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Review Article Mycobiome in the Gut: a Multiperspective Review

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Review Article Mycobiome in the Gut: a Multiperspective Review Hindawi Mediators of Inflammation Volume 2020, Article ID 9560684, 16 pages https://doi.org/10.1155/2020/9560684 Review Article Mycobiome in the Gut: A Multiperspective Review Voon Kin Chin ,1 Voon Chen Yong,1 Pei Pei Chong,1 Syafinaz Amin Nordin ,2 Rusliza Basir ,3 and Maha Abdullah 4 1School of Biosciences, Faculty of Health and Medical Sciences, Taylor’s University Lakeside Campus, 47500 Subang Jaya, Malaysia 2Department of Medical Microbiology and Parasitology, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia 3Department of Human Anatomy, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia 4Department of Pathology, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia Correspondence should be addressed to Maha Abdullah; [email protected] Received 6 September 2019; Revised 23 February 2020; Accepted 17 March 2020; Published 4 April 2020 Academic Editor: Elisabetta Buommino Copyright © 2020 Voon Kin Chin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Human gut is home to a diverse and complex microbial ecosystem encompassing bacteria, viruses, parasites, fungi, and other microorganisms that have an undisputable role in maintaining good health for the host. Studies on the interplay between microbiota in the gut and various human diseases remain the key focus among many researchers. Nevertheless, advances in sequencing technologies and computational biology have helped us to identify a diversity of fungal community that reside in the gut known as the mycobiome. Although studies on gut mycobiome are still in its infancy, numerous sources have reported its potential role in host homeostasis and disease development. Nonetheless, the actual mechanism of its involvement remains largely unknown and underexplored. Thus, in this review, we attempt to discuss the recent advances in gut mycobiome research from multiple perspectives. This includes understanding the composition of fungal communities in the gut and the involvement of gut mycobiome in host immunity and gut-brain axis. Further, we also discuss on multibiome interactions in the gut with emphasis on fungi-bacteria interaction and the influence of diet in shaping gut mycobiome composition. This review also highlights the relation between fungal metabolites and gut mycobiota in human homeostasis and the role of gut mycobiome in various human diseases. This multiperspective review on gut mycobiome could perhaps shed new light for future studies in the mycobiome research area. 1. Introduction tion nowadays. Studies on “mycobiome,” a term used to describe the fungal community of the microbiome, have Human gut is a complex ecosystem inhabited by a myriad of escalated despite still being in its infancy stage as it may be microorganisms including bacteria, fungi, archae, and significant in the context of human health and diseases [4]. viruses [1]. Thus far, studies on gut bacteria or gut “micro- The studies on human gut mycobiome have received little biome” have received the most attention due to the abun- attention for the past decades because fungal presence is dance of bacterial flora present in the gut. For example, relatively insignificant in the gut compared to the bacterial large-scale projects including Metagenomics of the Human communities. In addition to that, fungi have been tradition- Intestinal Tract (MetaHIT) and National Institutes of Health ally studied by culture-dependent methods [5, 6], which (NIH) Human Microbiome Project (HMP) were among the limits the in-depth understanding of the fungal microbiota. projects that were initiated to study the composition of bac- Nonetheless, recent advances in deep-sequencing technologies terial flora and their impacts on human health [1, 2]. Never- and bioinformatics analysis have shed light on the complexity theless, the shift in focus towards the “rare biosphere” [3] in of the fungal communities that reside on both mucosal and the gut, particularly on fungi, has gathered increasing trac- luminal surfaces in the gut and further highlighted our current 2 Mediators of Inflammation understanding on this poorly understood compartment that by Palmer et al. demonstrated that variable levels of fungi reside in the gut. Increasing evidences have demonstrated the were detected from the stool samples of healthy full-term undisputable role of fungal components in driving the infants after birth and also at defined intervals throughout pathogenesis of various gut-associated and metabolic diseases the first year of life using microarray and PCR analysis. Also, [7–9].Inadditiontothat,specific fungi possess the ability to the authors reported the absence of fungal species from the modulate host immune response and could be a risk factor initial stool sample in one of the healthy infants, where the for immunological disorders seen in genetically susceptible mother of the infant showed detectable fungal levels in the individuals [10]. More profoundly, gut mycobiome could be vagina, raising the possibility that vertical transmission (vag- the reservoir for opportunistic pathogens in immunocompro- inal microbiota) has minimal impact on shaping the fungal mised hosts [11–13]. These clearly indicate that gut mycobiome colonization in the infant [25]. Bliss et al. had demonstrated is crucial in host homeostasis and disease development. Thus, in vertical and horizontal transmission of C. albicans from this review, we seek to summarize the role of gut mycobiota mother to infant through DNA fingerprinting techniques from multiple perspectives and to highlight the latest research [26]. On the other hand, diet could affect the composition on gut mycobiome on disease development, in order to provide of the infant’s mycobiota as well. For instance, Candida spe- new insights and productive direction for future studies in this cies have been identified in breast-feeding women with newly emerged research area. symptoms of mammary candidiasis [27]. A study by LaTuga et al. identified several fungal species in extremely low birth 2. Fungal Communities in Gut weight infants in their first postnatal month. These fungal species include S. cerevisiae followed by Candida spp., Cla- In general, fungi constitute a minor component of the entire dosporium spp., and Cryptococcus spp. [28]. Another study gut microbiome. Recent shotgun metagenomics sequencing also reported a lack of fungal diversity and richness in eleven analysis has revealed that fungi consist of nearly 0.1% of the infants using combined NGS technology (targeted on fungal total microbes in the gut [1, 14]. On the other hand, despite ITS2 amplicons) with qPCR analysis. The most predominant numerous published data on gut mycobiome, the fungal fungi identified in this study were C. albicans, C. parapsilosis, communities in the gut remain poorly understood. There is and Leptosphaerulina, with C. albicans being detected in all no consensus in defining a healthy gut mycobiome due to a infants. The authors speculate that the relatively low diversity variety of factors such as low abundance and diversity of of fungi in infants as compared to adults could be due to age fungi in the gut, temporal instability of gut mycobiota factor where these infants may not yet been fully colonized by throughout the development periods, and high intervolun- a myriad of different fungal species. Further, the authors teer and intravolunteer variability of the gut mycobiome highlighted the challenge of detecting low abundance fungi, [15, 16]. Nevertheless, the fungal communities in the gut have where low levels of Candida parapsilosis and Candida krusei been highlighted in many studies [8, 16, 17]. In terms of phyla, sequences were detected in a few samples; however, their thus far, most studies have suggested that Ascomycota is the presence was only detected in one sample via species- most predominant phylum found in the gut, followed by Zygo- specific qPCR [29]. On the other hand, a study by Strati mycota and Basidiomycota phyla [15, 18–20]. Meanwhile, in et al. demonstrated the influence of age and gender on the the context of genus, a recent review by Hallen-Adams and gut fungal composition. In this study, the authors reported coworkers had identified potential fungal species that inhabit that infants and children have higher fungal richness than the intestinal niche, belonging to the genera Candida, Crypto- in adults via culture-independent analysis. Meanwhile, the coccus, Malassezia, Aspergillus, Saccharomyces, Galactomyces, diversity and fungal richness was also higher in female than Trichosporon,andCladosporium [21].Recently,throughthe male healthy subjects [30]. Together, the diversity of fungal Human Microbiome Project (HMP), Nash and coworkers composition, the timing and the mechanism involved in (2017) sequenced 317 stool samples in a healthy cohort via assembling fungi into gut microbiome, the influence of Internal Transcribed Spacer 2 (ITS2) region and 18S rRNA genetic and environmental factors in shaping the infant gene. The authors reported that gut mycobiota is mainly dom- mycobiota, and the contribution of fungi to the microbiome inated by Malassezia, Candida,andSaccharomyces,withS. cer- phenotype remain to be explored further. evisiae, M. restricta,andC. albicans identified in 96.8%, 88.3%, and 80.8% of the samples,
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