Co-Operative Biofilm Interactions between Aspergillus fumigatus and Pseudomonas aeruginosa through Secreted Galactosaminogalactan Exopolysaccharide

Ostapska, Hanna; Mauff, François Le; Gravelat, Fabrice N.; Snarr, Brendan D.; Bamford, Natalie C.; Loon, Jaime C. Van; McKay, Geoffrey A.; Nguyen, Dao M.; Howell, P. Lynne; Sheppard, Donald C.

doi:10.3390/jof8040336

Cited by 10 publications

(9 citation statements)

References 72 publications

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“…No significant growth alterations were noted for P. aeruginosa or A. fumigatus in coculture when compared to monoculture ( Fig. S1A, S1B ), and there was close association between these microbes during co-culture, as shown previously (13, 31, 32) ( Fig. 1A ).…”

Section: Resultssupporting

confidence: 84%

Convergent evolution in toxin detection and resistance provides evidence for conserved bacterial-fungal interactions

Dolan,

Duong,

Whiteley

2023

Preprint

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Microbes rarely exist in isolation, and instead form complex polymicrobial communities. As a result, microbes have developed intricate offensive and defensive strategies that enhance their fitness in these complex communities. Thus, identifying and understanding the molecular mechanisms controlling polymicrobial interactions is critical for understanding the function of microbial communities. In this study, we show that the Gram-negative opportunistic human pathogenPseudomonas aeruginosa, which frequently causes infection alongside a plethora of other microbes including fungi, encodes a genetic network which can detect, and defend against gliotoxin, a potent, disulfide-containing antimicrobial produced by the ubiquitous filamentous fungusAspergillus fumigatus. We show that gliotoxin exposure disruptsP. aeruginosazinc homeostasis, leading to transcriptional activation of a gene encoding a previously uncharacterized dithiol oxidase (DnoP), which detoxifies gliotoxin and structurally related toxins. While the enzymatic activity of DnoP is identical to that used byA. fumigatusto protect itself against gliotoxin, DnoP shares little homology to theA. fumigatusgliotoxin resistance protein. Thus, DnoP and its transcriptional induction by low zinc represent an example of both convergent evolution of toxin defense and environmental cue sensing across kingdoms. Collectively, these data support disulfide-containing natural products as mediators of inter-kingdom interactions and provide evidence thatP. aeruginosahas evolved to survive exposure to these molecules in the natural environment.Significance statementBacteria and fungi frequently exist as complex, polymicrobial communities during infection. Reconstructing ecological structure in the laboratory is challenging and, consequently, the precise molecular mechanisms which underpin microbial interactions remain elusive. Using a pre-clinical model that mimics the cystic fibrosis lung, we discovered that the bacteriumPseudomonas aeruginosadetects and defends against a disulfide-containing toxin produced by the fungusAspergillus fumigatus. In an example of both convergent evolution of toxin defense and environmental cue sensing across kingdoms, we discovered that these organisms use the same cue to produce/sense this toxin, and the same enzymatic mechanism to protect against toxicity. This discovery of convergent evolution provides strong evidence forP. aeruginosaexposure to microbially-produced disulfide-containing toxins in natural environments.

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Section: Resultssupporting

confidence: 84%

Convergent evolution in toxin detection and resistance provides evidence for conserved bacterial-fungal interactions

Dolan,

Duong,

Whiteley

2023

Preprint

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“…3A). To determine whether this operon drives the production of a Pel-like polysaccharide, dot-blot analysis was performed using a monoclonal antibody (mAb) raised against a trimer of N -acetylgalactosamine (22, 77). This antibody is highly specific for the Pel polysaccharide.…”

Section: Resultsmentioning

confidence: 99%

Autoaggregation inStreptococcus intermediusis driven by the Pel polysaccharide

Raju,

Turner,

Castro

et al. 2024

Preprint

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The Streptococcus Milleri Group (SMG) comprising ofStreptococcus intermedius, anginosusandconstellatusare commensal bacteria commonly found in healthy individuals. These bacteria are increasingly being recognized as opportunistic pathogens that can cause purulent infections at sterile body sites and have also been identified in the sputum of individuals with cystic fibrosis. Although the mechanisms of conversion to opportunistic pathogens are not well understood, auto-aggregation is a key driver of biofilm adhesion and cohesion in many Streptococci and Staphylococci. Here, we identify a gene cluster in theS. intermediusgenome with significant homology to the pel operons inBacillus cereusandPseudomonas aeruginosa, which are required for Pel exopolysaccharide production and biofilm formation in these species. Characterization of a panel of clinicalS. intermediusstrains identified a range of aggregating phenotypes. Analysis of the pel operon in the hyper-aggregating C1365 strain revealed that each of the canonicalpelDEADAFGgenes, but not the four additional genes are required for aggregation. Further, we demonstrate that C1365 produces a GalNAc-rich exopolysaccharide and that aggregates can be disrupted by the α-1,4N-acetylgalactosaminidases, PelA and Sph3, but not other glycoside hydrolases, proteinase K or DNase I. Using an abscess model of mouse infection, we show that Pel driven aggregation leads to longer lasting infections, and that lack of Pel allows for the bacteria to be cleared more effectively. The polymer also affects how the bacteria interacts with the host immune system. Collectively, our data suggest that the pel operon has relevancy toS. intermediuspathogenicity.

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“…Our studies were performed in iron-limiting conditions to maintain stress conditions. A possible basis of cooperation between the species is the fact that phenazine metabolites drive positive feedback, which enhances bacterial biofilm formation and facilitates the establishment and growth of A. fumigatus through iron bioavailability [ 57 ].…”

Section: Resultsmentioning

confidence: 99%

The Deciphering of Growth-Dependent Strategies for Quorum-Sensing Networks in Pseudomonas aeruginosa

Juříková,

Mácha,

Lupjanová

et al. 2023

Microorganisms

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Pseudomonas aeruginosa is recognized as a significant cause of morbidity and mortality among nosocomial pathogens. In respiratory infections, P. aeruginosa acts not only as a single player but also collaborates with the opportunistic fungal pathogen Aspergillus fumigatus. This study introduced a QS molecule portfolio as a potential new biomarker that affects the secretion of virulence factors and biofilm formation. The quantitative levels of QS molecules, including 3-o-C12-HSL, 3-o-C8-HSL, C4-HSL, C6-HSL, HHQ, PQS, and PYO, measured using mass spectrometry in a monoculture, indicated metabolic changes during the transition from planktonic to sessile cells. In the co-cultures with A. fumigatus, the profile of abundant QS molecules was reduced to 3-o-C12-HSL, C4-HSL, PQS, and PYO. A decrease in C4-HSL by 50% to 170.6 ± 11.8 ng/mL and an increase 3-o-C12-HSL by 30% up to 784.4 ± 0.6 ng/mL were detected at the stage of the coverage of the hyphae with bacteria. Using scanning electron microscopy, we showed the morphological stages of the P. aeruginosa biofilm, such as cell aggregates, maturated biofilm, and cell dispersion. qPCR quantification of the genome equivalents of both microorganisms suggested that they exhibited an interplay strategy rather than antagonism. This is the first study demonstrating the quantitative growth-dependent appearance of QS molecule secretion in a monoculture of P. aeruginosa and a co-culture with A. fumigatus.

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Co-Operative Biofilm Interactions between Aspergillus fumigatus and Pseudomonas aeruginosa through Secreted Galactosaminogalactan Exopolysaccharide

Cited by 10 publications

References 72 publications

Convergent evolution in toxin detection and resistance provides evidence for conserved bacterial-fungal interactions

Convergent evolution in toxin detection and resistance provides evidence for conserved bacterial-fungal interactions

Autoaggregation inStreptococcus intermediusis driven by the Pel polysaccharide

The Deciphering of Growth-Dependent Strategies for Quorum-Sensing Networks in Pseudomonas aeruginosa

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