Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach

Orr, Russell J. S.; Stüken, Anke; Rundberget, Thomas; Eikrem, Wenche; Jakobsen, Kjetill S.

doi:10.1016/j.hal.2011.05.003

Cited by 57 publications

(64 citation statements)

References 99 publications

(167 reference statements)

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“…It has been reported that a strain of A. affine can produce low levels of STX (Nguyen Ngoc, 2004), while other studies have found that strains do not produce STXs (Hallegraeff et al, 1991;Band-Schmidt et al, 2003;Stüken et al, 2011;Wang et al, 2006). A strain of Alexandrium andersoni (CCMP2222) was reported to produce low levels of STXs (Ciminiello et al, 2000;Frangopulos et al, 2004), while other studies based on CCMP2222 and other strains of A. andersoni have not detected STXs (Sampedro et al, 2013;Stüken et al, 2011;Orr et al, 2011;Touzet et al, 2008). It is possible that sxtA related genes are no longer expressed in CCMP2222, or that early reports of STX production were in error.…”

Section: Presence Of Sxta Domains A1 and A4 And Sxtgmentioning

confidence: 97%

“…In order to determine the evolution of sxt within dinoflagellates, a resolved phylogeny of the group, including the genus Alexandrium and closely related Pyrodinium bahamense is necessary. Alexandrium has often appeared to form a monophyletic clade in phylogenetic analyses based on regions of the ribosomal DNA array, with a selected outgroup (John et al, 2003;Leaw et al, 2005;Orr et al, 2011;Anderson et al, 2012). Questions remain about the evolution of Alexandrium, as different studies have shown that the most basal clade is either: A. taylori (John et al, 2003;Rogers et al, 2006), A. leei (Leaw et al, 2005), a clade composed of the species A. satoanum, A. monilatum, A. taylori, A. hiranoi, A. pseudogonyaulax , and a clade including most of those species and A. leei (Anderson et al, 2012), or a clade including A. minutum, A. tamutum and A. ostenfeldii .…”

Section: Introductionmentioning

confidence: 99%

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Gene duplication, loss and selection in the evolution of saxitoxin biosynthesis in alveolates

Murray

Diwan

Orr

et al. 2015

Molecular Phylogenetics and Evolution

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a b s t r a c tA group of marine dinoflagellates (Alveolata, Eukaryota), consisting of $10 species of the genus Alexandrium, Gymnodinium catenatum and Pyrodinium bahamense, produce the toxin saxitoxin and its analogues (STX), which can accumulate in shellfish, leading to ecosystem and human health impacts. The genes, sxt, putatively involved in STX biosynthesis, have recently been identified, however, the evolution of these genes within dinoflagellates is not clear. There are two reasons for this: uncertainty over the phylogeny of dinoflagellates; and that the sxt genes of many species of Alexandrium and other dinoflagellate genera are not known. Here, we determined the phylogeny of STX-producing and other dinoflagellates based on a concatenated eight-gene alignment. We determined the presence, diversity and phylogeny of sxtA, domains A1 and A4 and sxtG in 52 strains of Alexandrium, and a further 43 species of dinoflagellates and thirteen other alveolates. We confirmed the presence and high sequence conservation of sxtA, domain A4, in 40 strains (35 Alexandrium, 1 Pyrodinium, 4 Gymnodinium) of 8 species of STX-producing dinoflagellates, and absence from non-producing species. We found three paralogs of sxtA, domain A1, and a widespread distribution of sxtA1 in non-STX producing dinoflagellates, indicating duplication events in the evolution of this gene. One paralog, clade 2, of sxtA1 may be particularly related to STX biosynthesis. Similarly, sxtG appears to be generally restricted to STX-producing species, while three amidinotransferase gene paralogs were found in dinoflagellates. We investigated the role of positive (diversifying) selection following duplication in sxtA1 and sxtG, and found negative selection in clades of sxtG and sxtA1, clade 2, suggesting they were functionally constrained. Significant episodic diversifying selection was found in some strains in clade 3 of sxtA1, a clade that may not be involved in STX biosynthesis, indicating pressure for diversification of function.

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Section: Presence Of Sxta Domains A1 and A4 And Sxtgmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Gene duplication, loss and selection in the evolution of saxitoxin biosynthesis in alveolates

Murray

Diwan

Orr

et al. 2015

Molecular Phylogenetics and Evolution

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“…From a phylogenetic point of view, it appears that STX production is paraphyletic within the genus Alexandrium and that STXproducing (STX ϩ ) and -nonproducing (STX Ϫ ) strains of the same species coexist (5). The presence of sxtA correlates well with the pattern of STX production, although there may be some apparent exceptions (18).…”

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confidence: 98%

Evolutionary Acquisition and Loss of Saxitoxin Biosynthesis in Dinoflagellates: the Second “Core” Gene, sxtG

Orr

Stüken

Murray

et al. 2013

Appl Environ Microbiol

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115

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dSaxitoxin and its derivatives are potent neurotoxins produced by several cyanobacteria and dinoflagellate species. SxtA is the initial enzyme in the biosynthesis of saxitoxin. The dinoflagellate full mRNA and partial genomic sequences have previously been characterized, and it appears that sxtA originated in dinoflagellates through a horizontal gene transfer from a bacterium. So far, little is known about the remaining genes involved in this pathway in dinoflagellates. Here we characterize sxtG, an amidinotransferase enzyme gene that putatively encodes the second step in saxitoxin biosynthesis. In this study, the entire sxtG transcripts from Alexandrium fundyense CCMP1719 and Alexandrium minutum CCMP113 were amplified and sequenced. The transcripts contained typical dinoflagellate spliced leader sequences and eukaryotic poly(A) tails. In addition, partial sxtG transcript fragments were amplified from four additional Alexandrium species and Gymnodinium catenatum. The phylogenetic inference of dinoflagellate sxtG, congruent with sxtA, revealed a bacterial origin. However, it is not known if sxtG was acquired independently of sxtA. Amplification and sequencing of the corresponding genomic sxtG region revealed noncanonical introns. These introns show a high interspecies and low intraspecies variance, suggesting multiple independent acquisitions and losses. Unlike sxtA, sxtG was also amplified from Alexandrium species not known to synthesize saxitoxin. However, amplification was not observed for 22 non-saxitoxin-producing dinoflagellate species other than those of the genus Alexandrium or G. catenatum. This result strengthens our hypothesis that saxitoxin synthesis has been secondarily lost in conjunction with sxtA for some descendant species.

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“…Recent research describing a greater number of globally distributed sequences has confirmed the clustering, renamed the ribotypes numerically as Groups I-V, and initially shown that these ribotypes exclusively include either toxic or non-toxic member species (Emily L. Lilly et al, 2007). These ribotypes differ from each other by 13-18% in their ITS1/5.8S/ITS2 sequences (Orr, Stüken, Rundberget, Eikrem, & Jakobsen, 2011) and offspring from the mating of two of the ribotypes are inviable (Brosnahan et al, 2010). These ribotypes were then characterized as separate species and given the names A. fundyense (Group I), A. mediterraneum (Group II), A. tamarense (Group III), A. pacificum (Group IV), and A. australiense (Group V) (John et al, 2014).…”

Section: A Tamarense Species Complexmentioning

confidence: 99%

Phenotypic diversity within two toxic dinoflagellate genera: environmental and transcriptomic studies of species diversity in Alexandrium and Gambierdiscus

Pitz¹

2016

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Dinoflagellates are a diverse group of single-celled eukaryotic phytoplankton that are important for their unique genetics and molecular biology, the multitude of ecological roles they play, and the ability of multiple species to produce toxins that affect human and ecosystems health. Two dinoflagellate genera, Alexandrium and Gambierdiscus each contain species that can cause human poisoning syndromes, although the methods of toxin transfer, accumulation, and exposure are very different. Gambierdiscus is a benthic organism that produces lipophilic ciguatoxins that can bioaccumulate in coral reef fish and cause ciguatera fish poisoning (CFP) in human consumers. Alexandrium is a planktonic species that produces saxitoxins that can directly accumulate in shellfish and cause paralytic shellfish poisoning (PSP) in humans. Both genera contain multiple species that vary dramatically in toxicity and physiology. Through transcriptomic analysis, this thesis describes the genetic diversity present across dinoflagellates that produce saxitoxin, elaborating on differences in their complement of genes within the saxitoxin biosynthesis pathway. This study demonstrated retention and expression of some of these saxitoxin genes by non-toxic species within Alexandrium, as well as in Gambierdiscus, which does not produce saxitoxins. Furthermore it confirmed the presence of certain transcripts only in toxin-producing species. This thesis then developed novel fluorescence in situ hybridization (FISH) probes that can be used to identify and enumerate six Gambierdiscus species, thereby enabling the community composition of Gambierdiscus to be examined in a quantifiable manner. The probes were tested in the laboratory on cultures, and then successfully applied to field samples from Florida Keys and Hawai'i. Gambierdiscus species are diverse in both their toxicity and optimal temperature ranges for growth. Analysis of Gambierdiscus community composition in an area of variable temperature allowed the characterization of species shifts that were driven both by a seasonal increase in mean seawater temperatures and spatial variability of temperature experienced between tidal pools. Overall this thesis advances the knowledge of dinoflagellate genetics and ecology, aids in the characterization of species harmful to public health, and provides tools and approaches to help monitor and manage harmful effects from these species, including some that are projected to increase with climate change.

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Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach

Cited by 57 publications

References 99 publications

Gene duplication, loss and selection in the evolution of saxitoxin biosynthesis in alveolates

Gene duplication, loss and selection in the evolution of saxitoxin biosynthesis in alveolates

Evolutionary Acquisition and Loss of Saxitoxin Biosynthesis in Dinoflagellates: the Second “Core” Gene, sxtG

Phenotypic diversity within two toxic dinoflagellate genera: environmental and transcriptomic studies of species diversity in Alexandrium and Gambierdiscus

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