Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates
Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it...
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Published in | PloS one Vol. 6; no. 5; p. e20096 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
18.05.2011
Public Library of Science (PLoS) |
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Abstract | Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it is associated with eukaryotic dinoflagellates. However, several studies suggest that saxitoxin is not produced by dinoflagellates themselves, but by co-cultured bacteria. Here, we show that genes required for saxitoxin synthesis are encoded in the nuclear genomes of dinoflagellates. We sequenced >1.2×10(6) mRNA transcripts from the two saxitoxin-producing dinoflagellate strains Alexandrium fundyense CCMP1719 and A. minutum CCMP113 using high-throughput sequencing technology. In addition, we used in silico transcriptome analyses, RACE, qPCR and conventional PCR coupled with Sanger sequencing. These approaches successfully identified genes required for saxitoxin-synthesis in the two transcriptomes. We focused on sxtA, the unique starting gene of saxitoxin synthesis, and show that the dinoflagellate transcripts of sxtA have the same domain structure as the cyanobacterial sxtA genes. But, in contrast to the bacterial homologs, the dinoflagellate transcripts are monocistronic, have a higher GC content, occur in multiple copies, contain typical dinoflagellate spliced-leader sequences and eukaryotic polyA-tails. Further, we investigated 28 saxitoxin-producing and non-producing dinoflagellate strains from six different genera for the presence of genomic sxtA homologs. Our results show very good agreement between the presence of sxtA and saxitoxin-synthesis, except in three strains of A. tamarense, for which we amplified sxtA, but did not detect the toxin. Our work opens for possibilities to develop molecular tools to detect saxitoxin-producing dinoflagellates in the environment. |
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AbstractList | Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it is associated with eukaryotic dinoflagellates. However, several studies suggest that saxitoxin is not produced by dinoflagellates themselves, but by co-cultured bacteria. Here, we show that genes required for saxitoxin synthesis are encoded in the nuclear genomes of dinoflagellates. We sequenced >1.2×10(6) mRNA transcripts from the two saxitoxin-producing dinoflagellate strains Alexandrium fundyense CCMP1719 and A. minutum CCMP113 using high-throughput sequencing technology. In addition, we used in silico transcriptome analyses, RACE, qPCR and conventional PCR coupled with Sanger sequencing. These approaches successfully identified genes required for saxitoxin-synthesis in the two transcriptomes. We focused on sxtA, the unique starting gene of saxitoxin synthesis, and show that the dinoflagellate transcripts of sxtA have the same domain structure as the cyanobacterial sxtA genes. But, in contrast to the bacterial homologs, the dinoflagellate transcripts are monocistronic, have a higher GC content, occur in multiple copies, contain typical dinoflagellate spliced-leader sequences and eukaryotic polyA-tails. Further, we investigated 28 saxitoxin-producing and non-producing dinoflagellate strains from six different genera for the presence of genomic sxtA homologs. Our results show very good agreement between the presence of sxtA and saxitoxin-synthesis, except in three strains of A. tamarense, for which we amplified sxtA, but did not detect the toxin. Our work opens for possibilities to develop molecular tools to detect saxitoxin-producing dinoflagellates in the environment. Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it is associated with eukaryotic dinoflagellates. However, several studies suggest that saxitoxin is not produced by dinoflagellates themselves, but by co-cultured bacteria. Here, we show that genes required for saxitoxin synthesis are encoded in the nuclear genomes of dinoflagellates. We sequenced >1.2x10.sup.6 mRNA transcripts from the two saxitoxin-producing dinoflagellate strains Alexandrium fundyense CCMP1719 and A. minutum CCMP113 using high-throughput sequencing technology. In addition, we used in silico transcriptome analyses, RACE, qPCR and conventional PCR coupled with Sanger sequencing. These approaches successfully identified genes required for saxitoxin-synthesis in the two transcriptomes. We focused on sxtA, the unique starting gene of saxitoxin synthesis, and show that the dinoflagellate transcripts of sxtA have the same domain structure as the cyanobacterial sxtA genes. But, in contrast to the bacterial homologs, the dinoflagellate transcripts are monocistronic, have a higher GC content, occur in multiple copies, contain typical dinoflagellate spliced-leader sequences and eukaryotic polyA-tails. Further, we investigated 28 saxitoxin-producing and non-producing dinoflagellate strains from six different genera for the presence of genomic sxtA homologs. Our results show very good agreement between the presence of sxtA and saxitoxin-synthesis, except in three strains of A. tamarense, for which we amplified sxtA, but did not detect the toxin. Our work opens for possibilities to develop molecular tools to detect saxitoxin-producing dinoflagellates in the environment. Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it is associated with eukaryotic dinoflagellates. However, several studies suggest that saxitoxin is not produced by dinoflagellates themselves, but by co-cultured bacteria. Here, we show that genes required for saxitoxin synthesis are encoded in the nuclear genomes of dinoflagellates. We sequenced >1.2×106 mRNA transcripts from the two saxitoxin-producing dinoflagellate strains Alexandrium fundyense CCMP1719 and A. minutum CCMP113 using high-throughput sequencing technology. In addition, we used in silico transcriptome analyses, RACE, qPCR and conventional PCR coupled with Sanger sequencing. These approaches successfully identified genes required for saxitoxin-synthesis in the two transcriptomes. We focused on sxtA, the unique starting gene of saxitoxin synthesis, and show that the dinoflagellate transcripts of sxtA have the same domain structure as the cyanobacterial sxtA genes. But, in contrast to the bacterial homologs, the dinoflagellate transcripts are monocistronic, have a higher GC content, occur in multiple copies, contain typical dinoflagellate spliced-leader sequences and eukaryotic polyA-tails. Further, we investigated 28 saxitoxin-producing and non-producing dinoflagellate strains from six different genera for the presence of genomic sxtA homologs. Our results show very good agreement between the presence of sxtA and saxitoxin-synthesis, except in three strains of A. tamarense, for which we amplified sxtA, but did not detect the toxin. Our work opens for possibilities to develop molecular tools to detect saxitoxin-producing dinoflagellates in the environment. Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe human illness that may lead to paralysis and death. In freshwaters, the toxin is produced by prokaryotic cyanobacteria; in marine waters, it is associated with eukaryotic dinoflagellates. However, several studies suggest that saxitoxin is not produced by dinoflagellates themselves, but by co-cultured bacteria. Here, we show that genes required for saxitoxin synthesis are encoded in the nuclear genomes of dinoflagellates. We sequenced >1.2×10 6 mRNA transcripts from the two saxitoxin-producing dinoflagellate strains Alexandrium fundyense CCMP1719 and A. minutum CCMP113 using high-throughput sequencing technology. In addition, we used in silico transcriptome analyses, RACE, qPCR and conventional PCR coupled with Sanger sequencing. These approaches successfully identified genes required for saxitoxin-synthesis in the two transcriptomes. We focused on sxtA , the unique starting gene of saxitoxin synthesis, and show that the dinoflagellate transcripts of sxtA have the same domain structure as the cyanobacterial sxtA genes. But, in contrast to the bacterial homologs, the dinoflagellate transcripts are monocistronic, have a higher GC content, occur in multiple copies, contain typical dinoflagellate spliced-leader sequences and eukaryotic polyA-tails. Further, we investigated 28 saxitoxin-producing and non-producing dinoflagellate strains from six different genera for the presence of genomic sxtA homologs. Our results show very good agreement between the presence of sxtA and saxitoxin-synthesis, except in three strains of A. tamarense , for which we amplified sxtA , but did not detect the toxin. Our work opens for possibilities to develop molecular tools to detect saxitoxin-producing dinoflagellates in the environment. |
Audience | Academic |
Author | Jakobsen, Kjetill S Neilan, Brett A Kellmann, Ralf Orr, Russell J S Murray, Shauna A Stüken, Anke |
AuthorAffiliation | 1 Microbial Evolution Research Group (MERG), Department of Biology, University of Oslo, Oslo, Norway East Carolina University, United States of America 3 School of Biotechnology and Biomolecular Sciences and Australian Centre for Astrobiology, University of New South Wales, Sydney, Australia 5 Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway 2 Department of Molecular Biology, University of Bergen, Bergen, Norway 4 Sydney Institute of Marine Sciences, Mosman, New South Wales, Australia |
AuthorAffiliation_xml | – name: 5 Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway – name: 3 School of Biotechnology and Biomolecular Sciences and Australian Centre for Astrobiology, University of New South Wales, Sydney, Australia – name: 2 Department of Molecular Biology, University of Bergen, Bergen, Norway – name: 1 Microbial Evolution Research Group (MERG), Department of Biology, University of Oslo, Oslo, Norway – name: 4 Sydney Institute of Marine Sciences, Mosman, New South Wales, Australia – name: East Carolina University, United States of America |
Author_xml | – sequence: 1 givenname: Anke surname: Stüken fullname: Stüken, Anke organization: Microbial Evolution Research Group, Department of Biology, University of Oslo, Oslo, Norway – sequence: 2 givenname: Russell J S surname: Orr fullname: Orr, Russell J S – sequence: 3 givenname: Ralf surname: Kellmann fullname: Kellmann, Ralf – sequence: 4 givenname: Shauna A surname: Murray fullname: Murray, Shauna A – sequence: 5 givenname: Brett A surname: Neilan fullname: Neilan, Brett A – sequence: 6 givenname: Kjetill S surname: Jakobsen fullname: Jakobsen, Kjetill S |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21625593$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2011 Public Library of Science Copyright Public Library of Science May 2011 Stüken et al. 2011 |
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DocumentTitleAlternate | Saxitoxin Encoded by Dinoflagellate Genomes |
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Editor | Zhang, Baohong |
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Notes | Conceived and designed the experiments: AS RJSO SAM KSJ. Performed the experiments: AS RSJO SAM. Analyzed the data: AS RDJO SAM RK. Contributed reagents/materials/analysis tools: KSJ SAM BAN. Wrote the paper: AS SAM. Commented and approved the manuscript: RSJO RK BAN KSJ. Current address: Hormone Laboratory, Haukeland University Hospital, Bergen, Norway |
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References | GM Hallegraeff (ref1) 1995 I Yang (ref19) 2010; 11 TK Mihali (ref10) 2011; 6 A Moustafa (ref8) 2009; 4 HB Shen (ref43) 2007; 363 AYT Ho (ref55) 2006; 42 N Patron (ref51) 2005; 348 T Yoshida (ref14) 2002; 68 QH Le (ref27) 1997; 225 A Stamatakis (ref48) 2006; 22 J Piel (ref21) 2004; 21 G Taroncher-Oldenburg (ref15) 1999; 7 H Zhang (ref29) 2006; 53 PJ Keeling (ref65) 2008; 9 S Kumar (ref39) TR Bachvaroff (ref28) 2008; 3 B Chevreux (ref40) 2004; 14 RJS Orr (ref37) Y Shimizu (ref5) 1996; 50 Y Hou (ref53) 2009; 4 LD Stein (ref54) 2004; 431 K Katoh (ref46) 2008; 9 R Kellmann (ref20) 2010; 8 J Kyte (ref44) 1982; 157 A Negri (ref64) 2003; 39 A Stüken (ref60) 2010; 156 JD Hackett (ref56) 2005; 6 R Kellmann (ref6) 2008; 74 TK Mihali (ref7) 2009; 10 H Zhang (ref63) 2010; 162 P Uribe (ref58) 2008; 10 N Lartillot (ref50) 2006; 55 SA Murray (ref12) 2011; 28 DL Erdner (ref57) 2006; 7 TR Baker (ref25) 2003; 41 MA Doblin (ref35) 1999; 236 YY Hsiao (ref59) 2010 H Zhang (ref31) 2007; 104 KEM Hastings (ref33) 2005; 21 S Lin (ref52) 2006; 42 P Hoagland (ref2) 2006 F Abascal (ref47) 2005; 21 FG Plumley (ref17) 2001; 37 Y Sako (ref13) 2001; 37 R Cavaliere (ref34) 2008 M Wiese (ref11) 2010; 8 JD Bendtsen (ref42) 2004; 340 M Alam (ref3) 1973; 11 S Sato (ref23) 1998 EJ Schantz (ref4) 1966; 5 CA Martins (ref26) 2003; 69 (ref61) 2010 K Stucken (ref9) 2010; 5 GL Hold (ref22) 2001; 36 AZ Worden (ref66) 2010; 13 LD Harlow (ref18) 2007; 46 KB Lidie (ref32) 2007; 54 MJ Prol (ref24) 2009; 55 G Taroncher-Oldenburg (ref16) 2000; 66 CH Slamovits (ref62) 2008; 18 R Kellmann (ref41) 2005 N Lartillot (ref49) 2004; 21 RRL Guillard (ref36) 1993; 32 A Moustafa (ref30) 2010; 5 W Maddison (ref45) 1992 MF Jørgensen (ref38) 2004; 40 |
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Snippet | Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe... Saxitoxin is a potent neurotoxin that occurs in aquatic environments worldwide. Ingestion of vector species can lead to paralytic shellfish poisoning, a severe... |
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StartPage | e20096 |
SubjectTerms | Alexandrium catenella Alexandrium fundyense Alexandrium tamarense Algae Analysis Antibiotics Aphanizomenon Aquatic environment Astrobiology Bacteria Base Sequence Biology Cell Nucleus - metabolism Cyanobacteria Dinoflagellates Dinoflagellida - metabolism DNA Primers DNA sequencing Evolution Fresh water Gene expression Gene Expression Profiling Gene sequencing Genes Genomes Genomics Homology Ingestion Marine toxins Microorganisms Next-generation sequencing Paralysis Paralytic shellfish poisoning Polymerase Chain Reaction Pyrrophycophyta RNA Saxitoxin Saxitoxin - genetics Saxitoxin - metabolism Shellfish Splicing Strains (organisms) Studies Synthesis Taxonomy Toxins Use statistics |
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Title | Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates |
URI | https://www.ncbi.nlm.nih.gov/pubmed/21625593 https://www.proquest.com/docview/1299019312 https://pubmed.ncbi.nlm.nih.gov/PMC3097229 https://doaj.org/article/e9f4872649c9453d92ef2ef26a4228f9 http://dx.doi.org/10.1371/journal.pone.0020096 |
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