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Multi-site Analysis Reveals Widespread Antibiotic Resistance in the Marine Pathogen Vibrio vulnificus

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Abstract

Vibrio vulnificus is a serious opportunistic human pathogen commonly found in subtropical coastal waters, and is the leading cause of seafood-borne mortality in the USA. This taxon does not sustain prolonged presence in clinical or agricultural settings, where it would undergo human-induced selection for antibiotic resistance. Therefore, few studies have verified the effectiveness of commonly prescribed antibiotics in V. vulnificus treatment. Here we screened 151 coastal isolates and 10 primary septicaemia isolates against 26 antimicrobial agents representing diverse modes of action. The frequency of multiple resistances to antibiotics from all sources was unexpectedly high, particularly during summer months, and a substantial proportion of isolates (17.3%) were resistant to eight or more antimicrobial agents. Numerous isolates demonstrated resistance to antibiotics routinely prescribed for V. vulnificus infections, such as doxycycline, tetracycline, aminoglycosides and cephalosporins. These resistances were detected at similar frequencies in virulent and non-virulent strains (PCR-based virulence typing) and were present in septicaemia isolates, underlying the public health implications of our findings. Among environmental isolates, there were no consistent differences in the frequency of resistance between pristine and anthropogenically impacted estuaries, suggesting natural rather than human-derived sources of resistance traits. This report is the first to demonstrate prevalent antibiotic resistance in a human pathogen with no clinical reservoirs, implying the importance of environmental studies in understanding the spread, evolution and public health relevance of antibiotic resistance factors.

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Acknowledgements

We thank Blaine West, Charles Zemp, Kirk Kessler, Richard Gregory, and Marc Frischer for help accessing field sample collection sites. Brian Thompson and Brian Robinson are acknowledged for their assistance in isolate preparation. This work was supported by the National Oceanographic and Atmospheric Administration (NOAA) awards NA04OAR4600198 to Stepanauskas and NA05NOS4781244 to Oliver. Additional support was provided from the US Department of Energy Financial Assistance Award DE-FC09-96SR18546 to the University of Georgia Research Foundation.

Disclaimer

This report was prepared as an account of work sponsored by an agency of the United States Government. Neither the United States Government nor any agency thereof, nor any of their employees, makes any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed, or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process, or service by trade name, trademark, manufacturer, or otherwise does not necessarily constitute or imply its endorsement, recommendation, or favouring by the United States Government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or any agency thereof.

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Authors and Affiliations

  1. Savannah River Ecology Laboratory, Drawer E, Aiken, SC, USA

    Craig Baker-Austin, J. V. McArthur, Angela H. Lindell & Meredith S. Wright

  2. Savannah River National Laboratory, Bldg. 773-42A, Aiken, SC, USA

    R. Cary Tuckfield

  3. National Oceanographic and Atmospheric Administration, Charleston, SC, USA

    Jan Gooch

  4. Department of Biology, University of North Carolina at Charlotte, Charlotte, NC, USA

    Liza Warner & James Oliver

  5. Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, ME, USA

    Ramunas Stepanauskas

  6. Centre for Environment, Fisheries and Aquaculture Science, Weymouth Laboratory, Weymouth, Dorset, DT4 8UB, UK

    Craig Baker-Austin

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  1. Craig Baker-Austin
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  2. J. V. McArthur
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  8. James Oliver
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  9. Ramunas Stepanauskas
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Correspondence to Craig Baker-Austin.

Electronic Supplementary Materials

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Fig. S1

Box and whisker plots showing the temporal and seasonal distributions of V. vulnificus resistance profiles from the 151 environmental isolates. a Total number of resistances per isolates between sampling month and site. b Average resistance response (\(\tilde C_{ab\operatorname{Re} s} \)) association between sampling month and site. Shipyard Creek (SYC), LCP Chemicals (LCP) and the ACE Basin (ACE) (PDF 21.8 KB)

Table S1

Key physical and chemical conditions from the study sites (XLS 42.0 KB)

Table S2

Antimicrobial resistance data from all screened V. vulnificus isolates (XLS 57.0 KB)

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Baker-Austin, C., McArthur, J.V., Lindell, A.H. et al. Multi-site Analysis Reveals Widespread Antibiotic Resistance in the Marine Pathogen Vibrio vulnificus . Microb Ecol 57, 151–159 (2009). https://doi.org/10.1007/s00248-008-9413-8

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