Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: The second "core" gene, sxtG

Applied and Environmental Microbiology

Volumn 79, Issue 7, 2013, Pages 2128-2136

  Orr, Russell J S ^a   Stüken, Anke ^a   Murray, Shauna A ^b,c   Jakobsen, Kjetill S ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXANDRIUM; ALEXANDRIUM FUNDYENSE; ALEXANDRIUM MINUTUM; EVOLUTIONARY ACQUISITION; GENOMIC SEQUENCE; HORIZONTAL GENE TRANSFER; LEADER SEQUENCE; PHYLOGENETIC INFERENCE;

BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; GENE TRANSFER;

GENES;

AMIDINOTRANSFERASE; SAXITOXIN;

BACTERIUM; DINOFLAGELLATE; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; PHYLOGENETICS; TOXIN;

ARTICLE; BIOSYNTHESIS; CLUSTER ANALYSIS; DINOFLAGELLATE; DNA SEQUENCE; GENE DELETION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY;

AMIDINOTRANSFERASES; BIOSYNTHETIC PATHWAYS; CLUSTER ANALYSIS; DINOFLAGELLIDA; EVOLUTION, MOLECULAR; GENE DELETION; GENE TRANSFER, HORIZONTAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SAXITOXIN; SEQUENCE ANALYSIS, DNA;

ALEXANDRIUM; ALEXANDRIUM FUNDYENSE; ALEXANDRIUM MINUTUM; BACTERIA (MICROORGANISMS); CYANOBACTERIA; DINOPHYCEAE; EUKARYOTA; GYMNODINIUM CATENATUM;

EID: 84875517957     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03279-12     Document Type: Article

References (52)

1. Taylor FJR. 1987. General group characteristics, special features of interest, short history of dinoflagellate study, p 798. In Taylor FJR (ed), The biology of dinoflagellates. Botanical monographs, vol 21. Blackwell Scientific Publications, Oxford, United Kingdom.
2. Hallegraeff GM. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.
3. Deeds JR, Landsberg JH, Etheridge SM, Pitcher GC, Longan SW. 2008. Non-traditional vectors for paralytic shellfish poisoning. Mar. Drugs 6:308-348.
4. Wiese M, D'Agostino PM, Mihali TK, Moffitt MC, Neilan BA. 2010. Neurotoxic alkaloids: saxitoxin and its analogs. Mar. Drugs 8:2185-2211.
5. Orr RJS, Stüken A, Rundberget T, Eikrem W, Jakobsen KS. 2011. Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach. Harmful Algae 10:676-688.
6. Alam M, Ikawa M, Sasner JJ, Sawyer PJ. 1973. Purification of Aphanizomenon flos-aquae toxin and its chemical and physiological properties. Toxicon 11:65-72.
7. Schantz EJ, Lynch JM, Vayvada G, Matsumot K, Rapoport H. 1966. Purification and characterization of poison produced by Gonyaulax catenella in axenic culture. Biochemistry 5:1191-1195.
8. Smith JL, Boyer GL, Zimba PV. 2008. A review of cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture 280:5-20.
9. Shimizu Y. 1996. Microalgal metabolites: a new perspective. Annu. Rev. Microbiol. 50:431-465.
10. Shimizu Y. 1993. Microalgal metabolites. Chem. Rev. 93:1685-1698.
11. Kellmann R, Stüken A, Orr RJS, Svendsen HM, Jakobsen KS. 2010. Biosynthesis and molecular genetics of polyketides in marine dinoflagellates. Mar. Drugs 8:1011-1048.
12. Mihali T, Kellmann R, Neilan B. 2009. Characterisation of the paralytic shellfish toxin biosynthesis gene clusters in Anabaena circinalis AWQC131C and Aphanizomenon sp. NH-5. BMC Biochem. 10:8. doi:10 .1186/1471-2091-10-8.
13. Moustafa A, Loram JE, Hackett JD, Anderson DM, Plumley FG, Bhattacharya D. 2009. Origin of saxitoxin biosynthetic genes in cyanobacteria. PLoS One 4:e5758. doi:10.1371/journal.pone.0005758.
14. Kellmann R, Mihali TK, Jeon YJ, Pickford R, Pomati F, Neilan BA. 2008. Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl. Environ. Microbiol. 74: 4044-4053.
15. Stucken K, John U, Cembella A, Murillo AA, Soto-Liebe K, Fuentes- Valdes JJ, Friedel M, Plominsky AM, Vasquez M, Glockner G. 2010. The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One 5:e9235. doi:10.1371/journal.pone.0009235.
16. Mihali TK, Carmichael WW, Neilan BA. 2011. A putative gene cluster from a Lyngbya wollei bloom that encodes paralytic shellfish toxin biosynthesis. PLoS One 6:e14657. doi:10.1371/journal.pone.0014657.
17. Murray SA, Mihali TK, Neilan BA. 2011. Extraordinary conservation, gene loss, and positive selection in the evolution of an ancient neurotoxin. Mol. Biol. Evol. 28:1173-1182.
18. Stüken A, Orr RJS, Kellmann R, Murray SA, Neilan BA, Jakobsen KS. 2011. Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS One 6:e20096. doi:10.1371/journal.pone.0020096.
19. Zhang H, Hou YB, Miranda L, Campbell DA, Sturm NR, Gaasterland T, Lin SJ. 2007. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. U. S. A. 104:4618-4623.
20. Kodama M, Ogata T, Sakamoto S, Sato S, Honda T, Miwatani T. 1990. Production of paralytic shellfish toxins by a bacterium Moraxella sp. isolated from Protogonyaulax tamarensis. Toxicon 28:707-714.
21. Gallacher S, Flynn KJ, Franco JM, Brueggemann EE, Hines HB. 1997. Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp (Dinophyta) in culture. Appl. Environ. Microbiol. 63:239-245.
22. Vasquez M, Gruttner C, Gallacher S, Moore ERB. 2001. Detection and characterization of toxigenic bacteria associated with Alexandrium catenella and Aulacomya ater contaminated with PSP. J. Shellfish Res. 20: 1245-1249.
23. Murray SA, Wiese M, Neilan BA, Orr RJS, de Salas M, Brett S, Hallegraeff G. 2012. A reinvestigation of saxitoxin production and sxtA in the 'non-toxic' Alexandrium tamarense Group V clade. Harmful Algae 18:96-104.
24. Murray SA, Wiese M, Stüken A, Brett S, Kellmann R, Hallegraeff G, Neilan BA. 2011. sxtA-based quantitative molecular assay to identify saxitoxin- producing harmful algal blooms in marine waters. Appl. Environ. Microbiol. 77:7050-7057.
25. Guillard RRL, Hargraves PE. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236.
26. Blackburn SI, Bolch CJS, Haskard KA, Hallegraeff GM. 2001. Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycologia 40:78-87.
27. Hendriks L, Goris A, Neefs JM, Van de Peer Y, Hennebert G, Dewachter R. 1989. The nucleotide sequence of the small ribosomal-subunit RNA of the yeast Candida albicans and the evolutionary position of the Fungi among the Eukaryotes. Syst. Appl. Microbiol. 12:223-229.
28. Medlin L, Elwood HJ, Stickel S, Sogin ML. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491-499.
29. Gadberry MD, Malcomber ST, Doust AN, Kellogg EA. 2005. Primaclade- a flexible tool to find conserved PCR primers across multiple species. Bioinformatics 21:1263-1264.
30. Kibbe WA. 2007. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 35:W43-W46.
31. Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202.
32. Maddison WP, Maddison DR. 2000. MacClade, 4th ed. Sinauer Associates, Sunderland, MA.
33. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301.
34. Min XJ, Butler G, Storms R, Tsang A.2005. OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 33: W677-W680.
35. Katoh K, Toh H. 2008. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinform. 9:212. doi:10.1186/1471-2105-9-212.
36. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104-2105.
37. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
38. Kumar S, Skjaeveland A, Orr RJS, Enger P, Ruden T, Mevik BH, Burki F, Botnen A, Shalchian-Tabrizi K. 2009. AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinform. 10:357. doi:10.1186/1471-2105-10-357.
39. Galluzzi L, Penna A, Bertozzini E, Vila M, Garcés E, Magnani M. 2004. Development of a real-time PCR assay for rapid detection and quantification of Alexandrium minutum (a dinoflagellate). Appl. Environ. Microbiol. 70:1199-1206.
40. Lilly EL, Halanych KM, Anderson DM. 2007. Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol. 43:1329-1338.
41. Muenchhoff J, Siddiqui KS, Poljak A, Raftery MJ, Barrow KD, Neilan BA. 2010. A novel prokaryotic L-arginine:glycine amidinotransferase is involved in cylindrospermopsin biosynthesis. FEBS J. 277:3844-3860.
42. Slamovits CH, Keeling PJ. 2008. Widespread recycling of processed cDNAs in dinoflagellates. Curr. Biol. 18:R550 -R552.
43. Okamoto OK, Liu LY, Robertson DL, Hastings JW. 2001. Members of a dinoflagellate luciferase gene family differ in synonymous substitution rates. Biochemistry 40:15862-15868.
44. Rowan R, Whitney SM, Fowler A, Yellowlees D. 1996. Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8:539-553.
45. Zhang H, Lin SJ. 2003. Complex gene structure of the form II RUBISCO in the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol. 39:1160-1171.
46. Hoppenrath M, Leander BS. 2010. Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS One 5:e13220. doi:10.1371/journal.pone.0013220.
47. Bachvaroff TR, Place AR. 2008. From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 3:e2929. doi:10.1371/journal.pone.0002929.
48. Kim S, Bachvaroff TR, Handy SM, Delwiche CF. 2011. Dynamics of actin evolution in dinoflagellates. Mol. Biol. Evol. 28:1469-1480.
49. LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW. 2005. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J. Phycol. 41:880-886.
50. Orr RJS, Murray S, Stüken A, Rhodes L, Jakobsen KS. 2012. When naked became armored: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS One 7:e50004. doi:10.1371/journal .pone.0050004.
51. Hackett JD, Wisecaver JH, Brosnahan ML, Kulis DM, Anderson DM, Bhattacharya D, Plumley FG, Erdner DL. 2013. Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol. Biol. Evol. 30:70-78.
52. Ordás MC, Fraga S, Franco JM, Ordás A, Figueras A. 2004. Toxin and molecular analysis of Gymnodinium catenatum (Dinophyceae) strains from Galicia (NW Spain) and Andalucía (S Spain). J. Plankton Res. 26: 341-349.