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Investigations Into Abiotic and Biotic Factors Regulating Saxitoxin Synthesis in the Dinoflagellate Genus Alexandrium

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Investigations Into Abiotic and Biotic Factors Regulating Saxitoxin Synthesis in the Dinoflagellate Genus Alexandrium Investigations into abiotic and biotic factors regulating saxitoxin synthesis in the dinoflagellate genus Alexandrium A DISSERTATION SUBMITTED BY Maria Wiese (Dip. Biology University of Bremen, Germany) IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE AWARD OF DOCTOR OF PHILOSOPHY (Ph.D.) AT THE SCHOOL OF BIOTECHNOLOGY AND BIOMOLECULAR SCIENCES THE UNIVERSITY OF NEW SOUTH WALES SYDNEY, AUSTRALIA 2012 Supervisors PROF. BRETT A. NEILAN SUPERVISOR SCHOOL OF BIOLOGY AND BIOMOLECULAR SCIENCES THE UNIVERSITY OF NEW SOUTH WALES SYDNEY, AUSTRALIA DR. SHAUNA A. MURRAY JOINT-SUPERVISOR SCHOOL OF BIOLOGY AND BIOMOLECULAR SCIENCES THE UNIVERSITY OF NEW SOUTH WALES SYDNEY, AUSTRALIA PLEASE TYPE THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Wiese First name: Maria Other name/s: Abbreviation for degree as given in the University calendar: School: BABS Faculty: Science Title: Ms Abstract 350 words maximum: (PLEASE TYPE) Many Alexandrium species produce saxitoxin (STX) and its analogues, which are responsible for paralytic shellfish poisoning (PSP). However, the regulation of toxin production on a gene and enzyme level, and the basis of intra-strain and intra-specific differences in toxin production are not well understood. In this study the role of transcriptional regulation of the class II aminotransferase putatively involved in sax itoxin synthesis, sxtA4 was investigated during growth in batch culture and in different light conditions. No sign ificant differences in sxtA4 gene express ion were detected, w hile significant variances in PST production were measured, suggesting that post-tra nscriptional regulation might prevail in dinoflagellates. The preferential transcription of high GC genomic DNA copies of sxtA4 have been found to play a potential role in the transcriptional regul ation of sxtA4. Furthermore the impact of spectral light quality on PST production was investigated and red light was found to evoke a higher PST per cell content than blue light in Alexandrium catenella. Higher PST levels in red light were accompani ed by higher ch lorophyll production and photoacclimatory processes in the different light conditions. Based on the results it ca n be concl uded that A.catenella is likely to be more toxic in upper water layers where more red light is present. Bacteria are an integral part of the proximate environment of dinoflagellates. The involvement of bacteria in PST production has been reported, but is sti ll elusive. In this study bacterial communities associated with a toxic and non­ toxic Alexandrium strain were characterized in order to further unravel which biotic factors potentially impact harmful algal bloom development and toxicity of Alexandrium species. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here alter known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). / L ( lfi!LI!J/ .~ .......... .. ... ·········~>-----·· ·· ····· ············ ········ ··· ···· ················· .. -~ .~ ..1. (},fl.!..?. ..9.. f? .... Signature~.. Witness Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and re uire the a roval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: COPYRIGHT STATEMENT 'I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights. such as patent rights. I also retain the right to use in future works {such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International {this is applicable to doctoral theses only). I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright·material; where permission has not :i::sisordi!hbeen granted I have applied/will/.IIJj apply for a partial restriction of the digital copy of Date .. .....1.!i· ..t? .~ ~ .2. Qf.?!. ..... .. ···· ·· ···· ················· ··· AUTHENTICITY STATEMENT 'I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the :::~~nto ·~ · f1l·················· ·· ·· · ·· · · · · · · · ·· Date ....... .. ... ..... .... ..... ........... .. ..... .. ............................ .. .. ORIGINALITY STATEMENT '1 hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom 1 have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or :i:::·p;?;;'i.if.e~pre~!on 1s ackn~ledged. ' Date ......... /[.. 9.~.... ;P1..?. ....... ............. ABSTRACT Species of the dinoflagellate genus Alexandrium are prominent producers of saxitoxin and its analogs, known as paralytic shellfish toxins (PSTs), which are the causative agents of paralytic shellfish poisoning (PSP). Under certain environmental conditions, some species of the genus Alexandrium can proliferate and form harmful algal blooms (HABs). In this study, a real time PCR assay was developed and a set of suitable reference genes was tested to investigate the transcriptional regulation of the class II aminotransferase (sxtA4) putatively involved in saxitoxin synthesis, during growth in batch culture of Alexandrium catenella. No significant changes in transcript abundance of sxtA4 were detected at different growth rates. The phylogenetic analysis of sxtA4 and the comparison of cDNA and gDNA copies of sxtA4 revealed that preferential transcription of high GC genomic DNA copies of sxtA4, may play a role in its transcriptional regulation. Light plays a key role in the regulation of cell division, synchronized by the circadian rhythm and is therefore likely to be a major regulator of the signalling pathways leading to the development of toxic blooms. Light penetrates the water column with varying intensities and qualities, which impact the regulation of cell proliferation and nutritional status of microalgae. Light quality was shown to be a major regulator of PST production. Alexandrium catenella Group IV produced significantly higher amounts of the PSTs when grown in red and white light in comparison to blue light. Biotic factors which can influence PST production include the bacterial communities associated with Alexandrium. In this study, bacterial communities associated with toxic and non-toxic Alexandrium tamarense Group V strains were studied via PCR-based 454 pyrosequencing. The strains displayed a similar microbial diversity when analyzed on the family level, in both cases dominanted by the Rhodobacteraceae family, but differed on the genus and species level. The Rhodobacteraceae associated with the toxic strain were closely related to Thalassobacter genus, while the Rhodobacteraceae associated with the non-toxic Alexandrium were closer related to the genus Loktanella. Several orders with lower abundance such as Rhizobiales and Sphingomonadales were also identified in both strains. The novel molecular approaches implicated in this study are excellent tools complementing traditional methods in the investigation of the capacity and regulation of PST production of toxic Alexandrium strains. This work has shown that an integrative approach of molecular and traditional methods, as well as the combined investigation of biotic and abiotic fators are promising to further elucidate the evolution of PST production capacity in dinoflagellates. i Acknowledgement I would like to thank the Australian Research Council, Diagnostic Technology and the University of New South Wales for supporting this project (LP0989830) and I thank Prof. Brett Neilan for assigning the APAI scholarship for this project to me, sharing his enthusiasm for genes and giving me the freedom to pursue my own ideas. I would like to thank Prof. Gustaaf Hallegraeff for the supply of Alexandrium cultures. I thank Dr. Shauna Murray for help with editing and scientific writing of Chapters 1, 3-5,
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