Environmental Microbiology
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Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga

Authors

  • Rebecca J. Case,

    1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
    2. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
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    • Present address: Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA, USA.

  • Sharon R. Longford,

    1. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
    2. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia.
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  • Alexandra H. Campbell,

    1. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
    2. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia.
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  • Adrian Low,

    1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
    2. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
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  • Niina Tujula,

    1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
    2. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
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  • Peter D. Steinberg,

    1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
    2. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
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  • Staffan Kjelleberg

    Corresponding author
    1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia.
    2. Centre of Marine Bio-Innovation, University of New South Wales, Sydney, NSW, Australia.
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E-mail s.kjelleberg@unsw.edu.au; Tel. (+61) 2 93852102; Fax (+61) 2 9385 1779.

Summary

Host–pathogen interactions have been widely studied in humans and terrestrial plants, but are much less well explored in marine systems. Here we show that a marine macroalga, Delisea pulchra, utilizes a chemical defence – furanones – to inhibit colonization and infection by a novel bacterial pathogen, Ruegeria sp. R11, and that infection by R11 is temperature dependent. Ruegeria sp. R11 formed biofilms, invaded and bleached furanone-free, but not furanone-producing D. pulchra thalli, at high (24°C) but not low (19°C) temperatures. Bleaching is commonly observed in natural populations of D. pulchra near Sydney, Australia, during the austral summer when ocean temperatures are at their peak and the chemical defences of the alga are reduced. Furanones, produced by D. pulchra as a chemical defence, inhibit quorum sensing (QS) in bacteria, and this may play a role in furanone inhibition of R11 infection of furanone-free thalli as R11 produces QS signals. This interplay between temperature, an algal chemical defence mechanism and bacterial virulence demonstrates the complex impact environmental change can have on an ecosystem.

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Article Information

DOI

10.1111/j.1462-2920.2010.02356.x

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© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd

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Publication History

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  • Received 13 July, 2010; accepted 23 August, 2010.

Supporting Information

Table S1. Identification of acyl homoserine lactones (AHLs) produced by Ruegeria sp. R11 and Ruegeria sp. PR1b.

Video S1. Film of motile intracellular Ruegeria sp. R11 in furanone free (−) Delisea pulchra. The furanone (−) alga was inoculated with R11 (106 cells ml−1) at 24°C and the film taken on day 3 of the infection assay. The epidermis (E), vacuole (V) and bacterial microcolony (M) are labelled on the algal surface. The arrow denotes motile intracellular bacteria inside an epidermal cell. A surface biofilm has formed on the alga with a microcolony to the right of the film. The microcolony has penetrated the alga’s epidermis and R11 cells can be seen within the vacuole at the centre of the film. The intracellular bacteria are motile and their movement is observed in real time. Scale bar = 5 µm.

Video S2. Film of bleached furanone free (−) Delisea pulchra infected with Ruegeria sp. R11. The furanone (−) alga was inoculated with R11 (106 cells/ml) at 24°C and the film taken on day 4 of the infection assay. Healthy pigmented cortical cells (C) and necrotic bleached cortical cells (B) are labelled in the algae. The arrow denotes motile intracellular bacteria inside bleached cortical cells. Bleached thallus with necrotic cells is on the right and pigmented thallus with cells that have maintained integrity is on the left. The necrotic bleached cells are filled with swarming bacteria while the pigmented cells adjacent to the neurotic cells have a few intracellular bacteria within their vacuoles. Uninfected healthy cells are visibly a few cells distance from the line of bleaching. Scale bar = 5 µm.

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EMI_2356_sm_videoS1.avi3245KSupporting info item
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  1. 1Teaghan J. Mayers, Anna R. Bramucci, Kurt M. Yakimovich, Rebecca J. Case, A Bacterial Pathogen Displaying Temperature-Enhanced Virulence of the Microalga Emiliania huxleyi, Frontiers in Microbiology, 2016, 7CrossRef
  2. 2Francesco P. Mancuso, Sofie D'Hondt, Anne Willems, Laura Airoldi, Olivier De Clerck, Diversity and Temporal Dynamics of the Epiphytic Bacterial Communities Associated with the Canopy-Forming Seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin, Frontiers in Microbiology, 2016, 7CrossRef
  3. 3Lidia Rodrigo-Torres, María J. Pujalte, David R. Arahal, Draft genomes of Nautella italica strains CECT 7645T and CECT 7321: Two roseobacters with potential pathogenic and biotechnological traits, Marine Genomics, 2016, 26, 73CrossRef
  4. 4Enrique Zozaya-Valdés, Alexandra J. Roth-Schulze, Torsten Thomas, Effects of Temperature Stress and Aquarium Conditions on the Red Macroalga Delisea pulchra and its Associated Microbial Community, Frontiers in Microbiology, 2016, 7CrossRef
  5. 5Takaaki Kubota, Tohru Kobayashi, Takuro Nunoura, Fumito Maruyama, Shigeru Deguchi, Enantioselective Utilization of D-Amino Acids by Deep-Sea Microorganisms, Frontiers in Microbiology, 2016, 7CrossRef
  6. 6Tim Lachnit, Torsten Thomas, Peter Steinberg, Expanding our Understanding of the Seaweed Holobiont: RNA Viruses of the Red Alga Delisea pulchra, Frontiers in Microbiology, 2016, 6CrossRef
  7. 7Leen Labeeuw, Joleen Khey, Anna R. Bramucci, Harjot Atwal, A. Paulina de la Mata, James Harynuk, Rebecca J. Case, Indole-3-Acetic Acid Is Produced by Emiliania huxleyi Coccolith-Bearing Cells and Triggers a Physiological Response in Bald Cells, Frontiers in Microbiology, 2016, 7CrossRef
  8. 8Vipra Kumar, Enrique Zozaya-Valdes, Staffan Kjelleberg, Torsten Thomas, Suhelen Egan, Multiple opportunistic pathogens can cause a bleaching disease in the red seaweedDelisea pulchra, Environmental Microbiology, 2016Wiley Online Library
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  10. 10Melissa Garren, Kwangmin Son, Jessica Tout, Justin R Seymour, Roman Stocker, Temperature-induced behavioral switches in a bacterial coral pathogen, The ISME Journal, 2016, 10, 6, 1363CrossRef
  11. 11Enrique Zozaya-Valdes, Suhelen Egan, Torsten Thomas, A comprehensive analysis of the microbial communities of healthy and diseased marine macroalgae and the detection of known and potential bacterial pathogens, Frontiers in Microbiology, 2015, 6CrossRef
  12. 12M. Gardiner, T. Thomas, S. Egan, A glutathione peroxidase (GpoA) plays a role in the pathogenicity of Nautella italica strain R11 towards the red alga Delisea pulchra, FEMS Microbiology Ecology, 2015, 91, 4, fiv021CrossRef
  13. 13Leen Labeeuw, Patrick T Martone, Yan Boucher, Rebecca J Case, Ancient origin of the biosynthesis of lignin precursors, Biology Direct, 2015, 10, 1CrossRef
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  19. 19Melissa Gardiner, Neil D. Fernandes, Dennis Nowakowski, Mark Raftery, Staffan Kjelleberg, Ling Zhong, Torsten Thomas, Suhelen Egan, VarR controls colonization and virulence in the marine macroalgal pathogen Nautella italica R11, Frontiers in Microbiology, 2015, 6CrossRef
  20. 20Suhelen Egan, Neil Daniel Fernandes, Vipra Kumar, Melissa Gardiner, Torsten Thomas, Bacterial pathogens, virulence mechanism and host defence in marine macroalgae, Environmental Microbiology, 2014, 16, 4, 925Wiley Online Library

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