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      Acute Hepatopancreatic Necrosis Disease-Causing Vibrio parahaemolyticus Strains Maintain an Antibacterial Type VI Secretion System with Versatile Effector Repertoires

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          ABSTRACT

          Acute hepatopancreatic necrosis disease (AHPND) is a newly emerging shrimp disease that has severely damaged the global shrimp industry. AHPND is caused by toxic strains of Vibrio parahaemolyticus that have acquired a “selfish plasmid” encoding the deadly binary toxins PirA vp/PirB vp. To better understand the repertoire of virulence factors in AHPND-causing V. parahaemolyticus, we conducted a comparative analysis using the genome sequences of the clinical strain RIMD2210633 and of environmental non-AHPND and toxic AHPND isolates of V. parahaemolyticus. Interestingly, we found that all of the AHPND strains, but none of the non-AHPND strains, harbor the antibacterial type VI secretion system 1 (T6SS1), which we previously identified and characterized in the clinical isolate RIMD2210633. This finding suggests that the acquisition of this T6SS might confer to AHPND-causing V. parahaemolyticus a fitness advantage over competing bacteria and facilitate shrimp infection. Additionally, we found highly dynamic effector loci in the T6SS1 of AHPND-causing strains, leading to diverse effector repertoires. Our discovery provides novel insights into AHPND-causing pathogens and reveals a potential target for disease control.

          IMPORTANCE Acute hepatopancreatic necrosis disease (AHPND) is a serious disease that has caused severe damage and significant financial losses to the global shrimp industry. To better understand and prevent this shrimp disease, it is essential to thoroughly characterize its causative agent, Vibrio parahaemolyticus. Although the plasmid-encoded binary toxins PirA vp/PirB vp have been shown to be the primary cause of AHPND, it remains unknown whether other virulent factors are commonly present in V. parahaemolyticus and might play important roles during shrimp infection. Here, we analyzed the genome sequences of clinical, non-AHPND, and AHPND strains to characterize their repertoires of key virulence determinants. Our studies reveal that an antibacterial type VI secretion system is associated with the AHPND strains and differentiates them from non-AHPND strains, similar to what was seen with the PirA/PirB toxins. We propose that T6SS1 provides a selective advantage during shrimp infections.

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          Author and article information

          Contributors
          Role: Editor
          Journal
          Appl Environ Microbiol
          Appl. Environ. Microbiol
          aem
          aem
          AEM
          Applied and Environmental Microbiology
          American Society for Microbiology (1752 N St., N.W., Washington, DC )
          0099-2240
          1098-5336
          21 April 2017
          16 June 2017
          1 July 2017
          : 83
          : 13
          : e00737-17
          Affiliations
          [a ]Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas, USA
          [b ]Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, Texas, USA
          [c ]Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas, Texas, USA
          [d ]Department of Biophysics, University of Texas Southwestern Medical Center, Dallas, Texas, USA
          [e ]Department of Molecular Biology & Microbiology, Tufts University School of Medicine, Boston, Massachusetts, USA
          [f ]Howard Hughes Medical Institute, Tufts University School of Medicine, Boston, Massachusetts, USA
          [g ]Department of Biology, Indiana University, Bloomington, Indiana, USA
          [h ]School of Animal & Comparative Biomedical Sciences, University of Arizona, Tucson, Arizona, USA
          [i ]Department of Clinical Microbiology and Immunology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
          University of Georgia
          Author notes
          Address correspondence to Dor Salomon, dorsalomon@ 123456mail.tau.ac.il , or Kim Orth, kim.orth@ 123456utsouthwestern.edu .

          Citation Li P, Kinch LN, Ray A, Dalia AB, Cong Q, Nunan LM, Camilli A, Grishin NV, Salomon D, Orth K. 2017. Acute hepatopancreatic necrosis disease-causing Vibrio parahaemolyticus strains maintain an antibacterial type VI secretion system with versatile effector repertoires. Appl Environ Microbiol 83:e00737-17. https://doi.org/10.1128/AEM.00737-17.

          Author information
          http://orcid.org/0000-0002-8909-0414
          http://orcid.org/0000-0002-2009-9453
          http://orcid.org/0000-0002-0678-7620
          Article
          PMC5478980 PMC5478980 5478980 00737-17
          10.1128/AEM.00737-17
          5478980
          28432099
          d3c9d7c0-2485-4b8d-86d3-68fe4ec3870b
          Copyright © 2017 American Society for Microbiology.

          All Rights Reserved.

          History
          : 30 March 2017
          : 18 April 2017
          Page count
          supplementary-material: 1, Figures: 5, Tables: 1, Equations: 0, References: 65, Pages: 17, Words: 10690
          Funding
          Funded by: HHS | National Institutes of Health (NIH) https://doi.org/10.13039/100000002
          Award ID: GM094575
          Award Recipient : Nick Grishin
          Funded by: HHS | National Institutes of Health (NIH) https://doi.org/10.13039/100000002
          Award ID: AI056404
          Award Recipient : Kim Orth
          Funded by: HHS | National Institutes of Health (NIH) https://doi.org/10.13039/100000002
          Award ID: AI055058
          Award Recipient : Andrew Camilli
          Funded by: Welch Foundation https://doi.org/10.13039/100000928
          Award ID: I-1505
          Award Recipient : Nick Grishin
          Funded by: Welch Foundation https://doi.org/10.13039/100000928
          Award ID: I-1561
          Award Recipient : Kim Orth
          Funded by: Once Upon A Time Foundation https://doi.org/10.13039/100008909
          Award Recipient : Kim Orth
          Categories
          Environmental Microbiology
          Custom metadata
          July 2017

          type VI secretion system,AHPND,T3SS,T6SS, Vibrio , Vibrio parahaemolyticus ,shrimp,type III secretion system,MIX effectors

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