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The Fish Pathogen Biotype 2: Epidemiology, Phylogeny, and Virulence Factors Involved in Warm-Water Vibriosis

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  • Authors: Carmen Amaro1, Eva Sanjuán2, Belén Fouz3, David Pajuelo4, Chung-Te Lee5, Lien-I Hor6, Rodolfo Barrera7
  • Editor: Michael Sadowsky8
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Estructura de Investigación Multidisciplinar en Biotecnología y BioMedicina (ERI BioTecMed), Department of Microbiology and Ecology, University of Valencia, 46100 Valencia, Spain; 2: Estructura de Investigación Multidisciplinar en Biotecnología y BioMedicina (ERI BioTecMed), Department of Microbiology and Ecology, University of Valencia, 46100 Valencia, Spain; 3: Estructura de Investigación Multidisciplinar en Biotecnología y BioMedicina (ERI BioTecMed), Department of Microbiology and Ecology, University of Valencia, 46100 Valencia, Spain; 4: Estructura de Investigación Multidisciplinar en Biotecnología y BioMedicina (ERI BioTecMed), Department of Microbiology and Ecology, University of Valencia, 46100 Valencia, Spain; 5: Institute of Basic Medical Sciences and Department of Microbiology and Immunology, National Cheng Kung University, Tainan 701, Taiwan, Republic of China; 6: Institute of Basic Medical Sciences and Department of Microbiology and Immunology, National Cheng Kung University, Tainan 701, Taiwan, Republic of China; 7: Valenciana de Acuicultura S.A.; 8: University of Minnesota, St. Paul, MN
  • Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
  • Received 14 October 2014 Accepted 03 March 2015 Published 29 May 2015
  • Carmen Amaro, Carmen.amaro@uv.es
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  • Abstract:

    biotype 2 is the etiological agent of warm-water vibriosis, a disease that affects eels and other teleosts, especially in fish farms. Biotype 2 is polyphyletic and probably emerged from aquatic bacteria by acquisition of a transferable virulence plasmid that encodes resistance to innate immunity of eels and other teleosts. Interestingly, biotype 2 comprises a zoonotic clonal complex designated as serovar E that has extended worldwide. One of the most interesting virulence factors produced by serovar E is RtxA1, a multifunctional protein that acts as a lethal factor for fish, an invasion factor for mice, and a survival factor outside the host. Two practically identical copies of are present in all biotype 2 strains regardless of the serovar, one in the virulence plasmid and the other in chromosome II. The plasmid also contains other genes involved in survival and growth in eel blood: , a gene for an outer membrane (OM) lipoprotein involved in resistance to eel serum and , a gene for an OM receptor specific for eel-transferrin and, probably, other related fish transferrins. All the three genes are highly conserved within biotype 2, which suggests that they are under a strong selective pressure. Interestingly, the three genes are related with transferable plasmids, which emphasizes the role of horizontal gene transfer in the evolution of in nutrient-enriched aquatic environments, such as fish farms.

  • Citation: Amaro C, Sanjuán E, Fouz B, Pajuelo D, Lee C, Hor L, Barrera R. 2015. The Fish Pathogen Biotype 2: Epidemiology, Phylogeny, and Virulence Factors Involved in Warm-Water Vibriosis. Microbiol Spectrum 3(3):VE-0005-2014. doi:10.1128/microbiolspec.VE-0005-2014.

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107. Lee CT, Hor LI. 2010. The expression of a novel biotype 2 Vibrio vulnificus virulence factor is regulated by iron and ferric uptake regulator. Vibrios in the Environment 2010, Biloxi, MI.
108. Pajuelo D, Lee CT, Roig FJ, Hor L, Amaro C. 2015. Novel host-specific iron acquisition system in the zoonotic pathogen Vibrio vulnificus. Env Microbiol doi:10.1111/1462-2920.12782. [PubMed][CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.VE-0005-2014
2015-05-29
2017-11-19

Abstract:

biotype 2 is the etiological agent of warm-water vibriosis, a disease that affects eels and other teleosts, especially in fish farms. Biotype 2 is polyphyletic and probably emerged from aquatic bacteria by acquisition of a transferable virulence plasmid that encodes resistance to innate immunity of eels and other teleosts. Interestingly, biotype 2 comprises a zoonotic clonal complex designated as serovar E that has extended worldwide. One of the most interesting virulence factors produced by serovar E is RtxA1, a multifunctional protein that acts as a lethal factor for fish, an invasion factor for mice, and a survival factor outside the host. Two practically identical copies of are present in all biotype 2 strains regardless of the serovar, one in the virulence plasmid and the other in chromosome II. The plasmid also contains other genes involved in survival and growth in eel blood: , a gene for an outer membrane (OM) lipoprotein involved in resistance to eel serum and , a gene for an OM receptor specific for eel-transferrin and, probably, other related fish transferrins. All the three genes are highly conserved within biotype 2, which suggests that they are under a strong selective pressure. Interestingly, the three genes are related with transferable plasmids, which emphasizes the role of horizontal gene transfer in the evolution of in nutrient-enriched aquatic environments, such as fish farms.

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FIGURE 1

Survival in water of biotype 2. Survival experiments were performed with biotype 2-serovar E strain CECT 4604, isolated from diseased eel. I. Epifluorescence micrographs of samples stained by indirect immunofluorescence using a specific rabbit serum against inactivated-whole cells. (A) An elongated cell as a result of the direct viable count method after 4 weeks of incubation in a coastal seawater microcosm. (B) Cells from a microcosm of 0.8 μm filtered water from the brackish water eel farm after 2 weeks of incubation; the arrow indicates a flagellated cell. (C) Cells from a microcosm of 0.2 μm filtered and autoclaved water from the freshwater eel farm after 3 weeks of incubation; the arrow indicates a cell showing peritrichous-like flagellation. (D) Cells from an untreated natural seawater microcosm after 1 day of incubation. Notice that cells autoaggregated. Bars, approximately 2 μm. II. Survival of bacterial cells in microcosms containing water without treatment (○), filtered through 0.8 μm (⋄), filtered through 0.2 μm (Δ), or filtered through 0.2 μm and autoclaved (□) from coastal seawater (3.4% salinity) (A), eel farm freshwater (0.3% salinity) (B), and brackish water (1% salinity) (C) and coastal brackish water (2.2% salinity) (D). The survival was measured as culturable cells per ml. Bars represent the standard error. Figure taken from reference 54 . doi:10.1128/microbiolspec.VE-0005-2014.f1

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 2

Competence experiments. Survival of biotype 2 (in circles) in competition experiments with biotype 1 (A to D) and (E to H) (both of them in triangles) in mixed (A, C, E, and G) and single (B, D, F, and H) microcosms. The survival was measured as number of culturable cells per ml. Bars represent the standard error. (A, B) Strains CECT 4604 of biotype 2-serovar E and CECT 4608 of biotype 1. (C, D) Strains CECT 4603 of biotype 2-serovar E and CECT 4608. (E, F) Strains CECT 4604 and CECT 839 of . (G, H) Strains CECT 4603 and CECT 839 of . Figure taken from reference 54 . doi:10.1128/microbiolspec.VE-0005-2014.f2

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 3

Phylogeny of biotype 2. Maximum likelihood phylogenetic tree of 115 isolates obtained from the alignment of 7 loci concatenated. Biotype 1 isolates are in black, biotype 2-serovar in blue, biotype 2 nonserovar E in red, and biotype 3 in green. #human isolates; §diseased fish isolates. Figure updated from reference 44 taking into consideration the study in reference 63 . doi:10.1128/microbiolspec.VE-0005-2014.f3

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 4

Plasmids of biotype 2. The main features of the biotype 2 plasmids pC4602-1 (A), pC4602-2 (B), putative cointegrate (C), and pR99 (D). Some of the predicted ORFs are indicated with the arrows. The ORFs associated with virulence, conjugative transfer of plasmid, and other known functions are indicated in gray, black, and white, respectively. Regions ID1 and ID2 are labeled in strips. Seq10, seq25, and seq51, found by SSH ( 40 ) are indicated as black bars. The regions corresponding to pC4602-1 and pC4602-2, respectively, in the cointegrate are separated by the dashed lines. Figure adapted from reference 67 . doi:10.1128/microbiolspec.VE-0005-2014.f4

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 5

The two modalities of the eel warm-water vibriosis. The picture shows two naturally infected eels with biotype 2-serovar (A) and (B) suffering from brackish-water and fresh-water vibriosis, respectively. Large ulcers (A, a) and jaw degradation (B) are the main external clinical signs that differentiate both vibrioses. Hemorrhages in the fins (b), protruding and hemorrhagic anus (c) as well as petechiae (d) are external clinical signs common to both vibrioses. doi:10.1128/microbiolspec.VE-0005-2014.f5

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 6

Biofilm on the eel surface. Scanning electron micrographs of the eel body surface of one survivor from experimental cohabitation challenge with biotype 2-serovar E (strain CECT 4604). In pictures A, B, and C, it can be observed that the layer is actually eel skin, distinguishing the epidermis and the dermis below. Among epidermal cells there were microcolonies of bacteria (D to G), adhered to eel epidermis by means of an extracellular mesh-like substance (D and E), which also covered the bacterial cells (E to G). Arrows indicate wrinkled cells of eel epidermis (B and C), a fragment of the photo amplified in picture E (D), or a bacterial flagellum (F). The bars are 100 μm (A), 50 μm (B), 10 μm (C), 5 μm (D), 1 μm (E and F), or 0.5 μm (G). (H) Epifluorescence micrograph of the mucous layer coating the surface of one survivor elver. The sample was stained by immunostaining with an antiwhole-cell serum against serovar E. Bar, 5 μm. Figure adapted from reference 25 . doi:10.1128/microbiolspec.VE-0005-2014.f6

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 7

Histological analysis of the tissues of an eel suffering from warm-water vibriosis. The eel was infected by immersion with a strain of biotype 2-serovar E (CECT 4999). (A) Two bacteria (marked with arrows) in a renal capillary. Notice that one of them is closely associated to endothelial cells. Bar, 1 μm. (B) Macrophage with damaged erythrocytes (marked with arrows) engulfed within its cytoplasm. Bar, 1 μm. (C) Three images of head kidney showing granulocytes (marked with an arrow) in a degranulation process. The bars are 2 μm (a, c) or 5 μm (b). Figure adapted from reference 104 . doi:10.1128/microbiolspec.VE-0005-2014.f7

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 8

Surface envelopes of biotype 2. (A) Electron micrographs of one biotype 2 and serovar E strain (CECT 4999) (i) and its derivatives, deficient (ii), (O-deficient) deficient (iii), translucent variant (capsule deficient) (iv), complemented (v), and complemented (vi), after ruthenium red-staining of ultrathin sections. Bar corresponds to 0.1 μm. (B) Bactericidal activity of eel phagocytes from spleen, blood, and head kidney against the strain CECT 4999 and its derivatives after 1 h, 3 h, and 5 h of incubation. *Significant differences with the wild type with a p<0.001. Figure taken from reference 80 . doi:10.1128/microbiolspec.VE-0005-2014.f8

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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FIGURE 9

Capsule and gill colonization. Bacteria recovered from gills (cfu gr tissue) after immersion challenge with the two variants, opaque (with capsule) and translucent (without capsule), of the biotype 2-serovar E strain CECT 4999 (E. Valiente and C. Amaro, unpublished data). doi:10.1128/microbiolspec.VE-0005-2014.f9

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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Role of mucus and the protease Vvp in the attachment to gills. (A) Electron micrographs of cultured gills incubated with the biotype 2-serovar E strain CECT 4999 without (i) or with (ii) mucus. (B) Chemotaxis towards mucin (M), algae mucus (AM), eel skin mucus (SM), eel gill mucus (GM), eel intestine mucus (IM), and eel serum (ES). *Significant differences with the wild type strain with p<0.05. CECT 4999, the wild type strain; CT201, Δ mutant; CT250, CT201 complemented in with CT218, cured strain; YJ016, a biotype 1 strain isolated from human blood. Figure taken from reference 99 . doi:10.1128/microbiolspec.VE-0005-2014.f10

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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Comparison of multifunctional autoprocessing repeats in toxin (MARTX) produced by biotype 2 (type III) with those produced by biotypes 1 and 3 (types I and II) and phylogenetic relationships. (A) CPD, autocatalytic cysteine protease domain; hydrolase domain; Efa/LifA protein or Lymphostatin domain, also designated as McfDUF ( 102 ); RID, Rho-GTPase inactivation domain; DUF, domain with an unknown function; RTX PA, RTX of domain, also designated as PMT C1/C2 ( 97 ); ACD, actin cross-linking domain. (B) Maximum likelihood tree derived from complete gene sequences Bootstrap support values higher than 80% are indicated in the corresponding nodes. Figure taken from reference 102 (A) and from F.R. Roig and C. Amaro, unpublished results (B). doi:10.1128/microbiolspec.VE-0005-2014.f11

Source: microbiolspec May 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.VE-0005-2014
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