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Expansion of commensal fungus Wallemia mellicola in the gastrointestinal mycobiota enhances the severity of allergic airway disease in mice.

ABSTRACT: The gastrointestinal microbiota influences immune function throughout the body. The gut-lung axis refers to the concept that alterations of gut commensal microorganisms can have a distant effect on immune function in the lung. Overgrowth of intestinal Candida albicans has been previously observed to exacerbate allergic airways disease in mice, but whether subtler changes in intestinal fungal microbiota can affect allergic airways disease is less clear. In this study we have investigated the effects of the population expansion of commensal fungus Wallemia mellicola without overgrowth of the total fungal community. Wallemia spp. are commonly found as a minor component of the commensal gastrointestinal mycobiota in both humans and mice. Mice with an unaltered gut microbiota community resist population expansion when gavaged with W. mellicola; however, transient antibiotic depletion of gut microbiota creates a window of opportunity for expansion of W. mellicola following delivery of live spores to the gastrointestinal tract. This phenomenon is not universal as other commensal fungi (Aspergillus amstelodami, Epicoccum nigrum) do not expand when delivered to mice with antibiotic-depleted microbiota. Mice with Wallemia-expanded gut mycobiota experienced altered pulmonary immune responses to inhaled aeroallergens. Specifically, after induction of allergic airways disease with intratracheal house dust mite (HDM) antigen, mice demonstrated enhanced eosinophilic airway infiltration, airway hyperresponsiveness (AHR) to methacholine challenge, goblet cell hyperplasia, elevated bronchoalveolar lavage IL-5, and enhanced serum HDM IgG1. This phenomenon occurred with no detectable Wallemia in the lung. Targeted amplicon sequencing analysis of the gastrointestinal mycobiota revealed that expansion of W. mellicola in the gut was associated with additional alterations of bacterial and fungal commensal communities. We therefore colonized fungus-free Altered Schaedler Flora (ASF) mice with W. mellicola. ASF mice colonized with W. mellicola experienced enhanced severity of allergic airways disease compared to fungus-free control ASF mice without changes in bacterial community composition.

SUBMITTER: Skalski JH

PROVIDER: S-EPMC6147580 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Expansion of commensal fungus Wallemia mellicola in the gastrointestinal mycobiota enhances the severity of allergic airway disease in mice.

Skalski Joseph H JH Limon Jose J JJ Sharma Purnima P Gargus Matthew D MD Nguyen Christopher C Tang Jie J Coelho Ana Lucia AL Hogaboam Cory M CM Crother Timothy R TR Underhill David M DM

PLoS pathogens 20180920 9

The gastrointestinal microbiota influences immune function throughout the body. The gut-lung axis refers to the concept that alterations of gut commensal microorganisms can have a distant effect on immune function in the lung. Overgrowth of intestinal Candida albicans has been previously observed to exacerbate allergic airways disease in mice, but whether subtler changes in intestinal fungal microbiota can affect allergic airways disease is less clear. In this study we have investigated the effe ...[more]

PMID: 30235351

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Project description:On volcanic islands, the release of animals from predators and competitors can lead to increased body size and population density as well as the expanded habitat use of introduced animals relative to their mainland counterparts. Such alterations might facilitate the spread of diseases on islands when these exotic animals also carry pathogenic agents; however, this has rarely been investigated. The commensal Asian house rat (Rattus tanezumi) is confined to human residential surroundings in mainland Taiwan but can be observed in the forests of nearby Orchid Island, which is a tropical volcanic island. Orchid Island is also a hot spot for scrub typhus, a lethal febrile disease transmitted by larval trombiculid mites (chiggers) that are infected primarily with the rickettsia Orientia tsutsugamushi (OT). We predicted an increase in chigger abundance when rodents (the primary host of chiggers) invade forests from human settlements since soils are largely absent in the latter habitat but necessary for the survival of nymphal and adult mites. A trimonthly rodent survey at 10 sites in three habitats (human residential, grassland, and forest) found only R. tanezumi and showed more R. tanezumi and chiggers in forests than in human residential sites. There was a positive association between rodent and chigger abundance, as well as between rodent body weight and chigger load. Lastly, >95% of chiggers were Leptotrombidium deliense and their OT infection rates were similar among all habitats. Our study demonstrated potentially elevated risks of scrub typhus when this commensal rat species is allowed to invade natural habitats on islands. Additionally, while the success of invasive species can be ascribed to their parasites being left behind, island invaders might instead obtain more parasites if the parasite requires only a single host (e.g., trombiculid mite), is a host generalist (e.g., L. deliense), and is transferred from unsuitable to suitable habitats (i.e., human settlements on the mainland to forests on an island).

Project description:BACKGROUND: The basidomycete Wallemia ichthyophaga from the phylogenetically distinct class Wallemiomycetes is the most halophilic fungus known to date. It requires at least 10% NaCl and thrives in saturated salt solution. To investigate the genomic basis of this exceptional phenotype, we obtained a de-novo genome sequence of the species type-strain and analysed its transcriptomic response to conditions close to the limits of its lower and upper salinity range. RESULTS: The unusually compact genome is 9.6 Mb large and contains 1.67% repetitive sequences. Only 4884 predicted protein coding genes cover almost three quarters of the sequence. Of 639 differentially expressed genes, two thirds are more expressed at lower salinity. Phylogenomic analysis based on the largest dataset used to date (whole proteomes) positions Wallemiomycetes as a 250-million-year-old sister group of Agaricomycotina. Contrary to the closely related species Wallemia sebi, W. ichthyophaga appears to have lost the ability for sexual reproduction. Several protein families are significantly expanded or contracted in the genome. Among these, there are the P-type ATPase cation transporters, but not the sodium/ hydrogen exchanger family. Transcription of all but three cation transporters is not salt dependent. The analysis also reveals a significant enrichment in hydrophobins, which are cell-wall proteins with multiple cellular functions. Half of these are differentially expressed, and most contain an unusually large number of acidic amino acids. This discovery is of particular interest due to the numerous applications of hydrophobines from other fungi in industry, pharmaceutics and medicine. CONCLUSIONS: W. ichthyophaga is an extremophilic specialist that shows only low levels of adaptability and genetic recombination. This is reflected in the characteristics of its genome and its transcriptomic response to salt. No unusual traits were observed in common salt-tolerance mechanisms, such as transport of inorganic ions or synthesis of compatible solutes. Instead, various data indicate a role of the cell wall of W. ichthyophaga in its response to salt. Availability of the genomic sequence is expected to facilitate further research into this unique species, and shed more light on adaptations that allow it to thrive in conditions lethal to most other eukaryotes.

Dataset Information

Expansion of commensal fungus Wallemia mellicola in the gastrointestinal mycobiota enhances the severity of allergic airway disease in mice.

Publications

Expansion of commensal fungus Wallemia mellicola in the gastrointestinal mycobiota enhances the severity of allergic airway disease in mice.

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