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Fungal Interactions with the Human Host: Exploring the Spectrum of Symbiosis Hall, Rebecca; Noverr, Mairi University of Birmingham Fungal Interactions with the Human Host: Exploring the Spectrum of Symbiosis Hall, Rebecca; Noverr, Mairi DOI: 10.1016/j.mib.2017.10.020 License: Creative Commons: Attribution (CC BY) Document Version Publisher's PDF, also known as Version of record Citation for published version (Harvard): Hall, R & Noverr, M 2017, 'Fungal Interactions with the Human Host: Exploring the Spectrum of Symbiosis', Current Opinion in Microbiology, vol. 40, pp. 58-64. https://doi.org/10.1016/j.mib.2017.10.020 Link to publication on Research at Birmingham portal General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 27. Sep. 2021 Available online at www.sciencedirect.com ScienceDirect Fungal interactions with the human host: exploring the spectrum of symbiosis 1,3 2,3 Rebecca A Hall and Mairi C Noverr Fungi are ubiquitous transient or persistent human colonisers, response framework (DRF), which defines microbial vir- and form the mycobiome with shifts in niche specific ulence as a function of host damage [4]. Within this mycobiomes (dysbiosis) being associated with various framework, host damage (and therefore disease) can occur diseases. These complex interactions of fungal species with at either end of the host immune response spectrum (i.e. the human host can be viewed as a spectrum of symbiotic weakened or hyperactive immune defences). Along this relationships (i.e. commensal, parasitic, mutualistic, spectrum there is a continuum between pathogen-medi- amensalistic). The host relevant outcome of the relationship is ated and host-mediated damage, which results in disease the damage to benefit ratio, elegantly described in the damage only when damage impairs the normal function of the response framework. This review focuses on Candida albicans, host. which is the most well studied human fungal symbiont clinically and experimentally, its transition from commensalism Host damage also varies as a function of time, with several to parasitism within the human host, and the factors that possible outcomes of host–pathogen interactions. For influence this relationship. example, as the amount of damage increases over time and surpasses a threshold, disease ensues [4]. Fungal pathogens that are able to exist within the host for Addresses extended periods of time with limited damage lead to 1 Institute of Microbiology and Infection, School of Biosciences, other outcomes, including latency (Cryptococcus) or com- University of Birmingham, Birmingham, UK 2 mensalism. In addition, many fungal pathogens cause Department of Prosthodontics, Louisiana State University School of Dentistry, New Orleans, LA, USA chronic (long-term) infections, and therefore could also be classified as symbionts, albeit with different host/ Corresponding author: Hall, Rebecca A ([email protected]) 3 microbe damage to benefit ratios. The most well studied Authors contributed equally to this manuscript. fungal commensal is Candida albicans, which colonises the oral, genital and gastrointestinal tracts, but can cause host Current Opinion in Microbiology 2017, 40:58–64 damage and disease in the context of weakened or uncon- This review comes from a themed issue on Host-microbe interac- trolled immune responses. An environmental reservoir tions: fungi of C. albicans has not yet been identified. Therefore, Edited by Gordon Brown and Robin May C. albicans is considered an obligate commensal fungus. For a complete overview see the Issue and the Editorial This and its ability to fit within all six classes of the DRF Available online 11th November 2017 [5 ] have made C. albicans the model fungus for studying http://dx.doi.org/10.1016/j.mib.2017.10.020 the transition from commensal to pathogen and will be the main focus of this review. 1369-5274/ã 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons. org/licenses/by/4.0/). Symbiosis within the human ecosystem Symbiosis is a type of long-term close biological relation- ship between two or more species. These relationships Introduction can be mutualistic (all organisms benefit), commensalistic Fungi are ubiquitous within the environment. However, (one organism benefits without affecting the other), par- only a few species are routinely found associated with asitic (one organism benefits at the expense of the other), humans and are capable of causing disease. A handful of or amensalistic (one organism is inhibited or obliterated, these fungi are considered true pathogens, causing dis- while the other is unaffected). For example, most host– ease in healthy individuals (Histoplasma and Paracocci- pathogen interactions are parasitic with the pathogen dioides), while the majority of fungi are often classified as causing damage to the host. However, as mentioned opportunistic pathogens (i.e. Candida and Cryptococcus), above, periods of latency during an infection may be causing disease primarily in immunosuppressed individ- classed as a commensal relationship as damage to the uals [1]. However, it is apparent that some opportunistic host is minimal during this period. Interactions between fungal pathogens also cause disease in otherwise healthy members of the microbiome may be described as amen- individuals (i.e. Candida vaginitis or Cryptococcus gattii salistic as the presence of some species prevent the outbreaks) [2,3]. To understand and categorize the com- growth of others through nutrient depletion and the plexity of these different interactions between host and secretion of chemical mediators. This is an important pathogen, Casadevall and Pirofski proposed the damage factor as dysbiosis of the microbiome has been identified Current Opinion in Microbiology 2017, 40:58–64 www.sciencedirect.com Fungal interactions with the human host Hall and Noverr 59 Figure 1 Mutualism Tolerance Commensalism Inflammation Parasitism Host Damage Colonization Resistance Homeostasis Trauma, dysbiosis, virulence traits Pathogen Antagonism Epithelium L.P. Candida levels below threshold Candida levels below threshold Candida levels = low PRR signalling = low PRR signalling reach threshold for PRR signalling Inflammatory Signals PMN T cell PRR Yeast Hyphae Current Opinion in Microbiology Transition of C. albicans from commensal to parasite. During commensal growth C. albicans grows predominately as yeast and is tolerated by the host, and does not activate innate immune responses. Periods of dysbiosis and immune suppression permit C. albicans to proliferate, induce hyphal formation, and activate innate immune responses. At the vaginal mucosal, epithelial cells become sensitised resulting in hyperactivation of innate immune responses and neutrophil influx. This non-protective hyperactivation of neutrophils results in damage to the vaginal mucosa and symptomatic vaginal candidiasis. as a major contributor for several fungal infections (i.e. vagina [9,10], lung [11,12], and skin [13 ,14]. Over 75 gen- vulvovaginal candidiasis, atopic dermatitis). Although era of fungi have been identified in the oral cavity alone, common for bacterial species, the idea of mutualistic which can seed the respiratory or GI tract mycobiome. relationships between fungi and the human host is a The most common fungal species associated with the GI new concept as the potential benefit to the host of tract are Candida, Saccharamyces and Cladosporium, harbouring fungi is still unknown (Figure 1). although DNA from more than 50 genera of fungi has been detected. Stability and fluctuations in population Niche-specific fungal symbionts dynamics of the GI mycobiome is highly dependent on Fungal symbionts vary in route of acquisition, niche/s diet and host immune status. For example, Saccharomyces inhabited, and ultimately, the type of symbiotic relation- cerevisiae is commonly acquired from dietary sources and ship formed. Some species are acquired at birth by direct is considered to be a harmless or transient commensal. transmission, leading to colonization of the skin and However, inflammatory bowel diseases [15] and some mucosal surfaces, while many fungal pathogens are ubiq- autoimmune diseases [16,17] are associated with uitous within the environment, leading to constant expo- increased levels of
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