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Fungi in the Healthy Human Gastrointestinal Tract Heather E View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DigitalCommons@University of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in Food Science and Food Science and Technology Department Technology 10-2016 Fungi in the healthy human gastrointestinal tract Heather E. Hallen-Adams University of Nebraska-Lincoln, [email protected] Mallory J. Suhr University of Nebraska-Lincoln, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/foodsciefacpub Part of the Environmental Microbiology and Microbial Ecology Commons, and the Food Microbiology Commons Hallen-Adams, Heather E. and Suhr, Mallory J., "Fungi in the healthy human gastrointestinal tract" (2016). Faculty Publications in Food Science and Technology. 185. http://digitalcommons.unl.edu/foodsciefacpub/185 This Article is brought to you for free and open access by the Food Science and Technology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in Food Science and Technology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Virulence, 2016. doi:10.1080/21505594.2016.1247140 Copyright © 2016 Taylor & Francis. Used by permission. Submitted 20 July 2016; revised 7 September 2016; accepted 8 September 2016.; published online 13 October 2016. digitalcommons.unl.edu Fungi in the healthy human gastrointestinal tract Heather E. Hallen-Adams and Mallory J. Suhr Department of Food Science and Technology, University of Nebraska, Lincoln, NE, USA Corresponding author — Heather E. Hallen-Adams, Food Science and Technology, University of Nebraska-Lincoln, 1901 N. 21st St., Lincoln, NE 68588, USA. [email protected] Abstract Many species of fungi have been detected in the healthy human gut; however, nearly half of all taxa reported have only been found in one sample or one study. Fungi capable of growing in and colonizing the gut are limited to a small number of species, mostly Candida yeasts and yeasts in the family Dipodascaceae (Galactomyces, Geotrichum, Saprochaete). Malassezia and the filamentous fungusCladosporium are potential colonizers; more work is needed to clarify their role. Other commonly-detected fungi come from the diet or environment but ei- ther cannot or do not colonize (Penicillium and Debaryomyces species, which are common on fermented foods but cannot grow at human body temperature), while still others have dietary or environmental sources (Saccharomyces cerevisiae, a fermentation agent and sometime probiotic; Aspergillus species, ubiquitous molds) yet are likely to impact gut ecology. The gut mycobiome appears less stable than the bac- terial microbiome, and is likely subject to environmental factors. Keywords: Candida, Cladosporium, dietary fungi; Dipodascaceae, gut fungal ecology, gut mycobiome, gut mycobiota, Malassezia, yeasts Introduction decrease in cost and rise in capacity of next-genera- tion sequencing technologies, microbiome projects are The gastrointestinal tract of an animal provides an now more feasible to the single investigator. The con- attractive niche for organisms which have evolved to tribution of the microbiome to overall well-being is now withstand its unique challenges. Nutrients ingested by widely accepted and studied. the host are in steady supply and obviate the need to The healthy human gut microbiome contains mem- seek food. In the intestines, the outer mucus layer al- bers of all domains of life, with Eukarya primarily lows colonization and provides a nutrient rich hab- represented by the fungi and, in some populations, itat, while the dense inner layer segregates coloniz- protists, notably Blastocystis.8,9 The fungal compo- ing microbes from the dense concentration of immune nent—the mycobiome—has received little attention cells in the intestinal epithelium.1 To take advantage compared with bacteria, but steady work by a num- of these resources, organisms must be equipped to ber of researchers has produced a mature discipline, tolerate gut conditions: absence of oxygen; physiolog- as evidenced by this special issue. Several important ical temperatures (in mammals); peristaltic contrac- reviews have been published in this decade. Specif- tions and consequent movement of GI contents; vari- ically, whole-body perspectives of the human myco- able pH, from the highly acidic stomach to the alkaline biome are provided by Cui and colleagues, 10 Huffna- intestinal mucosa. gle and Noverr,11 Seed,12 and Underhill and Iliev,13 For most years since the development and accep- while the gut mycobiota is reviewed by Ianiro and col- tance of the germ theory, studies of human-associated leagues,14 Kirschner and colleagues,15 and Suhr and microbes focused on pathogens.2 While the existence Hallen-Adams.16 The role of the gut mycobiota in dis- of commensal and mutualistic relationships between ease is reviewed by Moyes and Naglik,17 Wang and col- humans and their gut microbiota has been known for leagues,18 Gouba and Drancourt,19 Mukherjee and col- well over a century (see, e.g., refs3,4), culture-based leagues,20 and Richard and colleagues.21 In this paper, methods precluded study of any but the most tracta- we focus on the gut mycobiome of healthy humans, ble organisms. The development of culture-indepen- with a particular emphasis on the relatively few fungi dent PCR-based methods revolutionized the study of that are widely distributed in human gut samples. We the whole, healthy, human microbiome.2 At the turn of will also discuss the contributions of diet and the en- the century, several large scale international healthy vironment to gut fungal composition, and the stability human microbiome projects were initiated.5-7 With the of the gut mycobiome over time. 1 2 Hallen-Adams & Suhr in Virulence (2016) Many fungi have been reported from the human gut, Categories of gut fungi but few are common. From 36 studies spanning 1917 to 2015 and using a broad array of culture-based and Fungi detected in the human gut can be split into res- nonculture- based methods, 267 distinct, valid spe- ident and non-resident. As a minimum requirement, cies were detailed.16 (Taxa identified only to genus, or a resident (or autochthonous) fungus must be able to as “undescribed,” in the studies were not included in grow at 37_C to colonize the gut. For a few species of this tally.) Two hundred species, or nearly 75%, were the wide and diverse yeast genus Candida, the mam- only reported in one study. A further 37 species were malian digestive tract can be considered the primary reported in 2 studies, and only 15 were reported in 5 niche. Species including Candida albicans, C. tropica- or more studies. When studies involve multiple sam- lis, C. parapsilosis, and C. glabrata may all be found ples a similar trend is observed: many species may be as natural, asymptomatic components of the human observed, but a majority are only detected in a single microbiome, and published estimates of C. albicans sample. The studies from our own lab identified 97 dis- carriage in healthy individuals range from 30–60%.24 tinct fungal taxa in 85 samples from 60 subjects.22,23 Furthermore, many of these species do not appear Forty-eight taxa were limited to a single sample, while to have a niche apart from living mammals; absent 14 occurred in 10 samples or more. The most com- a source of contamination, they will not be found in monly reported genera and species of gut fungi are significant concentrations in the air, or in soil, or in given in Table 1. Most rarely detected taxa are unlikely food.25,26 Malassezia is another genus of yeasts whose to play a role in gut ecology or host health, for reasons primary niche is the mammalian microbiome; in fact, discussed below. Malassezia species have lost the ability to synthesize their own lipids, so they are dependent on a host for Table 1. Most commonly-detected fungi in gut mycobiome their nutritional needs.27 The known niche for Malas- studies. sezia is skin, where it is the predominant fungal ge- Taxona # studies # samples Referencesd nus detected in 11 of 14 body sites (the exceptions all (%)b (%)c being on the foot; ref.28). Malassezia has also been re- Candida 32 (86%) 68 (80%) ported in significant abundance in fecal samples and C. albicans 26 (70%) 18 (21%) 3, 9, 22, 23, 31-33, 41-44, 46, 54- may play a role in the gut.29,30,23 To determine whether 57, 59, 60-63, 65, 66, 68, 69 any Malassezia is indigenous to the gut would require C. tropicalis 17 (46%) 57 (67%) 3, 22, 23, 29, 30- 33, 42, 44, 51, 54, 55, 60, 61, 62, 68 more invasive sampling techniques than the standard C. parapsilosis 13 (35%) 2 (2%) 9, 22, 30-33, 42, 55, 60, 61, 63, fecal collection, to eliminate the possibility of inocula- 67, 68, 69 tion of the feces by skin flora. C. glabrata 12 (32%) 0 3, 31, 41, 43, 44, 46, 54, 55, 59, 60, 61, 63 Two further groups of fungi reported repeatedly in C. krusei 10 (27%) 0 3, 23, 31-33, 44, 45, 54, 55, 60, 63 gut fungal studies likely do not have the gut as their C. lusitaniae 6 (16%) 0 30, 33, 43, 54, 55, 60 primary niche but may be considered potential colo- Saccharomyces 20 (54%) 5 (6%) S. cerevisiae 20 (54%) 5 (6%) 9, 22, 23, 30, 33, 34, 41-45, 51, nizers: Cladosporium, and yeasts in the Dipodasca- 54, 58, 59, 61-64, 69 ceae (includes Geotrichum/Saprochaete and Galac- Penicillium 14 (38%) 17 (20%) 9, 22, 42, 69d P. aff. commune 10 (27%) 10 (12%) 23, 29, 31, 41, 43, 44, 51, 58, 62, tomyces). Cladosporium, along with Aspergillus and 67 Penicillium (discussed below) is a filamentous fungus, Aspergillus 12 (32%) 20 (24%) 22, 23, 42, 43, 51, 58, 62 or mold; the other fungi commonly detected in the gut A.
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