., Cembella, A.D., Hallegraeff, G.M., Eds.; Springer: Berlin, Germany, 1998; pp. 381–403.
[14]  Yang, I.; John, U.; Beszteri, S.; Glockner, G.; Krock, B.; Goesmann, A.; Cembella, A.D. Comparative gene expression in toxic versus non-toxic strains of the marine dinoflagellate Alexandrium minutum. BMC Genomics 2010, 11, doi:10.1186/1471-2164-11-248.
[15]  Orr, R.J.S.; Stüken, A.; Rundberget, T.; Eikrem, W.; Jakobsen, K.S. Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach. Harmful Algae 2011, 10, 676–688, doi:10.1016/j.hal.2011.05.003.
[16]  Murray, S.A.; Mihali, T.K.; Neilan, B.A. Extraordinary conservation, gene loss, and positive selection in the evolution of an ancient neurotoxin. Mol. Biol. Evol. 2011, 28, 1173–1182, doi:10.1093/molbev/msq295.
[17]  Kodama, M.; Ogata, T.; Sato, S. Bacterial production of saxitoxin. Agric. Biol. Chem. 1988, 52, 1075–1077, doi:10.1271/bbb1961.52.1075.
[18]  Plumley, F.G. Purification of an enzyme involved in saxitoxin synthesis. J. Phycol. 2001, 37, 926–928, doi:10.1046/j.1529-8817.2001.37601.x.
[19]  Schopf, J.W. The Fosil Record: Tracing the Roots of the Cyanobacterial Lineage. In The Ecology of Cyanobacteria: Their Diversity in Time and Space; Whitton, B.A., Potts, M., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2000; pp. 13–35.
[20]  Moustafa, A.; Loram, J.E.; Hackett, J.D.; Anderson, D.M.; Plumley, F.G.; Bhattacharya, D. Origin of saxitoxin biosynthetic genes in cyanobacteria. PLoS One 2009, 4, e5758.
[21]  Kellmann, R.; Mihali, T.K.; Jeon, Y.J.; Pickford, R.; Pomati, F.; Neilan, B.A. Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl. Environ. Microbiol. 2008, 74, 4044–4053, doi:10.1128/AEM.00353-08.
[22]  Stüken, A.; Orr, R.J.S.; Kellmann, R.; Murray, S.A.; Neilan, B.A.; Jakobsen, K.S. Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS One 2011, 6, e20096.
[23]  Hackett, J.D.; Wisecaver, J.H.; Brosnahan, M.L.; Kulis, D.M.; Anderson, D.M.; Bhattacharya, D.; Plumley, F.G.; Erdner, D.L. Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol. Biol. Evol. 2013, 30, 70–78, doi:10.1093/molbev/mss142.
[24]  Kellmann, R.; Stüken, A.; Orr, R.J.S.; Svendsen, H.M.; Jakobsen, K.S. Biosynthesis and molecular genetics of polyketides in marine dinoflagellates. Mar. Drugs 2010, 8, 1011–1048, doi:10.3390/md8041011.
[25]  Shimizu, Y. Microalgal metabolites: A new perspective. Annu. Rev. Microbiol. 1996, 50, 431–465, doi:10.1146/annurev.micro.50.1.431.
[26]  Harlow, L.D.; Koutoulis, A.; Hallegraeff, G.M. S-Adenosylmethionine synthetase genes from eleven marine dinoflagellates. Phycologia 2007, 46, 46–53, doi:10.2216/06-28.1.
[27]  Hackett, J.D.; Scheetz, T.E.; Yoon, H.S.; Soares, M.B.; Bonaldo, M.F.; Casavant, T.L.; Bhattacharya, D. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 2005, 6, doi:10.1186/1471-2164-6-80.
[28]  Orr, R.J.S.; Stüken, A.; Murray, S.A.; Jakobsen, K.S. Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: The second “core” gene—sxtG. Appl. Environ. Microbiol. 2013, 79, 2128–2136, doi:10.1128/AEM.03279-12.
[29]  Silva, E.S. Intracellular bacteria: The origin of dinoflagellate toxicity. J. Environ. Pathol. Toxicol. 1990, 10, 124–128.
[30]  Green, D.H.; Llewellyn, L.E.; Negri, A.P.; Blackburn, S.I.; Bolch, C.J.S. Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum. FEMS Microbiol. Ecol. 2004, 47, 345–357, doi:10.1016/S0168-6496(03)00298-8.
[31]  Wichels, A.; Hummert, C.; Elbrachter, M.; Luckas, B.; Schutt, C.; Gerdts, G. Bacterial diversity in toxic Alexandrium tamarense blooms off the Orkney Isles and the Firth of Forth. Helgol. Mar. Res. 2004, 58, 93–103, doi:10.1007/s10152-004-0174-6.
[32]  Martins, C.A.; Alvito, P.; Tavares, M.J.; Pereira, P.; Doucette, G.; Franca, S. Reevaluation of production of paralytic shellfish toxin by bacteria associated with dinoflagellates of the Portuguese coast. Appl. Environ. Microbiol. 2003, 69, 5693–5698, doi:10.1128/AEM.69.9.5693-5698.2003.
[33]  Lu, Y.H.; Chai, T.J.; Hwang, D.F. Isolation of bacteria from toxic dinoflagellate Alexandrium minutum and their effects on algae toxicity. J. Nat. Toxins 2000, 9, 409–417.
[34]  Baker, T.R.; Doucette, G.J.; Powell, C.L.; Boyer, G.L.; Plumley, F.G. GTX(4) imposters: Characterization of fluorescent compounds synthesized by Pseudomonas stutzeri SF/PS and Pseudomonas/Alteromonas PTB-1, symbionts of saxitoxin-producing Alexandrium spp. Toxicon 2003, 41, 339–347, doi:10.1016/S0041-0101(02)00314-8.
[35]  Hold, G.L.; Smith, E.A.; Birkbeck, T.H.; Gallacher, S. Comparison of paralytic shellfish toxin (PST) production by the dinoflagellates Alexandrium lusitanicum NEPCC 253 and Alexandrium tamarense NEPCC 407 in the presence and absence of bacteria. FEMS Microbiol. Ecol. 2001, 36, 223–234, doi:10.1111/j.1574-6941.2001.tb00843.x.
[36]  Palacios, L.; Reguera, B.; Franco, J.; Marin, I. Phylogenetic diversity of bacteria associated with toxic and non-toxic strains of Alexandrium minutum. Afr. J. Mar. Sci. 2006, 28, 409–414, doi:10.2989/18142320609504188.
[37]  Pichersky, E.; Gang, D.R. Genetics and biochemistry of secondary metabolites in plants: An evolutionary perspective. Trends Plant Sci. 2000, 5, 439–445, doi:10.1016/S1360-1385(00)01741-6.
[38]  Lukes, J.; Leander, B.S.; Keeling, P.J. Cascades of convergent evolution: The corresponding evolutionary histories of euglenozoans and dinoflagellates. Proc. Natl. Acad. Sci. USA 2009, 106, 9963–9970, doi:10.1073/pnas.0901004106.
[39]  Gough, J. Convergent evolution of domain architectures (is rare). Bioinformatics 2005, 21, 1464–1471, doi:10.1093/bioinformatics/bti204.
[40]  Jost, M.C.; Hillis, D.M.; Lu, Y.; Kyle, J.W.; Fozzard, H.A.; Zakon, H.H. Toxin-resistant sodium channels: Parallel adaptive evolution across a complete gene family. Mol. Biol. Evol. 2008, 25, 1016–1024, doi:10.1093/molbev/msn025.
[41]  De la Cruz, F.; Davies, J. Horizontal gene transfer and the origin of species: Lessons from bacteria. Trends Microbiol. 2000, 8, 128–133, doi:10.1016/S0966-842X(00)01703-0.
[42]  Keeling, P.J.; Palmer, J.D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 2008, 9, 605–618, doi:10.1038/nrg2386.
[43]  Yoon, H.S.; Hackett, J.D.; van Dolah, F.M.; Nosenko, T.; Lidie, K.L.; Bhattacharya, D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 2005, 22, 1299–1308, doi:10.1093/molbev/msi118.
[44]  Morse, D.; Salois, P.; Markovic, P.; Hastings, J.W. A nuclear-encoded form II RuBisCO in dinoflagellates. Science 1995, 268, 1622–1624.
[45]  Wong, J.T.Y.; New, D.C.; Wong, J.C.W.; Hung, V.K.L. Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Eukaryot. Cell 2003, 2, 646–650, doi:10.1128/EC.2.3.646-650.2003.
[46]  Singh, S.P.; Hader, D.P.; Sinha, R.P. Bioinformatics evidence for the transfer of mycosporine-like amino acid core (4-deoxygadusol) synthesizing gene from cyanobacteria to dinoflagellates and an attempt to mutate the same gene (YP_324358) in Anabaena variabilis PCC 7937. Gene 2012, 500, 155–163, doi:10.1016/j.gene.2012.03.063.
[47]  Silva, E.S. Relationship between dinoflagellates and intracellular bacteria. Mar. Algae Pharmacol. Sci. 1982, 2, 269–288.
[48]  Hotopp, J.C.D.; Clark, M.E.; Oliveira, D.C.S.G.; Foster, J.M.; Fischer, P.; Torres, M.C.; Giebel, J.D.; Kumar, N.; Ishmael, N.; Wang, S.L.; et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317, 1753–1756, doi:10.1126/science.1142490.
[49]  Stüken, A.; Jakobsen, K.S. The cylindrospermopsin gene cluster of Aphanizomenon sp. strain 10E6: Organization and recombination. Microbiology 2010, 156, 2438–2451, doi:10.1099/mic.0.036988-0.
[50]  Salcedo, T.; Upadhyay, R.J.; Nagasaki, K.; Bhattacharya, D. Dozens of toxin-related genes are expressed in a nontoxic strain of the dinoflagellate Heterocapsa circularisquama. Mol. Biol. Evol. 2012, 29, 1503–1506, doi:10.1093/molbev/mss007.
[51]  Orr, R.J.S.; Murray, S.; Stüken, A.; Rhodes, L.; Jakobsen, K.S. When naked became armored: An eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS One 2012, 7, e50004.
[52]  Lilly, E.L.; Halanych, K.M.; Anderson, D.M. Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol. 2007, 43, 1329–1338, doi:10.1111/j.1529-8817.2007.00420.x.
[53]  Murray, S.A.; Wiese, M.; Neilan, B.A.; Orr, R.J.S.; de Salas, M.; Brett, S.; Hallegraeff, G. A reinvestigation of saxitoxin production and sxtA in the “non-toxic” Alexandrium tamarense Group V clade. Harmful Algae 2012, 18, 96–104, doi:10.1016/j.hal.2012.05.001.
[54]  Murray, S.A.; Wiese, M.; Stüken, A.; Brett, S.; Kellmann, R.; Hallegraeff, G.; Neilan, B.A. SxtA-based quantitative molecular assay to identify saxitoxin-producing harmful algal blooms in marine waters. Appl. Environ. Microbiol. 2011, 77, 7050–7057, doi:10.1128/AEM.05308-11.
[55]  Suikkanen, S.; Kremp, A.; Hautala, H.; Krock, B. Paralytic shellfish toxins or spirolides? The role of environmental and genetic factors in toxin production of the Alexandrium ostenfeldii complex. Harmful Algae 2013, 26, 52–59, doi:10.1016/j.hal.2013.04.001.
[56]  Hii, K.S.; Lim, P.T.; Tan, T.H.; Leaw, C.P. Characterization of the Saxitoxin Biosynthetic Starting Gene, sxta in the Toxic Dinoflagellate Alexandrium tamiyavanichii. In Proceedins of The 12th Symposium of the Malaysian Society of Applied Biology: Solutions to Global Challenges and Issues, Kuala Terengganu, Malaysia, 1–3 June 2012; pp. 196–202.
[57]  Wang, D.-Z.; Li, C.; Zhang, Y.; Wang, Y.-Y.; He, Z.-P.; Lin, L.; Hong, H.-S. Quantitative proteomic analysis of differentially expressed proteins in the toxicity-lost mutant of Alexandrium catenella (Dinophyceae) in the exponential phase. J. Proteomics 2012, 75, 5564–5577, doi:10.1016/j.jprot.2012.08.001.
[58]  Callahan, B.; Thattai, M.; Shraiman, B.I. Emergent gene order in a model of modular polyketide synthases. Proc. Natl. Acad. Sci. USA 2009, 106, 19410–19415, doi:10.1073/pnas.0902364106.
[59]  Doekel, S.; Marahiel, M.A. Biosynthesis of natural products on modular peptide synthetases. Metab. Eng. 2001, 3, 64–77, doi:10.1006/mben.2000.0170.
[60]  Zhang, H.; Hou, Y.B.; Miranda, L.; Campbell, D.A.; Sturm, N.R.; Gaasterland, T.; Lin, S.J. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA 2007, 104, 4618–4623.

Full-Text

comments powered by Disqus