Digestive tract mycobiota: A source of infection

Digestive tract mycobiota: A source of infection

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General review

Digestive tract mycobiota: A source of infection Le mycobiome digestif comme source d’infection N. Gouba , M. Drancourt ∗ Unité de recherche sur les maladies infectieuses et tropicales émergentes, UMR63, CNRS 7278, IRD 198, Inserm 1095, faculté de médecine, Aix-Marseille université, 27, boulevard Jean-Moulin, 13005 Marseille cedex 5, France Received 29 August 2014; accepted 13 January 2015

Abstract The human mycobiome includes 390 fungal species detected on the skin, in the vagina, in the oral cavity, and in the digestive tract that includes 335 species and 158 genera. Among these, 221 species are found only in the digestive tract, 88 only in the oral cavity, and 26 in both. These species belong to 126 genera of yeast and filamentous fungi, of the Ascomycota, Basidiomycota, and Zygomycota phyla. Forty species were identified only by culture, 188 species by molecular techniques, and 19 species with both techniques. Fungal diversity does not differ significantly according to sex but Basidiobolus ranarum is significantly more prevalent in male individuals and Paecilomyces fumosoroseus in female individuals. Fungal diversity is significantly higher in adults than in infants. Only 42 species are identified in the course of inflammatory bowel disease, with 27 species specific to IBD. Twenty-nine are identified in HBV infected patients including 17 specific species, and 11 in HIV-infected patients with the specific Histoplasma capsulatum. Genotyping proved that the gut mycobiome was a source of fungal infection caused by Candida albicans and Candida glabrata. The authors suggest updating the repertoire of the human digestive tract in healthy individuals and patients. Fungal culturomics must be intensified to complete this repertoire. © 2015 Published by Elsevier Masson SAS. Keywords: Gut; Mycobiome; Yeasts

Résumé Le mycobiome humain comprend 390 espèces fongiques détectées sur la peau, la cavité vaginale, la cavité orale et le tractus digestif qui comporte 335 espèces et 158 genres. Parmi les espèces, 221 sont trouvées uniquement dans le tube digestif, 88 dans la cavité buccale et 26 dans les deux. Ces espèces appartiennent à 126 genres de levures et des champignons filamenteux, des phyla Ascomycota, Basidiomycota et Zygomycota. Quarante espèces ont été trouvées uniquement par culture, 188 espèces par méthodes moléculaires et 19 espèces par les deux approches. La diversité fongique ne varie pas significativement avec le sexe mais Basidiobolus ranarum est significativement plus fréquent chez les hommes, Paecilomyces fumosoroseus chez les femmes ; elle est significativement plus grande chez les adultes que chez les nourrissons. Au cours des entéropathies inflammatoires, on retrouve 42 espèces dont 27 spécifiques de cette pathologie ; 29 chez les patients infectés par le virus de l’hépatite B dont 17 spécifiques ; et 11 chez les patients infectés par le VIH, présentant spécifiquement Histoplasma capsulatum. Le génotypage a démontré que le mycobiome digestif est une source de fungémie causée par Candida albicans et Candida glabrata. Cette revue propose une mise à jour du répertoire des champignons du tractus digestif humain des individus sains ainsi que des patients. La détection des champignons par isolement et culture doit être renforcée pour compléter ce répertoire. © 2015 Publi´e par Elsevier Masson SAS. Mots clés : Intestins ; Mycobiome ; Levures



Corresponding author. E-mail address: [email protected] (M. Drancourt).

http://dx.doi.org/10.1016/j.medmal.2015.01.007 0399-077X/© 2015 Published by Elsevier Masson SAS.

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1. Introduction The human mycobiome includes all fungal species detected in humans, a neglected component of the human microbiota [1]. Over the past 20 years, culture-independent methods such as high-throughput sequencing have provided new data on the mycobiome of the skin, vaginal and oral cavities, and digestive tract in healthy individuals and patients [2–6]. Currently, 390 different fungal species have been detected in the human microbiota belonging to the phyla Ascomycota, Basidiomycota, and Zygomycota [7]. The authors provide an overview of fungal species in the human digestive mycobiome, including the oral and intestinal mycobiome, and the differences between healthy individuals and patients, as well as the digestive mycobiota as a source of systemic infections. They reviewed 75 articles published in English between 1998 and 2014 listed in the PubMed database, using the keywords oral mycobiome, intestinal fungi, gastrointestinal fungi, and fungal infection. 2. Digestive mycobiota study methods The detection of fungal species can be achieved from oral samples, gastric biopsies, colonic biopsies, and stool samples. In various studies, the samples were reported as inoculated on 7 different solid media including Sabouraud, dextrose agar, malt-agar, potato dextrose agar, CZAPEK, Colombia, and glycine-vancomycin-polymyxin B agar, for 2 weeks, with a visual detection of colonies, 2 or 3 times per week (Fig. 1). A mix of broad-spectrum antibiotics including chloramphenicol, gentamycin, streptomycin and cycloheximide was added to limit bacterial growth [8]. The inoculated media were incubated at 25 ◦ C or at room temperature to isolate filamentous fungi for 4 days, and at 35–37 ◦ C for 5 days for yeasts [4,5,9–12]. Species Candida albicans, Candida glabrata, Candida rugosa, Candida parapsilosis, Candida tropicalis, Candida dubliniensis, Candida krusei, and Candida lusitaniae were usually isolated in stools [4,5,7]. The use of mass spectrometry (Matrix-Assisted Laser Desorption Ionization Time-Of-Flight Mass Spectrometry or MALDI-TOF-MS) has revolutionized the identification of fungi, now feasible in a few minutes after a minimal preparation of colonies. MALDI-TOF-MS identification is performed by comparing the profile of peptides with the appropriate database [13]. Fungal colonies are routinely prepared in 15 minutes and placed on a spectrometer plate with appropriate positive and negative controls. The result is obtained immediately. Therefore, a routine MALDI-TOF-MS identification is available in a few minutes compared to several hours for PCR-based identification. MALDI-TOF-MS identification costs less than 1 euro, far less than PCR identification. Interestingly, 29 fungal species cultured from stool and colonic biopsies can be identified by MALDI-TOF-MS with available databases that contain more than 150 fungal species (Table 1). MALDI-TOF-MS technique allows a high-speed identification of cultivated fungi, and should boost the use of routine culture. Indeed, studies using culture are based on the use of a single medium, or on specific media for the isolation

Table 1 Digestive tract fungal species isolated by culture and identified by MALDITOF-MS. Champignons isolés de tractus digestif et identifiables par spectrométrie de masse MALDI-TOF-MS. Species

MALDI TOF-MS identification

Aspergillus flavipes Aspergillus flavus Aspergillus ruber Aspergillus spp. Aspergillus versicolor Basidiobolus ranarum Beauveria bassiana Blastoschizomyces capitatus Candida albicans Candida dubliniensis Candida famata Candida glabrata Candida guilliermondii Candida incospicua Candida kefyr Candida krusei Candida lambica Candida lusitaniae Candida norvogensis Candida parapsilosis Candida sphaerica Candida spp. Candida tropicalis Candida utilis Candida zeynaloides Climacocystis sp. Cryptococcus albidus Cryptococcus luteolus Cryptococcus neoformans Cryptococcus sp. Exophiala dermatidis Fusarium sp. Galactomyces candidum Galactomyces geotrichum Geothricum spp. Geotrichum candida Geotrichum candidum (Goetrichum silvoca) Histoplasma capsulatum Hypocrea lixii Isaria farinosa Malassezia globosa Malassezia pachydermatis Malassezia restricta Mucor spp. Paracoccidioides brasiliensis Penicillium allii Penicillium brevicompactum Penicillium camemberti Penicillium dipodomyicola Penicillium solitum Penicillium spp. Rhodotorula glutinis Rhodotorula rubra Rhodotorula sp. Saccharomyces cerevisiae Saccharomyces sp. Trichosporon asahii Trichosporon beigelii Yarrowia lipolytica (Candida lipolytica)

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Fig. 1. Gut mycobiota culture and identification. Culture et identification des champignons intestinaux.

of yeasts, which limited the detection of other fungal species [4,5,14]. This contrasts with the concept of culturomics recently applied to the study of bacteria of the intestinal microbiota, which is based on the use of several different culture media and incubation conditions to increase the efficiency of detection of organisms by culture, then identified by MALDI-TOF-MS to expand the repertoire of bacterial species and find new species [15,16]. The intestinal mycobiome is also studied by culture independent molecular tools. Indeed, the specific detection and identification of fungi in gut samples were essentially based on culture independent techniques [1]. Culture methods detected 40 fungal species while 188 species were found by molecular techniques, and 19 species were detected by both approaches (Fig. 1). Three hundred and thirtyfive fungal species have been identified in the human digestive tract, including 88 species found only in the oral cavity, 221 species only in the intestine, and 26 species in both microbiota (Fig. 2). The human intestinal mycobiota includes 247 species belonging to 126 genera including phyla Ascomycota (63%), Basidiomycota (32%), Zygomycota (3%), and nonclassified fungi (2%). Penicillium spp., Saccharomyces spp., and Candida glabrata have been identified only in stools,

but not in gastrointestinal tract biopsies [7], while Basidiobolus ranarum, Histoplasma capsulatum, and Paracoccidioides brasiliensis were identified only in gastric and colonic biopsies, but not in stools [17,18]. 3. Oral and intestinal mycobiota Culture-independent methods recently allowed detecting 101 species in the oral cavity in 20 healthy individuals, belonging to 74 cultured fungal genera and 11 non-cultured genera [2,19]. Seven of these genera detected in the oral cavity were also frequently detected in the intestines: Candida spp. (75% of individuals), followed by Cladosporium (65%), Aureobasidium, Saccharomycetales (50%), Aspergillus (35%), Fusarium (30%), and Cryptococcus (20%). Fourteen species were detected in patients with oral thrush, especially in immunocompromised patients [20–22]. Some species were found in the oral cavity and intestines, such as Paracoccidioides brasiliensis, Histoplasma capsulatum, Aspergillus fumigatus, C. Albicans, and S. Cerevisiea. The differences observed between oral and intestinal mycobiota repertoire could be related to the variable sensitivity of fungal species to pH. Some species found only in the oral cavity have a narrow tolerance to pH variations, such

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Fig. 2. Gut and oral mycobiome. Comparaison des mycobiomes oraux et intestinaux.

as Aspergillus fumigatus (6 or 7.3), P. Marneffei (5 and 6), and Fusarium moniliforme (5.5 and 7) [23–25]. These species are probably destroyed by stomach acids. In contrast, some of the species found in the oral cavity and intestines can replicate in a wider pH range (2–8), such as S. Cerevisiae and C. Albicans [26,27]. 4. Diet and intestinal mycobiota Some fungal species detected in the gut have been associated with human diet, and fruits and vegetables are likely sources of these species (Table 2). For example, we observed that the fungal species detected in an obese patient (camemberti Penicillium, Penicillium rocquefortii, Penicillium brevicompactum, dipodomyicola Penicillium, Aspergillus flavipes, Galactomyces geotrichum) were different from those found in an anorexic patient (Penillium solitum, Aspergillus ruber, Cladosporium bruhnei, S. Cerevisiae) [10,28]. In particular, camemberti Penicillium, Penicillium rocquefortii, Penicillium brevicompactum, dipodomyicola Penicillium, Aspergillus flavipes, Galactomyces

geotrichum, Galactomyces candidum are natural contaminants of foods such as cheese and meat that can be contaminated by P. Solitum and A. Ruber. We identified respectively 16 and 10 fungal diet related species in an obese and an anorexic

Table 2 Intestinal fungi and food source. Sources alimentaires des champignons intestinaux. Intestinal fungal species

Source

Penicillium camemberti Penicillium brevicompactum Penicillium dipodomyicola Galactomyces geotrichum Penicillium allii Aspergillus flavipes Aspergillus ruber Penicillum solitum Cladosporium bruhnei Penicillium rocquefortii Saccharomyces cerevisiae

Cheese [10] Meat [10] Fruits [10] Cheese [10] Cereals [10] Cereals [10] Fruits [28] Fruits [28] Vegetables [28] Cheese [28] Beer [28]

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Table 3 Fungal species distribution in healthy individuals and in the course of diseases. Distribution des espèces fungiques chez les individus sains, et au cours de certaines pathologies. Healthy individuals

IBD

Hepatitis B

HIV infection

Acremonium Acremonium sp.a Agaricus Alternariaa Armillariaa Arxiozyma tellurisa Aspergillus Aspergillus ruber Aspergillus versicolor Asterophora parasiticaa Auriculariaa Bjerkandera adusta Blastoschizomyces capitatus Candida Candida albicans Candida edaphicusa Candida glabrata Candida guilliermondii Candida kefyr Candida krissii Candida krusei Candida lusitaniae Candida parapsilosis Candida rugosaa Candida spp. Candida tropicalis Candida zeynaloides Cephalosporium sp.a Ceratobasidium sp.a Ceratocystisa Ceriporiaa Chaetomium Chondrostereuma Cinereomycesa Cladosporium Clavicepsa Clavispora Cochliobolusa Colletotrichuma Coniosporiuma Cryotococcus Cryptococcus albidusa Cryptococcus luteolusa Debaryomycesa Eurotiuma Eutypellaa Exophiala Filobasidium Fusarium Fusarium spp. Galactomyces Galactomyces candidum Galactomyces geotrichum Galactomyces sp. Geothricum spp. Geotrichum candida Gloeotinia temulenta Glomerella Hanseniaspora Hymenochaete Hypholoma Kluyveromyces Kluyveromyces hubeiensis

Aureobasidium pullulans Bjerkandera adusta Bullera croceaa Candida albicans Candida austromarina Candida dubliensisa Candida incospicuaa Candida spp. Chaetomium globosum Cladosporium cladosporioides Cryptococcus carnescensa Cystofilobasidium capitatum Dacrymyces sp.a Dothideomycete sp.a Exidiopsis calceaa Filobasidium globisporuma Flammulina velutipesa Fomitopsis pinicolaa Fusarium oxysporum Galactomyces geotrichum Graphiola phoenicisa Madurella mycetomatisa Penicillium chrysogenuma Penicillium italicuma Penicillum sacculuma Pleospora herbaruma Raciborskiomyces longisetosuma Rhodotorula aurantiacaa Rhodotorula mucilaginosaa Saccharomyces cerevisiae Sclerotinia sclerotiorum Sclerotium sp. Sirococcus conigenusa Sporobolomyces ogasawarensis Trametes versicolora Tricholoma saponaceuma Trichosporon dermatisa Uncultured ascomycete a Uncultured basidiomycetea Uncultured ustilaginomycete a Ustilago maydisa Ustilago sp.a Yarrowia lipolytica

Aspergillus penicillioidesa Aspergillus versicolor Aureobasidium pullulans Candida albicans Candida austromarina Candida intermedia Candida krissii Candida milleria Candida solania Candida tropicalis Chaetomium globosum Chaetomium sp.a Cryptococcus fragicolaa Doratomyces stemonitisa Fusarium sp.a Galactomyces geotrichum Hyphozyma variabilisa Iodophanus carneusa Ophiocordyceps caloceroidesa Penicillium sp.a Rhizopus microsporusa Saccharomyces cerevisiae Saccharomyces paradoxus Saccharomyces sp. Simplicillium lanosoniveuma Simplicillium obclavatuma Uncultivatable Pezizomycotinaa Wallemia muriaea Wallemia sebia

Candida albicans Candida glabrata Candida krusei Candida parapsilosis Candida spp. Candida tropicalis Cryptococcus neoformans Geotrichum candida Histoplasma capsulatuma Penicillium marneffei Saccharomyces cerevisiae

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Table 3 (Continued) Healthy individuals

IBD

Hepatitis B

HIV infection

Lasiodiplodia Lentinus Lycogala flavofuscum Malassezia globosa Malassezia pachydermatis Malassezia restricta Metschnikowia Meyerozyma Microdochium Millerozyma Miptoporus Mucor Mucor racemosus Mucor spp. Mycocentrospora Mycosphaerella Neafusicoccum Nigrospora Ophiostoma Paecilomyces fumosoroseus Penicillium Penicillium freii Penicillium glabrum Penicillium roquefortii Penicillium spp. Perenniporia Phaeococcomyces Phanerochaete stereoides Phlebia Pichia Psathyrella candolleana Rhodotorula Rhodotorula glutinis Rhodotorula rubra Rhodotorula sp. Saccharomyces Saccharomyces bayanus Saccharomyces cerevisiae Saccharomyces paradoxus Saccharomyces sp. Skelotocutis Sporobolomyces ogasawarensis Stemphylium Sterigmatomyce elviae Strelitziana Teratsphaeria Thanatephorus Torulaspora Torulaspora pretoriensisa Trichosporon asahiia Trichosporon beigelii Trichosporon caseoruma Trichosporon cutaneuma Trichosporon spp. Trichpatuma Tyromycesa Uncultured Banisvelda Uncultured fungal spp.a Wallemia Xeromycesa Yarrowia lipolytica Zygosaccharomycesa a

Species only found in the corresponding disease.

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patient [10,28]. A great variety including 66 genera of fungi was detected in 98 healthy individuals with different diets [29]. Saccharomyces (89%), Candida (57%), and Cladosporidium were the most common genera and Candida was positively correlated with high carbohydrate diets. However, the possible role of fungi in the digestion of food remains unclear.

5. Intestinal mycobiota during systemic diseases The intestinal mycobiota was analyzed in the course of 13 conditions, including inflammatory bowel diseases, transplantation, gastric ulcer and gastritis, blood diseases, HIV infection and other immunodeficiencies, paracoccidioidomycosis, basidiobolomycosis, anorexia, and obesity by comparing hospitalized patients with healthy individuals. C. Albicans was identified in the stools of 63% of healthy individuals, 70% of inpatients, 91% of patients with inflammatory bowel disease, and 87% of patients (Table 3) [4,5,30,31]. However, there is a decrease of fungal species diversity among ill patients; 118 different fungal species were identified in healthy individuals, 42 species in patients presenting with inflammatory bowel disease (IBD), 29 species in patients presenting with hepatitis B, and 11 species in HIV infected patients; 33 species were identified only in healthy individuals, 27 species were identified only in patients presenting with IBD, 17 species only in patients presenting with hepatitis B, and H. Capsulatum only in HIV infected patients (Table 3) [7,31–35]. C. Glabrata was significantly more frequent in hospitalized patients than in healthy controls (P = 0.001) [4,5]. Candida spp. was significantly more prevalent in HIV infected patients in case of diarrhea and a recent antibiotic treatment, compared to healthy controls [29,36,37]. Intestinal Candida spp. colonization correlated significantly with IBD and graft versus host disease [31,38]. A greater fungal diversity was detected by molecular techniques in patients with IBD or hepatitis B, than in healthy controls [7,32]. 16 different fungal species were detected in the feces and intestinal contents of 2 intestinal transplant patients [39]. Some strict and opportunistic pathogens including Aspergillus flavus, Basidibolus ranarum, Cryptococcus noeformans, Exophilia dermatidis, H. Capsulatum, Paracoccidioides brasiliensis, and Penicillium marneffei were isolated in immunocompromised patients and in 1 patient with diarrhea [17,32–43].

6. Intestinal mycobiota as a source of fungal infection Intestinal fungi may be responsible for fungal infection [44]. Molecular typing used to trace the source of fungal infection [45], can be performed by pulsed field gel electrophoresis (PFGE), karyotyping, restriction fragment length polymorphism (RFLP), and random PCR amplification (RAPD). The same strain of C. Albicans was isolated in the feces and blood of an HIV infected patient and many patients presenting with candidemia using molecular typing RAPD [43,45–47]. The source of C. Albicans was assessed by RFLP in 34 newborns and an

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identical strain was isolated in the stools and blood. The same was true for 1 newborn infected by C. Glabrata [48,49]. 7. Conclusion Two hundred and forty-seven fungal species belonging to 126 genera were identified as the intestinal mycobiota by culture and by molecular techniques in feces and gastrointestinal biopsies. Culture allowed identifying only 40 species compared to molecular techniques that allowed identifying 188 species; 19 additional species were identified by both methods. The “culturomics” developed to examine bacteria by culture [50] should be used to study the intestinal mycobiome so as to expand the repertoire of intestinal fungi and clarify their role in intestinal infections and fungal infection. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. Acknowledgements Nina Guba and Michel Drancourt reviewed the literature and wrote the article. Nina Guba drafted the tables and figures. References [1] Cui L, Morris A, Ghedin E. The human mycobiome in health and disease. Genome Med 2013;5:63. [2] Ghannoum MA, Jurevic RJ, Mukherjee PK, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 2010;6:e1000713. [3] Ghannoum MA, Mukherjee PK. The human mycobiome and its impact on health and disease. Curr Fungal Infect Rep 2013;7:345–50. [4] Agirbasli H, Ozcan SA, Gedikoglu G. Fecal fungal flora of pediatric healthy volunteers and immunosuppressed patients. Mycopathologia 2005;159:515–20. [5] Khatib R, Riederer KM, Ramanathan, et al. Faecal fungal flora in healthy volunteers and inpatients. Mycoses 2001;44:151–6. [6] Zwolinska-Wcislo M, Budak A, Bogdal, et al. Fungal colonization of gastric mucosa and its clinical relevance. Med Sci Monit 2001;7:982–8. [7] Ott SJ, Kuhbacher T, Musfeldt M, et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol 2008;43:831–41. [8] Beuchat LR. Media for detecting and enumerating yeasts and moulds. Int J Food Microbio 1992;17:145–58. [9] Morris AJ, Byrne TC, Madden JF, et al. Duration of incubation of fungal cultures. J Clin Microbiol 1996;34:1583–5. [10] Gouba N, Raoult D, Drancourt M. Plant and fungal diversity in gut microbiota as revealed by molecular and culture investigations. PLoS One 2013;8:e59474. [11] Gouba N, Raoult D, Drancourt M. Eukaryote culturomics of the gut reveals new species. PLoS One 2014;9:e106994. [12] Scanlan PD, Marchesi JR. Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and -independent analysis of faeces. ISME J 2008;2:1183–93. [13] Gorton RL, Seaton S, Ramnarain P, McHugh TD, Kibbler CC. Evaluation of a short, on-plate formic acid (FA) extraction method for MALDI-TOF MSbased identification of clinically relevant yeast isolates. J Clin Microbiol 2014;52(4):1253–5.

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Please cite this article in press as: Gouba N, Drancourt M. Digestive tract mycobiota: A source of infection. Med Mal Infect (2015), http://dx.doi.org/10.1016/j.medmal.2015.01.007