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Title: Subinhibitory Concentrations of Amoxicillin, Lincomycin, and Oxytetracycline Commonly Used to Treat Swine Increase Streptococcus suis Biofilm Formation

Abstract

Streptococcus suis is a bacterial swine pathogen with a significant economic burden. It typically colonizes the tonsil and nasal cavity of swine causing a variety of symptoms ranging from asymptomatic carriage to lethal systemic disease. A key barrier toward the development of improved vaccines or interventions for S. suis infections is a gap in our understanding of the mechanisms contributing to persistence in the host, in which colonized pigs continue to shed and transmit S. suis. We hypothesized that exposure to sub-MICs of antibiotics commonly used by the swine industry would increase the biofilm capacity of S. suis strains. Using a 96-well plate MIC protocol, we experimentally determined the MIC for each of 12 antibiotics for a virulent strain of S. suis strain that consistently formed biofilms using a standard crystal violet assay. Using this static biofilm assay, we demonstrated that sub-MICs of bacitracin, carbadox, chlortetracycline, enrofloxacin, gentamicin, neomycin, sulfadimethoxine, tiamulin, and tylosin did not increase S. suis biofilms. In contrast, we demonstrated that sub-MICs of amoxicillin, lincomycin, and oxytetracycline increased overall biofilm formation under both static and flow conditions. The biofilm formation of 11 additional clinical isolates were measured using the relevant concentrations of amoxicillin, lincomycin, and oxytetracycline. Here,more » eight of the eleven strains increased the biofilm formation with lincomycin, seven with amoxicillin, and three with oxytetracycline. Collectively, our data demonstrate that exposure to sub-MICs of these commonly used antibiotics contributes to increased biofilm formation of S. suis, thereby potentially increasing survival and persistence within the respiratory tract of swine.« less

Authors:
 [1];  [2]
  1. Oak Ridge Institute for Science and Education, Oak Ridge, TN (United States); United States Dept. of Agriculture, Ames, IA (United States)
  2. United States Dept. of Agriculture, Ames, IA (United States)
Publication Date:
Research Org.:
Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1494697
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Streptococcus suis; biofilm; subinhibitory concentrations; antibiotics; swine; agriculture

Citation Formats

Waack, Ursula, and Nicholson, Tracy L. Subinhibitory Concentrations of Amoxicillin, Lincomycin, and Oxytetracycline Commonly Used to Treat Swine Increase Streptococcus suis Biofilm Formation. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.02707.
Waack, Ursula, & Nicholson, Tracy L. Subinhibitory Concentrations of Amoxicillin, Lincomycin, and Oxytetracycline Commonly Used to Treat Swine Increase Streptococcus suis Biofilm Formation. United States. doi:10.3389/fmicb.2018.02707.
Waack, Ursula, and Nicholson, Tracy L. Tue . "Subinhibitory Concentrations of Amoxicillin, Lincomycin, and Oxytetracycline Commonly Used to Treat Swine Increase Streptococcus suis Biofilm Formation". United States. doi:10.3389/fmicb.2018.02707. https://www.osti.gov/servlets/purl/1494697.
@article{osti_1494697,
title = {Subinhibitory Concentrations of Amoxicillin, Lincomycin, and Oxytetracycline Commonly Used to Treat Swine Increase Streptococcus suis Biofilm Formation},
author = {Waack, Ursula and Nicholson, Tracy L.},
abstractNote = {Streptococcus suis is a bacterial swine pathogen with a significant economic burden. It typically colonizes the tonsil and nasal cavity of swine causing a variety of symptoms ranging from asymptomatic carriage to lethal systemic disease. A key barrier toward the development of improved vaccines or interventions for S. suis infections is a gap in our understanding of the mechanisms contributing to persistence in the host, in which colonized pigs continue to shed and transmit S. suis. We hypothesized that exposure to sub-MICs of antibiotics commonly used by the swine industry would increase the biofilm capacity of S. suis strains. Using a 96-well plate MIC protocol, we experimentally determined the MIC for each of 12 antibiotics for a virulent strain of S. suis strain that consistently formed biofilms using a standard crystal violet assay. Using this static biofilm assay, we demonstrated that sub-MICs of bacitracin, carbadox, chlortetracycline, enrofloxacin, gentamicin, neomycin, sulfadimethoxine, tiamulin, and tylosin did not increase S. suis biofilms. In contrast, we demonstrated that sub-MICs of amoxicillin, lincomycin, and oxytetracycline increased overall biofilm formation under both static and flow conditions. The biofilm formation of 11 additional clinical isolates were measured using the relevant concentrations of amoxicillin, lincomycin, and oxytetracycline. Here, eight of the eleven strains increased the biofilm formation with lincomycin, seven with amoxicillin, and three with oxytetracycline. Collectively, our data demonstrate that exposure to sub-MICs of these commonly used antibiotics contributes to increased biofilm formation of S. suis, thereby potentially increasing survival and persistence within the respiratory tract of swine.},
doi = {10.3389/fmicb.2018.02707},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 2 works
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Figures / Tables:

Figure 1 Figure 1: Sub-MICs of specific antibiotics increase biofilms formed by S. suis. WT S. suis was incubated O/N in a 96-well plate with sub-MICs of commonly used antibiotics. After incubation, the OD600 of each well was measured and the plate was stained using a standard crystal violet assay and visualizedmore » by OD538. All OD538 values were normalized by OD600 values. Biofilm assay performed with sub-MICs of (A) Amoxicillin. (B) Lincomycin. (C) Oxytetracycline. Values are the means ± standard deviations (error bars) from three independent experiments, with three technical replicates in each experiment. Significant differences were assessed by ordinary one-way ANOVA with Dunnett’s multiple comparison post-test; ∗ p < 0.05, ∗ ∗ p < 0.01.« less

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Works referenced in this record:

The world of subinhibitory antibiotic concentrations
journal, October 2006

  • Davies, Julian; Spiegelman, George B.; Yim, Grace
  • Current Opinion in Microbiology, Vol. 9, Issue 5
  • DOI: 10.1016/j.mib.2006.08.006

Role of Biofilm Roughness and Hydrodynamic Conditions in Legionella pneumophila Adhesion to and Detachment from Simulated Drinking Water Biofilms
journal, March 2015

  • Shen, Yun; Monroy, Guillermo L.; Derlon, Nicolas
  • Environmental Science & Technology, Vol. 49, Issue 7
  • DOI: 10.1021/es505842v

Dual Effects of MLS Antibiotics
journal, September 2004


Environmental pH influences Candida albicans biofilms regarding its structure, virulence and susceptibility to fluconazole
journal, April 2014

  • Vasconcellos, Andréa Araújo de; Gonçalves, Letícia Machado; Del Bel Cury, Altair Antoninha
  • Microbial Pathogenesis, Vol. 69-70
  • DOI: 10.1016/j.micpath.2014.03.009

Bacterial biofilms: from the Natural environment to infectious diseases
journal, February 2004

  • Hall-Stoodley, Luanne; Costerton, J. William; Stoodley, Paul
  • Nature Reviews Microbiology, Vol. 2, Issue 2, p. 95-108
  • DOI: 10.1038/nrmicro821

Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies
journal, October 2013

  • de la Fuente-Núñez, César; Reffuveille, Fany; Fernández, Lucía
  • Current Opinion in Microbiology, Vol. 16, Issue 5
  • DOI: 10.1016/j.mib.2013.06.013

Low Levels of β-Lactam Antibiotics Induce Extracellular DNA Release and Biofilm Formation in Staphylococcus aureus
journal, July 2012


Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms
journal, April 2002


Evidence of In Vivo Prophage Induction during Clostridium difficile Infection
journal, August 2012

  • Meessen-Pinard, Mathieu; Sekulovic, Ognjen; Fortier, Louis-Charles
  • Applied and Environmental Microbiology, Vol. 78, Issue 21
  • DOI: 10.1128/AEM.02275-12

Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics
journal, December 2002

  • Goh, E. -B.; Yim, G.; Tsui, W.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 26
  • DOI: 10.1073/pnas.252607699

Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria
journal, March 2017

  • Hall, Clayton W.; Mah, Thien-Fah
  • FEMS Microbiology Reviews, Vol. 41, Issue 3
  • DOI: 10.1093/femsre/fux010

Growth in a Biofilm Induces a Hyperinfectious Phenotype in Vibrio cholerae
journal, June 2010

  • Tamayo, R.; Patimalla, B.; Camilli, A.
  • Infection and Immunity, Vol. 78, Issue 8
  • DOI: 10.1128/IAI.00048-10

Characterization and Comparison of Biofilm Development by Pathogenic and Commensal Isolates of Histophilus somni
journal, July 2007

  • Sandal, I.; Hong, W.; Swords, W. E.
  • Journal of Bacteriology, Vol. 189, Issue 22
  • DOI: 10.1128/JB.00479-07

Bacterial Biofilms: A Common Cause of Persistent Infections
journal, May 1999


Effects of Low-Dose Amoxicillin on Staphylococcus aureus USA300 Biofilms
journal, February 2016

  • Mlynek, Kevin D.; Callahan, Mary T.; Shimkevitch, Anton V.
  • Antimicrobial Agents and Chemotherapy, Vol. 60, Issue 5
  • DOI: 10.1128/AAC.02070-15

Role of biofilm in children with recurrent upper respiratory tract infections
journal, October 2014

  • Nazzari, E.; Torretta, S.; Pignataro, L.
  • European Journal of Clinical Microbiology & Infectious Diseases, Vol. 34, Issue 3
  • DOI: 10.1007/s10096-014-2261-1

Quantitative proteomic analysis of sub-MIC erythromycin inhibiting biofilm formation of S. suis in vitro
journal, February 2015


The Bordetella Bps Polysaccharide Is Required for Biofilm Formation and Enhances Survival in the Lower Respiratory Tract of Swine
journal, May 2017

  • Nicholson, Tracy L.; Brockmeier, Susan L.; Sukumar, Neelima
  • Infection and Immunity, Vol. 85, Issue 8
  • DOI: 10.1128/IAI.00261-17

Quantification of biofilm structures by the novel computer program comstat
journal, October 2000


Candida albicans survival and biofilm formation under starvation conditions
journal, July 2012


Inducibility of Tn916 conjugative transfer in Enterococcus faecalis by subinhibitory concentrations of ribosome-targeting antibiotics
journal, July 2017

  • Scornec, Hélène; Bellanger, Xavier; Guilloteau, Hélène
  • Journal of Antimicrobial Chemotherapy, Vol. 72, Issue 10
  • DOI: 10.1093/jac/dkx202

Streptococcus suis Serotype 2 Biofilms Inhibit the Formation of Neutrophil Extracellular Traps
journal, March 2017


Biofilm production by Staphylococcus aureus associated with intramammary infection
journal, May 2005


Microbiological effects of sublethal levels of antibiotics
journal, May 2014

  • Andersson, Dan I.; Hughes, Diarmaid
  • Nature Reviews Microbiology, Vol. 12, Issue 7
  • DOI: 10.1038/nrmicro3270

Livestock-Associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) Isolates of Swine Origin Form Robust Biofilms
journal, August 2013


Sub-MICs of Azithromycin Decrease Biofilm Formation of Streptococcus suis and Increase Capsular Polysaccharide Content of S. suis
journal, October 2016


Roles of ionic strength and biofilm roughness on adhesion kinetics of Escherichia coli onto groundwater biofilm grown on PVC surfaces
journal, May 2013


Antibiotic-Induced Biofilm Formation
journal, September 2011

  • Kaplan, Jeffrey B.
  • The International Journal of Artificial Organs, Vol. 34, Issue 9
  • DOI: 10.5301/ijao.5000027

Sub-MIC Tylosin Inhibits Streptococcus suis Biofilm Formation and Results in Differential Protein Expression
journal, March 2016


    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.