Abstract

Bacteria and Candida albicans are prominent gut microbiota, and the translocation of these organisms into blood circulation might induce mixed-organism biofilms, which warrants the exploration of mixed- versus single-organism biofilms in vitro and in vivo. In single-organism biofilms, Acinetobacter baumannii and Pseudomonas aeruginosa (PA) produced the least and the most prominent biofilms, respectively. C. albicans with P. aeruginosa (PA+CA) induced the highest biofilms among mixed-organism groups as determined by crystal violet straining. The sessile form of PA+CA induced higher macrophage responses than sessile PA, which supports enhanced immune activation toward mixed-organism biofilms. In addition, Candida incubated in pre-formed Pseudomonas biofilms (PA>CA) produced even higher biofilms than PA+CA (simultaneous incubation of both organisms) as determined by fluorescent staining on biofilm matrix (AF647 color). Despite the initially lower bacteria during preparation, bacterial burdens by culture in mixed-organism biofilms (PA+CA and PA>CA) were not different from biofilms of PA alone, supporting Candida-enhanced Pseudomonas growth. Moreover, proteomic analysis in PA>CA biofilms demonstrated high AlgU and mucA with low mucB when compared with PA alone or PA+CA, implying an alginate-related mucoid phenotype in PA>CA biofilms. Furthermore, mice with PA>CA biofilms demonstrated higher bacteremia with more severe sepsis compared with mice with PA+CA biofilms. This is possibly due to the different structures. Interestingly, l-cysteine, a biofilm matrix inhibitor, attenuated mixed-organism biofilms both in vitro and in mice. In conclusion, Candida enhanced Pseudomonas alginate–related biofilm production, and Candida presentation in pre-formed Pseudomonas biofilms might alter biofilm structures that affect clinical manifestations but was attenuated by l-cysteine.

Highlights

  • Biofilms are a community of microorganisms that grow on both nonliving and biotic surfaces to survive in harsh environments by producing multilayers of high-abundance extracellular matrix (ECM) consisting of proteins, polysaccharides, and nucleic acids (Flemming et al, 2007; de Kievit, 2009; Ghafoor et al, 2011; Flemming et al, 2016)

  • Candida albicans enhanced biofilm production of P. aeruginosa through the induction of alginate-related proteins and was attenuated by L-cysteine, which has been proposed as an interesting anti-biofilm in clinical situations

  • Crystal violet– stained biofilms were higher in P. aeruginosa plus C. albicans (PA+CA) as early as 48 h post-incubation (Figure 1B)

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Summary

Introduction

Biofilms are a community of microorganisms that grow on both nonliving and biotic surfaces to survive in harsh environments by producing multilayers of high-abundance extracellular matrix (ECM) consisting of proteins, polysaccharides, and nucleic acids (Flemming et al, 2007; de Kievit, 2009; Ghafoor et al, 2011; Flemming et al, 2016). Surface-adherent (sessile) bacteria in biofilms become more antibiotic resistant than the free living (planktonic) form and result in recurrent infections (Darouiche et al, 2002; Aslam and Darouiche, 2011). Biofilms possibly form nidus at the surface for the attachment of other pathogens that lead to biofilms of multiple bacteria or multiorganisms (Yang et al, 2011). Catheter-related colonization of Gram-positive bacteria from skin microbiota (Streptococcus spp. and Staphylococcus spp.) is common, biofilms in the inner lumen of the catheter consist of both Gram-positive and -negative bacteria (Murga et al, 2001)

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