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The Pathogen of the Great Barrier Reef Sponge Rhopaloeides odorabile Is a New Strain of Pseudoalteromonas agarivorans Containing Abundant and Diverse Virulence-Related Genes

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Abstract

Sponge diseases have increased dramatically, yet the causative agents of disease outbreaks have eluded identification. We undertook a polyphasic taxonomic analysis of the only confirmed sponge pathogen and identified it as a novel strain of Pseudoalteromonas agarivorans. 16S ribosomal RNA (rRNA) and gyraseB (gyrB) gene sequences along with phenotypic characteristics demonstrated that strain NW4327 was most closely related to P. agarivorans. DNA-DNA hybridization and in silico genome comparisons established NW4327 as a novel strain of P. agarivorans. Genes associated with type IV pili, mannose-sensitive hemagglutinin pili, and curli formation were identified in NW4327. One gene cluster encoding ATP-binding cassette (ABC) transporter, HlyD and TolC, and two clusters related to the general secretion pathway indicated the presence of type I secretion system (T1SS) and type II secretion system (T2SS), respectively. A contiguous gene cluster of at least 19 genes related to type VI secretion system (T6SS) which included all 13 core genes was found. The absence of T1SS and T6SS in nonpathogenic P. agarivorans S816 established NW4327 as the virulent strain. Serine proteases and metalloproteases of the classes S8, S9, M4, M6, M48, and U32 were identified in NW4327, many of which can degrade collagen. Collagenase activity in NW4327 and its absence in the nonpathogenic P. agarivorans KMM 255T reinforced the invasiveness of NW4327. This is the first report unambiguously identifying a sponge pathogen and providing the first insights into the virulence genes present in any pathogenic Pseudoalteromonas genome. The investigation supports a theoretical study predicting high abundance of terrestrial virulence gene homologues in marine bacteria.

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Acknowledgements

Financial support through sanction no. SR/SO/BB-0114/2010 to JM and RG and INSPIRE fellowship no. IF110045 to JDC from the Department of Science and Technology (http://www.dst.gov.in), Ministry of Science and Technology, Government of India is thankfully acknowledged. NSW was funded through an Australian Research Council Future Fellowship (FT120100480).

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Authors and Affiliations

  1. School of Environmental Studies, Jadavpur University, Kolkata, 700 032, India

    Jayanta D. Choudhury, Arnab Pramanik & Joydeep Mukherjee

  2. Australian Institute of Marine Science, PMB 3, Townsville MC, Townsville, Queensland, 4810, Australia

    Nicole S. Webster & Lyndon E. Llewellyn

  3. Department of Life Science and Biotechnology, Jadavpur University, Kolkata, 700 032, India

    Ratan Gachhui

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  1. Jayanta D. Choudhury
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Correspondence to Joydeep Mukherjee.

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Choudhury, J.D., Pramanik, A., Webster, N.S. et al. The Pathogen of the Great Barrier Reef Sponge Rhopaloeides odorabile Is a New Strain of Pseudoalteromonas agarivorans Containing Abundant and Diverse Virulence-Related Genes. Mar Biotechnol 17, 463–478 (2015). https://doi.org/10.1007/s10126-015-9627-y

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