Interactions of  Aspergillus fumigatus  and  Stenotrophomonas maltophilia  in an  in vitro  Mixed Biofilm Model: Does the Strain Matter?

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Abstract

Introduction: Aspergillus fumigatus (Af) and Stenotrophomonas maltophilia (Sm) are pathogenic microorganisms, which coexist in the respiratory tract of cystic fibrosis (CF) patients. We recently developed an in vitro model of mixed biofilm associating Af ATCC 13073-GFP (Af13073) and Sm ATCC 13637 (Sm13637) and described an antibiosis effect. The present study aim was to assess the antibiosis of Sm on Af using different strains and to analyze the potential synergistic virulence of these strains in an in vivo Galleria mellonella model.

Methods: The effect of Sm13637 was evaluated on eight Af strains and the effect of nine Sm strains was evaluated on Af13073. The strains originated from clinical cases (human and animal) and from environment. Fungal and bacterial inocula were simultaneously inoculated to initiate mixed biofilm formation. Fungal growth inhibition was analyzed by qPCR and CLSM and the fungal cell wall modifications by TEM analysis. The virulence of different Sm strains was assessed in association with Af in G. mellonella larvae.

Results: All strains of Af and Sm were able to produce single and mixed biofilms. The antibiosis effect of Sm13637 was similar whatever the Af strain tested. On the other hand, the antibiosis effect of Sm strains was bacterial-fitness and strain dependent. One strain (1/9) originated from animal clinical case was never able to induce an antibiosis, even with high bacterial concentration. In the G. mellonella model, co-inoculation with Sm13637 and Af13073 showed synergism since the mortality was 50%, i.e., more than the summed virulence of both.

Conclusion: Human clinical strains of Sm yielded in higher antibiosis effect on Af and in a thinner mixed biofilm, probably due to an adaptive effect of these strains. Further research covering Af increased wall thickness in the presence of Sm strains, and its correlation with modified antifungal susceptibility is encouraged in patients with chronic respiratory infections by these 2 microorganisms.

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Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists.

P. Frey-Klett, P Burlinson, A Deveau … (2011)

Bacteria and fungi can form a range of physical associations that depend on various modes of molecular communication for their development and functioning. These bacterial-fungal interactions often result in changes to the pathogenicity or the nutritional influence of one or both partners toward plants or animals (including humans). They can also result in unique contributions to biogeochemical cycles and biotechnological processes. Thus, the interactions between bacteria and fungi are of central importance to numerous biological questions in agriculture, forestry, environmental science, food production, and medicine. Here we present a structured review of bacterial-fungal interactions, illustrated by examples sourced from many diverse scientific fields. We consider the general and specific properties of these interactions, providing a global perspective across this emerging multidisciplinary research area. We show that in many cases, parallels can be drawn between different scenarios in which bacterial-fungal interactions are important. Finally, we discuss how new avenues of investigation may enhance our ability to combat, manipulate, or exploit bacterial-fungal complexes for the economic and practical benefit of humanity as well as reshape our current understanding of bacterial and fungal ecology.

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Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation.

James Brian Jones, Ranjith Rajendran, Gordon Ramage … (2010)

Aspergillus fumigatus is often isolated from the lungs of cystic fibrosis (CF) patients, but unlike in severely immunocompromised individuals, the mortality rates are low. This suggests that competition from bacteria within the CF lung may be inhibitory. The purpose of this study was to investigate how Pseudomonas aeruginosa influences A. fumigatus conidial germination and biofilm formation. Aspergillus fumigatus biofilm formation was inhibited by direct contact with P. aeruginosa, but had no effect on preformed biofilm. A secreted heat-stable soluble factor was also shown to exhibit biofilm inhibition. Coculture of P. aeruginosa quorum-sensing mutants (PAO1:ΔLasI, PAO1:ΔLasR) did not significantly inhibit A. fumigatus biofilms (52.6-58.8%) to the same extent as that of the PA01 wild type (22.9-30.1%), both by direct and by indirect interaction (P<0.001). Planktonic and sessile inhibition assays with a series of short carbon chain molecules (decanol, decanoic acid and dodecanol) demonstrated that these molecules could both inhibit and disrupt biofilms in a concentration-dependent manner. Overall, this suggests that small diffusible and heat-stable molecules may be responsible for the competitive inhibition of filamentous fungal growth in polymicrobial environments such as the CF lung. © 2010 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.

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Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action.

Xiangcheng Zhu, Philip D. Harris, Mu-xing Li … (2006)

A screen for antifungal compounds from Lysobacter enzymogenes strain C3, a bacterial biological control agent of fungal diseases, has previously led to the isolation of heat-stable antifungal factor (HSAF). HSAF exhibits inhibitory activities against a wide range of fungal species and shows a novel mode of antifungal action by disrupting the biosynthesis of a distinct group of sphingolipids. We have now determined the chemical structure of HSAF, which is identical to that of dihydromaltophilin, an antifungal metabolite with a unique macrocyclic lactam system containing a tetramic acid moiety and a 5,5,6-tricyclic skeleton. We have also identified the genetic locus responsible for the biosynthesis of HSAF in strain C3. DNA sequencing of this locus revealed genes for a hybrid polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS), a sterol desaturase, a ferredoxin reductase, and an arginase. The disruption of the PKS-NRPS gene generated C3 mutants that lost the ability to produce HSAF and to inhibit fungal growth, demonstrating a hybrid PKS-NRPS that catalyzed the biosynthesis of the unique macrolactam system that is found in many biologically active natural products isolated from marine organisms. In addition, we have generated mutants with disrupted sterol desaturase, ferredoxin reductase, and arginase and examined the metabolites produced in these mutants. The work represents the first study of the genetic basis for the biosynthesis of the tetramic acid-containing macrolactams. The elucidation of the chemical structure of HSAF and the identification of the genetic locus for its biosynthesis establish the foundation for future exploitation of this group of compounds as new fungicides or antifungal drugs.

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Author and article information

Contributors

Elise Melloul: URI : http://loop.frontiersin.org/people/604334/overview

Paul-Louis Woerther: URI : http://loop.frontiersin.org/people/610074/overview

Veronica Risco: URI : http://loop.frontiersin.org/people/470158/overview

Jacques Guillot: URI : http://loop.frontiersin.org/people/577869/overview

Eric Dannaoui: URI : http://loop.frontiersin.org/people/350997/overview

Jean-Winoc Decousser: URI : http://loop.frontiersin.org/people/515357/overview

Françoise Botterel: URI : http://loop.frontiersin.org/people/390607/overview

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 27 November 2018

Publication date Collection: 2018

Volume: 9

Electronic Location Identifier: 2850

Affiliations

[1] ¹EA 7380 Dynamyc, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est Créteil , Créteil, France

[2] ²Service de Parasitologie-Mycologie , Limoges, France

[3] ³Unité de Bactériologie-Hygiéne, Département de Microbiologie, Assistance Publique – Hôpitaux de Paris, Hôpital Henri Mondor , Créteil, France

[4] ⁴Unité de Parasitologie-Mycologie, Ecole Nationale Vétérinaire d’Alfort , Maisons-Alfort, France

[5] ⁵Unité de Parasitologie-Mycologie, Service de Microbiologie, Hôpital Européen Georges Pompidou, Assistance Publique – Hôpitaux de Paris, Faculté de Médecine, Université Paris-Descartes , Paris, France

[6] ⁶Unité de Parasitologie-Mycologie, Département de Microbiologie, Groupe Hospitalier Henri Mondor – Albert Chenevier, Assistance Publique – Hôpitaux de Paris, Université Paris-Est Créteil , Créteil, France

Author notes

Edited by: Hector Mora Montes, Universidad de Guanajuato, Mexico

Reviewed by: Dinesh Sriramulu, Shres Consultancy (Life Sciences), Chennai, India; Sonia Rozental, Universidade Federal do Rio de Janeiro, Brazil

*Correspondence: Françoise Botterel, francoise.botterel@ 123456aphp.fr

This article was submitted to Fungi and Their Interactions, a section of the journal Frontiers in Microbiology

Article

DOI: 10.3389/fmicb.2018.02850

PMC ID: 6277776

SO-VID: 7ee9861f-9db0-4cb3-aa4c-0429417fb4b5

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This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 27 August 2018

Date accepted : 06 November 2018

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Figures: 7, Tables: 2, Equations: 0, References: 43, Pages: 13, Words: 0

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Interactions of Aspergillus fumigatus and Stenotrophomonas maltophilia in an in vitro Mixed Biofilm Model: Does the Strain Matter?

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Most cited references 39

Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists.

Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation.

Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action.

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