Synergistic interactions of Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro wound model
In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence. One of the most prevalent types of polymicrobial infection occurs in chronic wounds, where Pseudomonas aeruginosa and Staphylococcus aureus ar...
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| Vydáno v: | Infection and immunity Ročník 82; číslo 11; s. 4718 |
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| Hlavní autoři: | , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
01.11.2014
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| ISSN: | 1098-5522, 1098-5522 |
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| Abstract | In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence. One of the most prevalent types of polymicrobial infection occurs in chronic wounds, where Pseudomonas aeruginosa and Staphylococcus aureus are the two most common causes. Although they are the most commonly associated microbial species in wound infections, very little is known about their interspecies relationship. Evidence suggests that P. aeruginosa-S. aureus coinfections are more virulent than monoculture infection with either species; however, difficulties in growing these two pathogens together in vitro have hampered attempts to uncover the mechanisms involved. Here we describe a simple and clinically relevant in vitro wound model that supported concomitant growth of P. aeruginosa and S. aureus. We observed that the ability of P. aeruginosa and S. aureus to survive antibiotic treatment increased when they were grown together in planktonic cocultures and that antibiotic tolerance was further enhanced when they were grown together in the wound model. We attributed this enhanced tolerance to both the "host-derived" and "bacterium-derived" matrix components. Taken together, our data indicate that P. aeruginosa and S. aureus may benefit each other by coinfecting wounds and that the host-derived matrix may serve as important a role as the bacterium-derived matrix in protecting bacteria from some antibiotics. |
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| AbstractList | In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence. One of the most prevalent types of polymicrobial infection occurs in chronic wounds, where Pseudomonas aeruginosa and Staphylococcus aureus are the two most common causes. Although they are the most commonly associated microbial species in wound infections, very little is known about their interspecies relationship. Evidence suggests that P. aeruginosa-S. aureus coinfections are more virulent than monoculture infection with either species; however, difficulties in growing these two pathogens together in vitro have hampered attempts to uncover the mechanisms involved. Here we describe a simple and clinically relevant in vitro wound model that supported concomitant growth of P. aeruginosa and S. aureus. We observed that the ability of P. aeruginosa and S. aureus to survive antibiotic treatment increased when they were grown together in planktonic cocultures and that antibiotic tolerance was further enhanced when they were grown together in the wound model. We attributed this enhanced tolerance to both the "host-derived" and "bacterium-derived" matrix components. Taken together, our data indicate that P. aeruginosa and S. aureus may benefit each other by coinfecting wounds and that the host-derived matrix may serve as important a role as the bacterium-derived matrix in protecting bacteria from some antibiotics.In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence. One of the most prevalent types of polymicrobial infection occurs in chronic wounds, where Pseudomonas aeruginosa and Staphylococcus aureus are the two most common causes. Although they are the most commonly associated microbial species in wound infections, very little is known about their interspecies relationship. Evidence suggests that P. aeruginosa-S. aureus coinfections are more virulent than monoculture infection with either species; however, difficulties in growing these two pathogens together in vitro have hampered attempts to uncover the mechanisms involved. Here we describe a simple and clinically relevant in vitro wound model that supported concomitant growth of P. aeruginosa and S. aureus. We observed that the ability of P. aeruginosa and S. aureus to survive antibiotic treatment increased when they were grown together in planktonic cocultures and that antibiotic tolerance was further enhanced when they were grown together in the wound model. We attributed this enhanced tolerance to both the "host-derived" and "bacterium-derived" matrix components. Taken together, our data indicate that P. aeruginosa and S. aureus may benefit each other by coinfecting wounds and that the host-derived matrix may serve as important a role as the bacterium-derived matrix in protecting bacteria from some antibiotics. In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence. One of the most prevalent types of polymicrobial infection occurs in chronic wounds, where Pseudomonas aeruginosa and Staphylococcus aureus are the two most common causes. Although they are the most commonly associated microbial species in wound infections, very little is known about their interspecies relationship. Evidence suggests that P. aeruginosa-S. aureus coinfections are more virulent than monoculture infection with either species; however, difficulties in growing these two pathogens together in vitro have hampered attempts to uncover the mechanisms involved. Here we describe a simple and clinically relevant in vitro wound model that supported concomitant growth of P. aeruginosa and S. aureus. We observed that the ability of P. aeruginosa and S. aureus to survive antibiotic treatment increased when they were grown together in planktonic cocultures and that antibiotic tolerance was further enhanced when they were grown together in the wound model. We attributed this enhanced tolerance to both the "host-derived" and "bacterium-derived" matrix components. Taken together, our data indicate that P. aeruginosa and S. aureus may benefit each other by coinfecting wounds and that the host-derived matrix may serve as important a role as the bacterium-derived matrix in protecting bacteria from some antibiotics. |
| Author | Clinton, Allie Horswill, Alexander R Rumbaugh, Kendra P Fowler, Haley Everett, Jake DeLeon, Stephanie |
| Author_xml | – sequence: 1 givenname: Stephanie surname: DeLeon fullname: DeLeon, Stephanie organization: Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas, USA – sequence: 2 givenname: Allie surname: Clinton fullname: Clinton, Allie organization: Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas, USA Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, Texas, USA – sequence: 3 givenname: Haley surname: Fowler fullname: Fowler, Haley organization: Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas, USA – sequence: 4 givenname: Jake surname: Everett fullname: Everett, Jake organization: Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas, USA Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, Texas, USA – sequence: 5 givenname: Alexander R surname: Horswill fullname: Horswill, Alexander R organization: Department of Microbiology, Carver College of Medicine, University of Iowa, Iowa City, Iowa, USA – sequence: 6 givenname: Kendra P surname: Rumbaugh fullname: Rumbaugh, Kendra P email: kendra.rumbaugh@ttuhsc.edu organization: Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas, USA kendra.rumbaugh@ttuhsc.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25156721$$D View this record in MEDLINE/PubMed |
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| PublicationTitleAlternate | Infect Immun |
| PublicationYear | 2014 |
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| References_xml | – reference: 7986003 - Antimicrob Agents Chemother. 1994 Aug;38(8):1732-41 – reference: 17562773 - Infect Immun. 2007 Aug;75(8):3715-21 – reference: 21557060 - Adv Exp Med Biol. 2011;715:105-23 – reference: 20236200 - J Eur Acad Dermatol Venereol. 2010 Sep;24(9):1017-25 – reference: 16411377 - Br J Biomed Sci. 2005;62(4):175-8 – reference: 24101503 - Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18380-5 – reference: 111024 - Microbiol Rev. 1979 Mar;43(1):73-102 – reference: 11157916 - J Antimicrob Chemother. 2001 Feb;47(2):239-40 – reference: 18211573 - Wound Repair Regen. 2008 Jan-Feb;16(1):2-10 – reference: 15995954 - J Infect Dis. 2005 Aug 1;192(3):410-9 – reference: 19207742 - FEMS Microbiol Rev. 2009 Jul;33(4):704-17 – reference: 25054067 - J Pathog. 2014;2014:173053 – reference: 24126517 - Infect Immun. 2014 Jan;82(1):92-100 – reference: 16286361 - J Antimicrob Chemother. 2005 Dec;56(6):1042-6 – reference: 4014440 - Am J Pathol. 1985 Jul;120(1):13-21 – reference: 20216488 - J Wound Care. 2010 Feb;19(2):45-6, 48-50, 52-3 – reference: 20616768 - J Wound Care. 2010 Jul;19(7):272-8, 280-1 – reference: 16984578 - Int Wound J. 2006 Sep;3(3):225-31 – reference: 15673721 - Antimicrob Agents Chemother. 2005 Feb;49(2):479-87 – reference: 22009290 - Eur J Clin Microbiol Infect Dis. 2012 Jul;31(7):1347-52 – reference: 18508940 - J Clin Microbiol. 2008 Aug;46(8):2717-22 – reference: 20961515 - Euro Surveill. 2010 Oct 14;15(41):19688 – reference: 20418950 - PLoS One. 2010;5(4):e10146 – reference: 8419592 - J Pediatr. 1993 Jan;122(1):1-9 – reference: 19188357 - Infect Immun. 2009 Apr;77(4):1623-35 – reference: 239464 - Thromb Res. 1975 Jun;6(6):501-10 – reference: 22132176 - PLoS One. 2011;6(11):e27943 – reference: 22076151 - PLoS One. 2011;6(11):e27317 – reference: 15866058 - J Diabetes Complications. 2005 May-Jun;19(3):138-41 – reference: 23007678 - Med Microbiol Immunol. 2013 Apr;202(2):131-41 – reference: 15215091 - Antimicrob Agents Chemother. 2004 Jul;48(7):2431-6 – reference: 19128252 - Wound Repair Regen. 2008 Nov-Dec;16(6):805-13 – reference: 4313167 - Appl Microbiol. 1969 Nov;18(5):766-70 – reference: 17873029 - J Bacteriol. 2007 Nov;189(22):8079-87 – reference: 18325110 - BMC Microbiol. 2008;8:43 – reference: 23451098 - PLoS One. 2013;8(2):e56846 – reference: 16879411 - Mol Microbiol. 2006 Sep;61(5):1308-21 – reference: 18603682 - Indian J Pathol Microbiol. 2008 Apr-Jun;51(2):204-8 – reference: 19389780 - Microbiology. 2009 Jul;155(Pt 7):2148-56 – reference: 15302726 - Chest. 2004 Aug;126(2):412-9 – reference: 23433007 - Int Wound J. 2015 Feb;12(1):47-52 – reference: 3104732 - Microbios. 1987;49(198):55-64 – reference: 11407793 - J Bone Joint Surg Am. 2001 Jun;83-A(6):855-61 – reference: 17449616 - J Bacteriol. 2007 Jun;189(12):4367-74 – reference: 19816382 - J Wound Care. 2009 Oct;18(10):426-31 – reference: 16751497 - Appl Environ Microbiol. 2006 Jun;72(6):3916-23 – reference: 23751003 - Environ Microbiol. 2013 Oct;15(10):2865-78 – reference: 20835702 - Diabetologia. 2011 Jan;54(1):58-64 – reference: 18211572 - Wound Repair Regen. 2008 Jan-Feb;16(1):1 – reference: 16030221 - J Bacteriol. 2005 Aug;187(15):5267-77 – reference: 19564370 - Antimicrob Agents Chemother. 2009 Sep;53(9):3914-22 – reference: 20081576 - J Wound Care. 2009 Dec;18(12):508, 510-12 – reference: 17419768 - FEMS Microbiol Lett. 2007 May;270(2):179-88 – reference: 19812273 - J Clin Microbiol. 2009 Dec;47(12):4084-9 – reference: 16030228 - J Bacteriol. 2005 Aug;187(15):5341-6 – reference: 21544190 - PLoS One. 2011;6(4):e19036 – reference: 17172450 - Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19890-5 – reference: 18086294 - Wound Repair Regen. 2008 Jan-Feb;16(1):37-44 |
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| Snippet | In individuals with polymicrobial infections, microbes often display synergistic interactions that can enhance their colonization, virulence, or persistence.... |
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| SubjectTerms | Anti-Bacterial Agents - pharmacology Bacteriological Techniques - methods Coculture Techniques - methods Drug Resistance, Bacterial - physiology Pseudomonas aeruginosa - drug effects Pseudomonas aeruginosa - physiology Staphylococcus aureus - drug effects Staphylococcus aureus - physiology |
| Title | Synergistic interactions of Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro wound model |
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