Interspecies competition triggers virulence and mutability in Candida albicans–Pseudomonas aeruginosa mixed biofilms

Abstract

Inter-kingdom and interspecies interactions are ubiquitous in nature and are important for the survival of species and ecological balance. The investigation of microbe-microbe interactions is essential for understanding the in vivo activities of commensal and pathogenic microorganisms. Candida albicans, a polymorphic fungus, and Pseudomonas aeruginosa, a Gram-negative bacterium, are two opportunistic pathogens that interact in various polymicrobial infections in humans. To determine how P. aeruginosa affects the physiology of C. albicans and vice versa, we compared the proteomes of each species in mixed biofilms versus single-species biofilms. In addition, extracellular proteins were analyzed. We observed that, in mixed biofilms, both species showed differential expression of virulence proteins, multidrug resistance-associated proteins, proteases and cell defense, stress and iron-regulated proteins. Furthermore, in mixed biofilms, both species displayed an increase in mutability compared with monospecific biofilms. This characteristic was correlated with the downregulation of enzymes conferring protection against DNA oxidation. In mixed biofilms, P. aeruginosa regulates its production of various molecules involved in quorum sensing and induces the production of virulence factors (pyoverdine, rhamnolipids and pyocyanin), which are major contributors to the ability of this bacterium to cause disease. Overall, our results indicate that interspecies competition between these opportunistic pathogens enhances the production of virulence factors and increases mutability and thus can alter the course of hostpathogen interactions in polymicrobial infections.

Harnessing Bacterial Signals for Suppression of Biofilm Formation in the Nosocomial Fungal Pathogen Aspergillus fumigatus

“…The P. aeruginosa signaling molecules HHQ and PQS have previously been shown to possess interkingdom activity, influencing the phenotypic and transcriptional behavior of both microbes and higher order organisms (Reen et al, 2011; Tashiro et al, 2013; Trejo-Hernandez et al, 2014), including mammalian cells (Kim et al, 2010). While the P. aeruginosa secretome has previously been shown to suppress biofilm formation in A. fumigatus (Mowat et al, 2010), the extent of the active components remained to be defined.…”

“…The AHL class of quorum sensing signal has also been shown to play a role in modulating biofilm formation in these fungal pathogens (McAlester et al, 2008; Mowat et al, 2010), while HHQ and PQS have previously been shown to modulate biofilm formation in C. albicans (Reen et al, 2011, 2016). Apart from signal mediated interactions, there is recent evidence to suggest that interspecies and interkingdom interactions can foster mutability in co-existing organisms (Michelsen et al, 2014; Trejo-Hernandez et al, 2014). It must also be considered that microbial signals are just one factor in the process of fungal biofilm formation in the host.…”

The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil

“…In this study, we found a potential ‘coalescence’ of bacterial and fungal biofilms. Multi-species biofilms can prevail in nature (Hogan and Kolter, 2002; Brandl et al, 2011; Morales et al, 2013; Trejo-Hernández et al, 2014) if they confer a survival strategy to the partners. In such biofilms, the ECM, composed of secreted compounds, establishes a complex matrix structure (Flemming and Wingender, 2010).…”

Candida Survival Strategies

“…Furthermore farnesol inhibits the swarming activity of P. aeruginosa (Cugini et al, 2007;McAlester et al, 2008;Williams & Camara, 2009). A recent comparison of the proteome of both species in mixed-species biofilms revealed that the coexistence of both species leads to enhanced production of virulence factors and increased mutability in both species, potentially altering hostepathogen interactions (Trejo-Hernandez, Andrade-Dominguez, Hernandez, & Encarnacion, 2014). Although the relationship between P. aeruginosa and C. albicans is generally antagonistic, P. aeruginosa can also promote C. albicans virulence under distinct conditions, e.g., in patients with severe burn wounds (Branski et al, 2009;Sun et al, 2012).…”