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Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms

Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms
Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms
Most biofilms in their natural environments are likely to consist of consortia of species that influence each other in synergistic and antagonistic manners. However, few reports specifically address interactions within multispecies biofilms. In this study, 17 epiphytic bacterial strains, isolated from the surface of the marine alga Ulva australis, were screened for synergistic interactions within biofilms when present together in different combinations. Four isolates, Microbacterium phyllosphaerae, Shewanella japonica, Dokdonia donghaensis, and Acinetobacter lwoffii, were found to interact synergistically in biofilms formed in 96-well microtiter plates: biofilm biomass was observed to increase by >167% in biofilms formed by the four strains compared to biofilms composed of single strains. When exposed to the antibacterial agent hydrogen peroxide or tetracycline, the relative activity (exposed versus nonexposed biofilms) of the four-species biofilm was markedly higher than that in any of the single-species biofilms. Moreover, in biofilms established on glass surfaces in flow cells and subjected to invasion by the antibacterial protein-producing Pseudoalteromonas tunicata, the four-species biofilms resisted invasion to a greater extent than did the biofilms formed by the single species. Replacement of each strain by its cell-free culture supernatant suggested that synergy was dependent both on species-specific physical interactions between cells and on extracellular secreted factors or less specific interactions. In summary, our data strongly indicate that synergistic effects promote biofilm biomass and resistance of the biofilm to antimicrobial agents and bacterial invasion in multispecies biofilms.
0099-2240
3916-3923
Burmolle, Mette
43036356-ea3e-435e-ba32-c63d5397a6b0
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Rao, Dhana
53623cf3-0196-43cb-a592-16479aacb918
Hansen, Lars H.
5fa838ac-8e1c-47a2-aea7-063390fd2c0b
Sorensen, Soren J.
b39b2a92-0609-445b-b23d-5b8caaa21bf6
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e
Burmolle, Mette
43036356-ea3e-435e-ba32-c63d5397a6b0
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Rao, Dhana
53623cf3-0196-43cb-a592-16479aacb918
Hansen, Lars H.
5fa838ac-8e1c-47a2-aea7-063390fd2c0b
Sorensen, Soren J.
b39b2a92-0609-445b-b23d-5b8caaa21bf6
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e

Burmolle, Mette, Webb, Jeremy S., Rao, Dhana, Hansen, Lars H., Sorensen, Soren J. and Kjelleberg, Staffan (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Applied and Environmental Microbiology, 72 (6), 3916-3923. (doi:10.1128/AEM.03022-05).

Record type: Article

Abstract

Most biofilms in their natural environments are likely to consist of consortia of species that influence each other in synergistic and antagonistic manners. However, few reports specifically address interactions within multispecies biofilms. In this study, 17 epiphytic bacterial strains, isolated from the surface of the marine alga Ulva australis, were screened for synergistic interactions within biofilms when present together in different combinations. Four isolates, Microbacterium phyllosphaerae, Shewanella japonica, Dokdonia donghaensis, and Acinetobacter lwoffii, were found to interact synergistically in biofilms formed in 96-well microtiter plates: biofilm biomass was observed to increase by >167% in biofilms formed by the four strains compared to biofilms composed of single strains. When exposed to the antibacterial agent hydrogen peroxide or tetracycline, the relative activity (exposed versus nonexposed biofilms) of the four-species biofilm was markedly higher than that in any of the single-species biofilms. Moreover, in biofilms established on glass surfaces in flow cells and subjected to invasion by the antibacterial protein-producing Pseudoalteromonas tunicata, the four-species biofilms resisted invasion to a greater extent than did the biofilms formed by the single species. Replacement of each strain by its cell-free culture supernatant suggested that synergy was dependent both on species-specific physical interactions between cells and on extracellular secreted factors or less specific interactions. In summary, our data strongly indicate that synergistic effects promote biofilm biomass and resistance of the biofilm to antimicrobial agents and bacterial invasion in multispecies biofilms.

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Published date: June 2006

Identifiers

Local EPrints ID: 41045
URI: http://eprints.soton.ac.uk/id/eprint/41045
ISSN: 0099-2240
PURE UUID: 5ce7c3cd-df50-4154-b095-cd43addcd5d8
ORCID for Jeremy S. Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 14 Jul 2006
Last modified: 10 Dec 2019 01:43

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