Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Applied and Environmental Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
ENVIRONMENTAL AND PUBLIC HEALTH MICROBIOLOGY

Phages Infecting Vibrio vulnificus Are Abundant and Diverse in Oysters (Crassostrea virginica) Collected from the Gulf of Mexico

Angelo DePaola, Miles L. Motes, Amy M. Chan, Curtis A. Suttle
Angelo DePaola
Gulf Coast Seafood Laboratory, U.S. Food and Drug Administration, Dauphin Island, Alabama, 36528, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Miles L. Motes
Gulf Coast Seafood Laboratory, U.S. Food and Drug Administration, Dauphin Island, Alabama, 36528, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Amy M. Chan
Departments of Earth and Ocean Sciences (Oceanography), Botany and Microbiology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Curtis A. Suttle
Departments of Earth and Ocean Sciences (Oceanography), Botany and Microbiology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AEM.64.1.346-351.1998
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Phages infecting Vibrio vulnificus were abundant (>104 phages g of oyster tissue−1) throughout the year in oysters (Crassostrea virginica) collected from estuaries adjacent to the Gulf of Mexico (Apalachicola Bay, Fla.; Mobile Bay, Ala.; and Black Bay, La.). Estimates of abundance ranged from 101 to 105 phages g of oyster tissue−1 and were dependent on the bacterial strain used to assay the sample. V. vulnificus was near or below detection limits (<0.3 cell g−1) from January through March and was most abundant (103 to 104 cells g−1) during the summer and fall, when phage abundances also tended to be greatest. The phages isolated were specific to strains of V. vulnificus, except for one isolate that caused lysis in a few strains of V. parahaemolyticus. Based on morphological evidence obtained by transmission electron microscopy, the isolates belonged to the Podoviridae,Styloviridae, and Myoviridae, three families of double-stranded DNA phages. One newly described morphotype belonging to the Podoviridae appears to be ubiquitous in Gulf Coast oysters. Isolates of this morphotype have an elongated capsid (mean, 258 nm; standard deviation, 4 nm; n = 35), with some isolates having a relatively broad host range among strains of V. vulnificus. Results from this study indicate that a morphologically diverse group of phages which infect V. vulnificus is abundant and widely distributed in oysters from estuaries bordering the northeastern Gulf of Mexico.

Vibrio vulnificus is an estuarine bacterium (10, 22, 24, 28, 29, 34, 37) that is capable of causing primary septicemia following its ingestion and secondary septicemia through skin lesions in individuals with underlying chronic diseases (7, 25). In both cases, the onset of illness is usually rapid and potentially fatal. Most food-borne illness due to V. vulnificus is linked to consumption of raw oysters (19). Typically, Gulf Coast oysters harbor about 103 to 104V. vulnificus cells g−1 during the warmer months of April through October and usually fewer than 10 cells g−1during other months (13, 36). Both physical and biological factors probably regulate the abundance of V. vulnificus in nature. For example, the survival of V. vulnificus in seawater has been shown to be temperature and salinity dependent (21), while within oysters, V. vulnificus is readily phagocytized by oyster hemocytes (16). Phages are another factor that may affect populations of V. vulnificuswithin oysters and estuarine waters. Phages are extremely abundant in marine systems, with concentrations in excess of 107 phages ml−1 routinely measured in coastal waters of the Gulf of Mexico (8, 20, 32). Moreover, phages infectingVibrio spp. can be readily isolated from seawater. Moebus and Nattkemper (27) found that 362 of 366 phage-sensitive bacteria isolated from the Atlantic belonged to the familyVibrionaceae and that 280 of them could be assigned toVibrio spp. Phages which infect Vibrio parahaemolyticus have been isolated from a variety of estuarine samples as well, with greater abundances associated with higher water temperatures and higher concentrations of mesophilic vibrios (5, 6). A variety of Vibrio phages are also prevalent in the Gulf of Mexico (23); recently, phages causing lysis ofV. vulnificus were recovered in approximately 5% of estuarine water samples collected from Louisiana (30).

Given that phages infecting V. vulnificus can be isolated in estuarine waters of the northern Gulf of Mexico, we wished to determine whether they were also present in oysters from this region. In this study, we used a quantitative assay for phages infecting V. vulnificus to determine the seasonal distribution and abundance of these phages in oysters collected from Louisiana, Alabama, and Florida. In addition, we collected representative isolates of these phages and characterized them by transmission electron microscopy and through host range studies.

Source of bacterial host strains.Strains of V. vulnificus were provided by the following individuals: strains A-9 (moderately virulent environmental isolate) and J-7 (a virulent environmental isolate), Jerry Stelma, Environmental Protection Agency, Cincinnati, Ohio (31); strain VBNO (isolated from a Blue Crab, Callinectes sapidus), Ron Sizemore, University of North Carolina—Wilmington; strain 304C (isolated from an oyster,Crassostrea virginica), David Cook, Gulf Coast Seafood Laboratory, U.S. Food and Drug Administration, Dauphin Island, Ala.; strain MO6-24 (human primary septicemia blood isolate), Glenn Morris, Center for Vaccine Development, University of Maryland, Baltimore, Md. Virulence was determined by the method of Stelma et al. (31); isolate A-9 was lethal to mice that were simultaneously iron overloaded and immunosuppressed, and isolate J-7 was lethal to mice that were iron overloaded.

Sample collection and preparation.Oysters were collected weekly from October through December 1994 and March through September 1995 from Apalachicola Bay, Fla., Mobile Bay, Ala., and Black Bay, La., with tongs or a dredge. These areas were sampled monthly in January and February 1995. The oysters were held at 5 to 10°C during shipment for 24 to 30 h prior to analysis. Duplicate oyster samples (12 each) were scrubbed, shucked, mixed with an equal (1:1) weight of Butterfield’s phosphate-buffered saline and blended (4).

V. vulnificus enumeration.The abundance ofV. vulnificus was determined by most-probable-number analysis with enzyme immunoassay identification by the FDA Bacteriological Analytical Manual method (12). Tenfold dilutions of oyster homogenate were inoculated into alkaline peptone water (three tubes per dilution) and incubated at 35°C for 12 to 16 h. Portions from tubes with turbid growth were streaked to modified cellobiose-polymyxin-colistin agar, and plates were incubated at 39°C for 18 to 24 h for colony isolation. Cellobiose-fermenting colonies (yellow), typical of V. vulnificus, were picked with sterile toothpicks and transferred for confirmation as V. vulnificus by an enzyme immunoassay. The V. vulnificus species-specific monoclonal antibody used for the enzyme immunoassay was prepared in-house as previously described (35).

Phage enumeration and isolation.Phages were enumerated directly in the supernatant of oyster homogenates as previously described (11). All media and diluents were prepared in seawater (35 ppt collected 50 km offshore from Alabama), which was filtered through 0.2-μm-pore-size cellulose-acetate bottletop filters (Corning Glass Works, Corning, N.Y.) and diluted with deionized seawater to 20 ppt. Casamino Acids peptone marine (CPM) broth (5.0 g of Casamino Acids [Difco], 5.0 g of Bacto Peptone [Difco], and 1.0 liter of seawater, autoclaved for 15 min at 121°C) was used as a growth medium. Serial 10-fold dilutions of oyster supernatant were prepared in sterile seawater. Aliquots (0.1 ml) of each dilution were adsorbed to 0.2 ml of log-phase host cultures for 15 min, and virulent phages were enumerated by using the soft-agar overlay technique (2). The plating medium and soft-agar overlay were prepared with CPM medium supplemented with 1.5 and 0.7% Bacto Agar (Difco), respectively. The plates were incubated at 26°C, and plaques were counted at 24 and 48 h.

Purification and preparation of phage stock.Plaque assays were performed by using either enrichment or direct enumeration procedures; a Pasteur pipette was used to pull plugs of agar containing plaques from plates containing fewer than 250 PFU. The plugs were suspended in sterile seawater, and dilutions of this suspension were replated to purify the phage. This procedure was repeated. High-titer stocks of phages (108 to 1010 phages ml−1) were prepared from the highest dilution of a phage suspension which gave confluent lysis on a soft-agar overlay plate. The phages were extracted by covering the agar surface with 10 ml of sterile seawater and storing the plate at 3°C for 1 to 2 h. The seawater-phage suspension was centrifuged as described above and filtered through a 0.2-μm-pore-size filter.

Bacterial susceptibility.Five strains of V. vulnificus and 18 other isolates of mesophilic Vibriospp. were grown to log phase and plated on CPM medium by the soft-agar overlay technique. After 1 h, 4 μl from a phage stock was spotted onto the plates, and the plates were incubated overnight at 26°C. Bacterial strains were considered susceptible to phages that produced either clear or turbid plaques.

Phage morphology.The morphology of the phage isolates was determined by transmission electron microscopy (33). Phage lysates were filtered through 0.2-μm-pore-size filters and, if necessary, concentrated by ultracentrifugation (146,000 ×g) at 20°C in an AH-629 swinging-bucket rotor (Sorvall) for 2.5 h. The phages were transferred to 400-mesh carbon-coated copper grids by floating the grids on drops of filtered lysate for ca. 30 min. The grids were stained with 1% uranyl acetate and photographed at 80 kV with a Philips EM 301 transmission electron microscope. The sizes of the six different phage morphotypes were estimated from photographic images of negatively stained phage particles. A diffraction grating replica calibration standard (2,160 lines/mm) with latex beads (0.216 mm in diameter) was used to calibrate the magnification of the electron microscope.

Changes in the abundances of phages and V. vulnificus.Phages infecting a clinical strain (strain MO6-24) and a virulent environmental isolate (strain J-7) of V. vulnificus were abundant throughout the year in oysters from Apalachicola Bay, Fla., Mobile Bay, Ala., and Black Bay, La., three distinct estuaries along the northern coast of the Gulf of Mexico (Fig.1C and F). Abundances ranged from 103 to more than 105 phages g of oyster tissue−1 for strain J-7, with the greatest concentrations occurring in the summer and fall in oysters from Black Bay (Fig. 1C). The abundance of phages infecting strain MO6-24 tended to be less variable and ranged from ca. 104 to 105 phages g−1. Phages infecting strain A-9 (Fig. 1A), a moderately virulent environmental isolate, and strain 304C (Fig. 1E), an oyster isolate of unknown virulence, were not as abundant and ranged in titer from 102 to 104 phages g−1, except for a few occasions when the abundance was <102 phages g−1. The phages infecting strain VBNO of V. vulnificus, which was isolated from a blue crab and is of unknown virulence, were typically the least abundant and varied between being undetectable (<5 phages g−1) to ca. 103phages g−1 (Fig. 1D). Relative to the abundance of infectious phages, V. vulnificus was much more variable, ranging from near or below detection limits (<0.3 cell g−1) from January through March to ca. 103 to 104 cells g−1 during April through October (Fig. 1A). The densities of V. vulnificus and its phages were remarkably similar among the Gulf Coast estuaries (Fig. 1).

Fig. 1.
  • Open in new tab
  • Download powerpoint
Fig. 1.

Seasonal changes in the abundance of V. vulnificus (A) and of phages that infect strains of V. vulnificus (B to F) in oysters from Florida (▵), Alabama (+), and Louisiana (○).

Morphology of phages and host range studies.We examined 43 different phage isolates with the electron microscope and found six distinct phage morphologies belonging to the bacteriophage familiesMyoviridae, Styloviridae, andPodoviridae (Fig. 2). The first morphotype was a stylophage with a collar-like structure between the head and tail and a thin threadlike extension from the end of the noncontractile tail (Bradley group B-1; Fig. 2A). The mean head diameter was 65 nm (standard deviation [SD] = 4 nm; n= 10), and the mean total length of the phage was 219 nm (SD = 14 nm; n = 10). The second morphotype was a myophage with a long contractile tail that ended in a plate-like structure (Bradley group A-1; Fig. 2B). The mean head diameter was 109 nm (SD = 12 nm; n = 11), and the mean total length of the phage was 366 nm (SD = 45 nm; n = 11). The third morphotype was a stylophage with appendages at the end of the thin, flexible tail (Bradley group B-1; Fig. 2C). The mean head diameter was 90 nm (SD = 4 nm; n = 6), and the mean total length of the phage was 262 nm (SD = 9 nm; n = 6). The fourth morphotype was a podophage with short extensions at the neck (Bradley group C-1; Fig. 2D). The mean head diameter was 72 nm (SD = 5 nm;n = 20). The fifth morphotype was a stylophage with elongated head (Bradley group B-2; Fig. 2E). The mean head length was 109 nm (SD = 10 nm; n = 10), and the mean head width was 64 nm (SD = 5 nm; n = 10). The mean total length of this phage was 274 nm (SD = 8 nm;n = 10). The sixth morphotype was a podophage with an extensively elongated head (Bradley group C-3; Fig. 2F). The mean head length was 258 nm (SD = 4 nm; n = 35), and the mean head width was 47 nm (SD = 3 nm; n = 35). The mean total length of this phage was 270 nm (SD = 5 nm;n = 35).

Fig. 2.
  • Open in new tab
  • Download powerpoint
Fig. 2.

Transmission electron micrographs of representativeV. vulnificus phages. (A) Stylophage with collar. A thin threadlike structure extends from the end of the tail; isolated from location for isolate 70A-4. (B) Myophage with contracted tail sheath revealing tail core and plate-like structure at the end of the tail; isolated from location for isolate 1-11. (C) Stylophage; isolated from location for isolate 11-8. (D) Podophage; isolated from location for 1-9. (E) Stylophage with elongated capsid; isolated from location for isolate 353B. (F) Podophage with very elongated capsid; isolated from location for isolate 71A-6. Bars, 50 nm.

Host range studies with the five host strains of V. vulnificus revealed 16 distinct morphotype and host range patterns among the 25 phage strains tested (Table1). Podoviridae strains in Bradley groups C-1 and C-3 caused lysis in all five host strains. The Bradley C-3 morphotype has not previously been reported for phages infecting Vibrio spp., yet it was one of the most common morphotypes observed in this investigation. Nineteen mesophilic bacterial isolates, primarily Vibrio spp., were tested for susceptibility to 25 representative V. vulnificus phage isolates. A single phage isolate lysed several atypical (cellobiose-fermentering) V. parahaemolyticus strains. Other bacterial species including V. cholerae (seven strains),V. alginolyticus (three strains), V. parahaemolyticus (two strains), V. fluvialis (one strain), V. mimicus (one strain), Aeromonas hydrophila (one strain), and Pseudomonas putricida (one strain) were resistant to all 25 of the phage isolates.

View this table:
  • View inline
  • View popup
Table 1.

V. vulnificus phage morphology and host specificity

Phage abundance and distribution.This study demonstrates that a diverse group of phages infecting V. vulnificus was abundant in oysters from estuaries in the northern Gulf of Mexico. Pelon et al. (30) reported a low incidence of phages infecting V. vulnificus in estuarine water samples from Louisiana; quantitative procedures for enumeration were not used. The total concentration of phages infecting V. vulnificus cannot be determined from our data. Many of the phages that we isolated caused lysis in only one of the five stains assayed, indicating that only a subset was detected. This finding suggests that more phages would be found if a larger number of host strains were used to assay the phages. It is also possible that the efficiencies of the plaque assays were lower than 100%. Nonetheless, given the abundance and diversity of phages that we detected in oysters from the Gulf of Mexico, it seems evident that phages probably play an important role in the ecology of cooccurring V. vulnificus.

Phages that cause lysis of V. parahaemolyticus have been isolated from seawater samples (18) and have also been found in molluscan shellfish from Washington and Oregon (5, 6). The abundance of these phages in shellfish increased with increasing water temperatures and with the abundance of mesophilic vibrios but not with increases in the abundance of V. parahaemolyticus. Baross et al. (5) hypothesized that other mesophilic vibrios served as hosts for phages that infected V. parahaemolyticus. We also observed that the abundance of phages infecting some strains of V. vulnificus remained high even when V. vulnificus was present in small or undetectable numbers. We examined 19 mesophilic isolates for susceptibility to 25 phages that caused lysis of V. vulnificus in order to test the hypothesis that other Vibrio spp. might serve as alternate hosts. Of these phages, only a single phage isolate was able to cause lysis of a bacterial strain other than V. vulnificus, namely, several atypical strains (cellobiose fermenters) of V. parahaemolyticus. Although the possibility remains that the production of phages which infect V. vulnificus was supported by other species of bacteria, we were not able to provide convincing evidence of this in our experiments.

Phage morphology and host range.The phages found in our study were morphologically diverse, and several were distinct from those previously isolated from Louisiana waters (30). A number of the phages we isolated belonged to the Podoviridae C Bradley group, although they have not been reported in past surveys ofVibrio phages (1). However, in an extensive study of phages isolated from the North Atlantic which infected 366 strains of bacteria belonging primarily to the Vibrionaceae, Moebus and coworkers (14, 26, 27) isolated a number of phages belonging to the Podoviridae. The group of short-tailed phages that have an exceptionally long capsid (Fig. 2F) appear to belong to a previously undescribed morphotype within thePodoviridae. Unlike most of the phage isolates, which had relatively narrow host ranges and caused lysis only of the strain on which they were originally isolated, some of the phages belonging to the newly described group lysed all five of the host strains as well as all clinical isolates of V. vulnificus tested thus far (data not shown).

That many of the phages have a relatively narrow host range suggests that they may be useful in developing a phage-typing system forV. vulnificus, such as has been used for epidemiological studies of related pathogens including V. cholerae (3, 9, 15). Indeed, susceptibility patterns of V. vulnificus strains to the phage isolates listed in Table 1 clearly distinguished among the five host strains of V. vulnificus. Moreover, encapsulated (associated with virulence) strains of V. vulnificus appear to be more susceptible to infection by phages than unencapsulated (not associated with virulence) strains do (30). Phage typing may also be useful in distinguishing strain virulence, a capability not currently available (17).

ACKNOWLEDGMENTS

We thank Florida State Department of Natural Resources, Alabama State Health Department, and Louisiana State Department of Health and Hospitals for assistance with sample collection and shipment.

FOOTNOTES

    • Received 16 July 1997.
    • Accepted 10 October 1997.
  • Copyright © 1998 American Society for Microbiology

REFERENCES

  1. 1.↵
    1. Ackermann H. W.,
    2. Kasatiya S. S.,
    3. Kawata T.,
    4. Koga T.,
    5. Lee J. V.,
    6. Mbiguino A.,
    7. Newman F. S.,
    8. Vieu J. F.,
    9. Zachary A.
    Classification of Vibrio bacteriophages. Intervirology 22 1984 61 71
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    1. Adams M. H.
    Bacteriophages. 1959 Interscience New York, N.Y
  3. 3.↵
    1. Almeida R. J.,
    2. Cameron D. N.,
    3. Cook W. L.,
    4. Wachsmuth I. K.
    Vibriophage VcA-3 as an epidemic strain marker for the U.S. Gulf Coast Vibrio cholerae O1 clone. J. Clin. Microbiol. 30 1992 300 304
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    American Public Health Association Recommended procedures for the examination of seawater and shellfish 4th ed. 1970 American Public Health Association Washington, D.C
  5. 5.↵
    1. Baross J. A.,
    2. Liston J.,
    3. Morita R. Y.
    Incidence of Vibrio parahaemolyticus bacteriophages and other Vibrio bacteriophages in marine samples. Appl. Environ. Microbiol. 36 1978 492 499
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    1. Baross J. A.,
    2. Liston J.,
    3. Morita R. Y.
    Ecological relationship between Vibrio parahaemolyticus and agar-digesting vibrios as evidenced by bacteriophage susceptibility patterns. Appl. Environ. Microbiol. 36 1978 500 505
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    1. Blake P. A.,
    2. Merson A. M.,
    3. Weaver R. E.,
    4. Hollis D. G.,
    5. Heublein P. C.
    Disease caused by a marine Vibrio: clinical characteristics and epidemiology. N. Engl. J. Med. 300 1979 1 5
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    1. Boehme J.,
    2. Frischer M. E.,
    3. Jiang S. C.,
    4. Kellogg C. A.,
    5. Pichard S.,
    6. Rose J. B.,
    7. Steinway C.,
    8. Paul J. H.
    Phages, bacterioplankton, and phytoplankton in the southeastern Gulf of Mexico: distribution and contribution to oceanic DNA pools. Mar. Ecol. Prog. Ser. 97 1993 1 10
    OpenUrlCrossRefWeb of Science
  9. 9.↵
    1. Chattopadhyay D. J.,
    2. Sarkar B. L.,
    3. Ansari M. Q.,
    4. Chakrabarti B. K.,
    5. Roy M. K.,
    6. Ghosh A. N.,
    7. Pal S. C.
    New phage typing scheme for Vibrio cholerae O1 biotype El Tor strains. J. Clin. Microbiol. 31 1993 1579 1585
    OpenUrlAbstract/FREE Full Text
  10. 10.↵
    1. DePaola A.,
    2. Capers G. M.,
    3. Alexander D.
    Densities of Vibrio vulnificus in the intestines of fish from the U.S. Gulf Coast. Appl. Environ. Microbiol. 60 1994 984 988
    OpenUrl
  11. 11.↵
    1. DePaola A.,
    2. McLeroy S.,
    3. McManus G.
    Distribution of Vibrio vulnificus phage in oyster tissues and other estuarine habitats. Appl. Environ. Microbiol. 63 1997 2464 2467
    OpenUrlAbstract/FREE Full Text
  12. 12.↵
    1. Elliot E. L.,
    2. Kaysner C. A.,
    3. Tamplin M. L.
    V. cholerae,V. vulnificus, and other Vibrio spp. FDA bacteriological analytical manual 7th ed. 1992 111 140 Association of Official Analytical Chemists Arlington, Va
  13. 13.↵
    Food and Drug Administration Hazard analysis of Vibrio vulnificus in oysters. 1996 Food and Drug Administration Dauphin Island, Ala
  14. 14.↵
    1. Frank H.,
    2. Moebus K.
    An electron microscopic study of bacteriophages from marine waters. Helgol. Meeresunters. 41 1987 385 414
    OpenUrlCrossRef
  15. 15.↵
    1. Goldberg S.,
    2. Murphy J. R.
    Molecular epidemiological studies of United States Gulf Coast Vibrio cholerae strains: integration site of mutator vibriophage VcA-3. Infect. Immun. 42 1983 224 230
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    1. Harris-Young L.,
    2. Tamplin M. L.,
    3. Fisher W. S.,
    4. Mason J. W.
    Effects of physicochemical factors and bacterial colony morphotype on association of Vibrio vulnificus with hemocytes of Crassostrea virginica. Appl. Environ. Microbiol. 59 1993 1012 1017
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    1. Hayat U.,
    2. Reddy G. P.,
    3. Bush C. A.,
    4. Johnson J. A.,
    5. Wright A. C.,
    6. Morris J. G. Jr.
    Capsular types of Vibrio vulnificus: an analysis of strains from clinical and environmental sources. J. Infect. Dis. 168 1993 758 762
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Hidaka T.,
    2. Tokushige A.
    Isolation and characterization of Vibrio parahaemolyticus bacteriophages in sea water. Mem. Fac. Fish. Kagoshima Univ. 27 1978 79 90
    OpenUrl
  19. 19.↵
    1. Hlady G.
    Risk assessment and current data Proceedings of the 1994 Vibrio vulnificus Workshop. Watkins W., McCarthy S. 1994 27 37 Food and Drug Administration Washington, D.C
  20. 20.↵
    1. Jiang S. C.,
    2. Paul J. H.
    Seasonal and diel abundance of phages and occurrence of lysogeny/bacteriocinogeny in the marine environment. Mar. Ecol. Prog. Ser. 104 1994 163 172
    OpenUrlCrossRefWeb of Science
  21. 21.↵
    1. Kaspar C. W.,
    2. Tamplin M. L.
    Effects of temperature and salinity on the survival of Vibrio vulnificus in seawater and shellfish. Appl. Environ. Microbiol. 59 1993 2425 2429
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    1. Kaysner C. A.,
    2. Abeyta C. Jr.,
    3. Wekell M. M.,
    4. DePaola A. Jr.,
    5. Stott R. F.,
    6. Leitch J. M.
    Virulent strains of Vibrio vulnificus isolated from estuaries of the United States West Coast. Appl. Environ. Microbiol. 53 1987 1349 1351
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    1. Kellogg C. A.,
    2. Rose J. B.,
    3. Jiang S. C.,
    4. Thurmond JM,
    5. Paul J. H.
    Genetic diversity of related vibriophages isolated from marine environments around Florida and Hawaii, USA. Mar. Ecol. Prog. Ser. 120 1995 89 98
    OpenUrlCrossRefWeb of Science
  24. 24.↵
    1. Kelly M. T.
    Effect of temperature and salinity on Vibrio (Beneckea) vulnificus occurrence in a Gulf Coast environment. Appl. Environ. Microbiol. 44 1982 820 824
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    1. Klontz K. C.,
    2. Lieb S.,
    3. Schreiber M.,
    4. Janowski H. T.,
    5. Baldy L. M.,
    6. Gnn R. A.
    Syndromes of Vibrio vulnificus infections, clinical and epidemiologic features in Florida cases, 1981–1987. Ann. Intern. Med. 109 1988 318 323
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    1. Moebus K.,
    2. Nattkemper H.
    Bacteriophage sensitivity patterns among bacteria isolated from marine waters. Helgol. Meeresunters. 34 1981 375 385
    OpenUrlCrossRef
  27. 27.↵
    1. Moebus K.,
    2. Nattkemper H.
    Taxonomic investigations of bacteriophage sensitive bacteria isolated from marine waters. Helgo. Meeresunters. 36 1983 357 373
    OpenUrl
  28. 28.↵
    1. Oliver J. D.,
    2. Warner R. A.,
    3. Cleland D. R.
    Distribution of Vibrio vulnificus and other lactose-fermenting vibrios in the marine environment. Appl. Environ. Microbiol. 45 1983 985 998
    OpenUrlAbstract/FREE Full Text
  29. 29.↵
    1. O’Neill K. R.,
    2. Jones S. H.,
    3. Grimes D. J.
    Seasonal incidence of Vibrio vulnificus in the Great Bay Estuary of New Hampshire and Maine. Appl. Environ. Microbiol. 58 1992 3257 3262
    OpenUrlAbstract/FREE Full Text
  30. 30.↵
    1. Pelon W.,
    2. Siebeling R. J.,
    3. Simonson J.,
    4. Luftig R. B.
    Isolation of bacteriophage infectious for Vibrio vulnificus. Curr. Microbiol. 30 1995 331 336
    OpenUrlCrossRefPubMed
  31. 31.↵
    1. Stelma G. N. Jr.,
    2. Reyes A. L.,
    3. Peeler J. T.,
    4. Johnson C. H.,
    5. Spaulding P. L.
    Virulence characteristics of clinical and environmental isolates of Vibrio vulnificus. Appl. Environ. Microbiol. 58 1992 2776 2782
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    1. Suttle C. A.,
    2. Chan A. M.,
    3. Cottrell M. T.
    Infection of phytoplankton by phages and reduction of primary productivity. Nature 347 1990 467 469
    OpenUrlCrossRef
  33. 33.↵
    1. Suttle C. A.,
    2. Chan A. M.
    Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar. Ecol. Prog. Ser. 92 1993 99 109
    OpenUrlCrossRefWeb of Science
  34. 34.↵
    1. Tamplin M.,
    2. Rodrick G. E.,
    3. Blake N. J.,
    4. Cuba T.
    Isolation and characterization of Vibrio vulnificus from two Florida estuaries. Appl. Environ. Microbiol. 44 1982 1466 1477
    OpenUrlAbstract/FREE Full Text
  35. 35.↵
    1. Tamplin M. L.,
    2. Martin A. L.,
    3. Ruple A. D.,
    4. Cook D. W.,
    5. Kaspar C. W.
    Enzyme immunoassay for identification of Vibrio vulnificus in seawater, sediment, and oysters. Appl. Environ. Microbiol. 57 1991 1235 1240
    OpenUrlAbstract/FREE Full Text
  36. 36.↵
    1. Tamplin M. L.
    The seasonal occurrence of Vibrio vulnificus in shellfish, seawater, and sediment of United States coastal waters and the influence of environmental factors on survival and virulence. 1994Final report to the Salstonstall-Kennedy Program.
  37. 37.↵
    1. Wright A. C.,
    2. Hill R. T.,
    3. Johnson J. A.,
    4. Roghman M.,
    5. Colwell R. R.,
    6. Morris J. G.
    Distribution of Vibrio vulnificus in the Chesapeake Bay. Appl. Environ. Microbiol. 62 1996 717 724
    OpenUrlAbstract/FREE Full Text
PreviousNext
Back to top
Download PDF
Citation Tools
Phages Infecting Vibrio vulnificus Are Abundant and Diverse in Oysters (Crassostrea virginica) Collected from the Gulf of Mexico
Angelo DePaola, Miles L. Motes, Amy M. Chan, Curtis A. Suttle
Applied and Environmental Microbiology Jan 1998, 64 (1) 346-351; DOI: 10.1128/AEM.64.1.346-351.1998

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Applied and Environmental Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Phages Infecting Vibrio vulnificus Are Abundant and Diverse in Oysters (Crassostrea virginica) Collected from the Gulf of Mexico
(Your Name) has forwarded a page to you from Applied and Environmental Microbiology
(Your Name) thought you would be interested in this article in Applied and Environmental Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Phages Infecting Vibrio vulnificus Are Abundant and Diverse in Oysters (Crassostrea virginica) Collected from the Gulf of Mexico
Angelo DePaola, Miles L. Motes, Amy M. Chan, Curtis A. Suttle
Applied and Environmental Microbiology Jan 1998, 64 (1) 346-351; DOI: 10.1128/AEM.64.1.346-351.1998
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

bacteriophages
Ostreidae
Vibrio

Related Articles

Cited By...

About

  • About AEM
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AppEnvMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

 

Print ISSN: 0099-2240; Online ISSN: 1098-5336