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Characterisation of Opportunistic Bacterial Pathogens of the Marine Macroalga Delisea Pulchra Vipra Kumar Doctor of Philosophy

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Characterisation of Opportunistic Bacterial Pathogens of the Marine Macroalga Delisea Pulchra Vipra Kumar Doctor of Philosophy Characterisation of opportunistic bacterial pathogens of the marine macroalga Delisea pulchra Vipra Kumar A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biotechnology and Biomolecular Sciences Faculty of Science The University of New South Wales Sydney, Australia August 2015 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Kumar First name: Vipra Other name/s: Nandani Abbreviation for degree as given in the University calendar: PhD School: Biotechnology and Biomolecular Sciences Faculty: Science Title: Characterisation of opportunistic bacterial pathogens of the marine macroalga Delisea pulchra Abstract Macroalgae, the major habitat-formers of temperate marine ecosystems are susceptible to disease, yet in many cases the aetiological agent/s remain unknown. The red macroalga Delisea pulchra suffers from a bleaching disease, which can be induced by the bacteria Nautella italica R11 and Phaeobacter sp. LSS9 under laboratory conditions. However recent analyses suggest that these strains are not representative of the dominant pathogens in the environment. Therefore, the aim of this thesis was to determine if multiple pathogens of D. pulchra exist and to further understand the microbial dynamics of bleaching in D. pulchra. To achieve this aim, a culture collection of bacterial strains present on bleached and adjacent-to-bleached tissues of D. pulchra was generated. Bacterial strains that were also overrepresented in previous culture independent studies were subsequently assessed for virulence-related traits, including motility, biofilm-formation, resistance to chemical defences of D. pulchra and the degradation of algal polysaccharides. Ten bacterial isolates with the broadest range of virulence traits were thereafter tested for the ability to induce in vivo bleaching of D. pulchra following the development of a new infection assay. Two Alteromonas sp. (LSS17 and BL110), two Aquimarina sp. (AD1 and BL5) and one Agarivorans sp. (BL7) were identified as new pathogens of D. pulchra. Deep-sequencing of 16S rRNA gene amplicons from the microbial community of D. pulchra demonstrated an increased abundance of Aquimarina sp. AD1 and Alteromonas sp. BL110 strains in diseased hosts post infection with these pathogens providing evidence for Koch’s postulates. Moreover reduced diversity and increased dispersion of microbial communities was observed for diseased algae compared to healthy individuals. Finally, insights into the molecular mechanisms of disease was obtained through a comparative genomic analysis of the newly identified pathogens. Mechanisms for virulence unique to representatives of Alteromonadaceae included chemotaxis, motility and secretion systems whereas por-secretion systems, gliding motility and specific surface appendages were found to be unique to Aquimarina sp. In conclusion, this work provides evidence that multiple opportunistic pathogens of a single host organism are more common in marine systems than previously anticipated and further highlights the complex nature of host-pathogen-microbiome interactions. 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 after 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). 31 August 2015 ……………………………………………… ……………………………………..… ……….……………………...…….… 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 require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: Originality Statement ‘I 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 I 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 in style, presentation and linguistic expression is acknowledged.’ Signed: Date: 31 August 2015 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 been granted I have applied/will apply for a partial restriction of the digital copy of my thesis or dissertation.' Signed: Date: 31 August 2015 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 conversion to digital format.’ Signed: Date: 31 August 2015 i Abstract Macroalgae, the major habitat-formers of temperate marine ecosystems are susceptible to disease, yet in many cases the aetiological agent/s remain unknown. The red macroalga Delisea pulchra suffers from a bleaching disease, which can be induced by the bacteria Nautella italica R11 and Phaeobacter sp. LSS9 under laboratory conditions. However recent analyses suggest that these strains are not representative of the dominant pathogens in the environment. Therefore, the aim of this thesis was to determine if multiple pathogens of D. pulchra exist and to further understand the microbial dynamics of bleaching in D. pulchra. To achieve this aim, a culture collection of bacterial strains present on bleached and adjacent-to-bleached tissues of D. pulchra was generated. Bacterial strains that were also overrepresented in previous culture independent studies were subsequently assessed for virulence-related traits, including motility, biofilm-formation, resistance to chemical defences of D. pulchra and the degradation of algal polysaccharides. Ten bacterial isolates with the broadest range of virulence traits were thereafter tested for the ability to induce in vivo bleaching of D. pulchra following the development of a new infection assay. Two Alteromonas sp. (LSS17 and BL110), two Aquimarina sp. (AD1 and BL5) and one Agarivorans sp. (BL7) were identified as new pathogens of D. pulchra. Deep-sequencing of 16S rRNA gene amplicons from the microbial community of D. pulchra demonstrated an increased abundance of Aquimarina sp. AD1 and Alteromonas sp. BL110 strains in diseased hosts post infection with these pathogens providing evidence for Koch’s postulates. Moreover reduced diversity and increased dispersion of microbial communities was observed for diseased algae compared to healthy individuals. Finally, insights into the molecular mechanisms of disease was obtained through a comparative genomic analysis of the newly identified pathogens. Mechanisms for virulence unique to representatives of Alteromonadaceae included chemotaxis, motility and secretion systems whereas por-secretion systems, gliding motility and specific surface appendages were found to be unique to Aquimarina sp. In conclusion, this work provides evidence that multiple opportunistic pathogens of a single host organism are more common in marine systems than previously anticipated and further highlights the complex nature of host-pathogen-microbiome interactions. ii List of Publications Egan S, Fernandes ND, Kumar V, Gardiner M & Thomas T (2014) Bacterial pathogens, virulence mechanism and host defence in marine macroalgae. Environmental Microbiology 6: 925-38. Egan S, Kumar V, Nappi J & Gardiner M (2014) Microbial interactions with seaweeds. In: Algae and Cyanobacteria Symbiosis (Grube M, Muggia L & Seckbach, J. eds). Nova Publishers, New York, USA. Kumar V, Zozaya-Valdes E, Kjelleberg S, Thomas T & Egan S (2015) Multiple opportunistic pathogens in the bleaching disease of the red seaweed Delisea pulchra, submitted. Kumar V, Tebben, J & Egan S (2015) Development of an alternative in vivo infection model in the red algae Delisea pulchra, in prep.
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