Influences of Biofilm Structure and Antibiotic Resistance Mechanisms on Indirect Pathogenicity in a Model Polymicrobial Biofilm

Abstract

Indirect pathogenicity (IP), the commensal protection of antibiotic-sensitive pathogens by resistant microorganisms of low intrinsic virulence, can prevent the eradication of polymicrobial infections. The contributions of antibiotic resistance mechanisms and biofilm structure to IP within polymicrobial biofilms were investigated using a model two-member consortium. Escherichia coli ATCC 33456 was transformed with vectors conferring either ampicillin or spectinomycin resistance, creating two distinct populations with different resistance mechanisms. Each strain alone or the consortium was grown as biofilms in flow cells and planktonically in chemostats. Comparisons in survival and activity were made on the basis of MICs and minimum biofilm preventative concentrations, a newly introduced descriptor. In ampicillin-containing medium, commensal interactions were evident during both modes of cultivation, but the sensitive strain experienced a greater benefit in the chemostat, indicating that the biofilm environment limited the commensal interaction between the Amp r and Spt r strains. In spectinomycin-containing medium, growth of the sensitive strain in chemostats and biofilms was not aided by the resistant strain. However, green fluorescent protein expression by the sensitive strain was greater in mixed-population biofilms (9% ؎ 1%) than when the strain was grown alone (2% ؎ 0%). No comparable benefit was evident during growth in the chemostat, indicating that the biofilm structure contributed to enhanced activity of the sensitive strain.The concept of indirect pathogenicity (IP) describes the circumstance where, in a mixed infection, an antibiotic-resistant microorganism of low intrinsic virulence protects an antibiotic-sensitive pathogen from eradication. IP was recognized during treatment failure of polymicrobial infections, and numerous examples involving beta-lactamaseproducing bacteria have been reported (3,15,16). IP is a form of commensalism, which is an interactive association where one organism benefits while the other is not affected (2). In the case of beta-lactamase-producing bacteria, susceptible antibiotics including penicillins and cephalosporins are inactivated via hydrolysis of the cyclic amide bond (25), leading to commensal protection of the sensitive strain. The occurrence of IP in microbial biofilms, or surface-attached communities of microorganisms, could have broad significance, because diverse kinds of polymicrobial infections are biofilm based, including device-related infections (8), ventilator-associated pneumonia (1), wounds (9), and abscesses (4). Presently, little information is available on the role of biofilm structure in the severity of IP or the development of IP in the presence of non-beta-lactam antibiotics.In a polymicrobial infection exhibiting IP, the efficiency of antibiotic inactivation by a resistant microorganism should determine the extent of the commensal protection provided to the sensitive microorganism. To investigate the role of antibiotic detoxification mechanisms in...

Biological activities ofRosmarinus officinalisL. (rosemary) extract as analyzed in microorganisms and cells

“…In polymicrobial biofilms, the different species may compete and this could harm or favor the development of each other. 6,7 In association of C. albicans (85.87 AE 17.48%) with E. faecalis (93.03 AE 2.44%), there was no significant difference between the reductions presented by the yeast and the bacterium. Cruz et al,…”

“…In these associations, a microorganism may favor or hinder the development of other, interfere with antimicrobial susceptibility, as well as interfere with the expression of genes that may lead to generation of pathogenic forms. 6,7 C. albicans biofilm can be formed after contact with a suitable surface, and its development will depend on favorable conditions. In the initial stage, the adhered yeast forms initiate the formation of germ tube, and subsequently, in the intermediate phase, there will be an elongation of these hyphae and production of extracellular matrix, composed of carbohydrates and proteins.…”

The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus

“…In general, the main complication resulting from biofilm formation is that bacteria inside these biofilms are protected well and become much more resistant to antibiotic treatment as compared to planktonic cells (34)(35)(36)(37) and this, in turn, contributes to the further progression of the infection.…”

Pathogenesis of Polymicrobial Biofilms

“…This phenomenon describes an interactive association where one organism benefits while the other is not affected [30]. For example, in a mixed infection, an antibiotic-resistant microorganism of low intrinsic virulence protects an antibiotic-sensitive pathogen from eradication [30,31]. Interestingly, a similar phenomenon was recently described for S. aureus and C. albicans where the coexistence of these human pathogens in a biofilm resulted in increased S. aureus resistance to vancomycin [32].…”

“…This phenomenon describes an interactive association where one organism benefits while the other is not affected [30]. For example, in a mixed infection, an antibiotic-resistant microorganism of low intrinsic virulence protects an antibiotic-sensitive pathogen from eradication [30,31].…”