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Mycobiome and Cancer: What Is the Evidence?

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Mycobiome and Cancer: What Is the Evidence? cancers Review Mycobiome and Cancer: What Is the Evidence? Natalia Vallianou 1,*, Dimitris Kounatidis 1 , Gerasimos Socrates Christodoulatos 2, Fotis Panagopoulos 1, Irene Karampela 3 and Maria Dalamaga 2,* 1 First Department of Internal Medicine, Evangelismos General Hospital, 45-47 Ipsilantou Str., 10676 Athens, Greece; [email protected] (D.K.); [email protected] (F.P.) 2 Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 75 Mikras Asias, Goudi, 11527 Athens, Greece; [email protected] 3 Second Department of Critical Care, Attikon General University Hospital, Medical School, National and Kapodistrian University of Athens, 1 Rimini St, Haidari, 12462 Athens, Greece; [email protected] * Correspondence: [email protected] (N.V.); [email protected] (M.D.) Simple Summary: Although comprising a much smaller proportion of the human microbiome, the fungal community has gained much more attention lately due to its multiple and yet undiscovered interactions with the human bacteriome and the host. Head and neck cancer carcinoma, colorectal carcinoma, and pancreatic ductal adenocarcinoma have been associated with dissimilarities in the composition of the mycobiome between cases with cancer and non-cancer subjects. In particular, an abundance of Malassezia has been associated with the onset and progression of colorectal carcinoma and pancreatic adenocarcinoma, while the genera Schizophyllum, a member of the oral mycobiome, is suggested to exhibit anti-cancer potential. The use of multi-omics will further assist in establishing whether alterations in the human mycobiome are causal or a consequence of specific types of cancers. Citation: Vallianou, N.; Kounatidis, D.; Christodoulatos, G.S.; Abstract: Background: To date, most researchhas focused on the bacterial composition of the human Panagopoulos, F.; Karampela, I.; microbiota. In this review, we synopsize recent data on the human mycobiome and cancer, highlight- Dalamaga, M. Mycobiome and ing specific cancer types based on current available evidence, presenting interesting perspectives Cancer: What Is the and limitations of studies and laboratory methodologies. Recent findings: Head and neck cancer Evidence? Cancers 2021, 13, 3149. carcinoma (HNCC), colorectal carcinoma (CRC) and pancreatic ductal adenocarcinoma (PDA) have https://doi.org/10.3390/ been associated with dissimilarities in the composition of mycobiota between cancer cases and cancers13133149 non-cancer participants. Overall, fungal dysbiosis with decreased fungal richness and diversity was common in cancer patients; however, a specific mycobiotic signature in HNSCC or CRC has not Academic Editor: Erle S. Robertson emerged. Different strains of Candida albicans have been identified among cases with HNCC, whilst Received: 22 May 2021 Lichtheimia corymbifera, a member of the Mucoraceae family, has been shown to predominate among Accepted: 23 June 2021 patients with oral tongue cancer. Virulence factors of Candida spp. include the formation of biofilm Published: 24 June 2021 and filamentation, and the secretion of toxins and metabolites. CRC patients present a dysregulated ratio of Basidiomycota/Ascomycota. Abundance of Malassezia has been linked to the occurrence and Publisher’s Note: MDPI stays neutral progression of CRC and PDA, particularly in animal models of PDA. Interestingly, Schizophyllum, with regard to jurisdictional claims in a component of the oral mycobiome, may exhibit anti-cancer potential. Conclusion: The human published maps and institutional affil- mycobiome, per se, along with its interactions with the human bacteriome and the host, may be iations. implicated in the promotion and progression of carcinogenesis. Fungi may be used as diagnostic and prognostic/predictive tools or treatment targets for cancer in the coming years. More large-scale, prospective, multicentric and longitudinal studies with an integrative multi-omics methodology are required to examine the precise contribution of the mycobiome in the etiopathogenesis of cancer, and Copyright: © 2021 by the authors. to delineate whether changes that occur in the mycobiome are causal or consequent of cancer. Licensee MDPI, Basel, Switzerland. This article is an open access article Keywords: cancer; colorectal cancer; fungi; head and neck cancer; microbiome; mycobiome; pancre- distributed under the terms and atic cancer conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Cancers 2021, 13, 3149. https://doi.org/10.3390/cancers13133149 https://www.mdpi.com/journal/cancers Cancers 2021, 13, x 2 of 20 Cancers 2021, 13, 3149 2 of 21 1. Introduction 1. IntroductionFungi have recently been estimated to consist of up to 3.8 million species; thus, they representFungi a taxonomic have recently and functional been estimated diversity toconsist of life forms, of up being to 3.8 implicated million species; in complex thus, andthey yet represent unknown a taxonomicinteractions and with functional other livi diversityng microorganisms of life forms, [1]. beingFungi implicatedare microeu- in karyotescomplex and and constitute yet unknown a smaller interactions part of the with human other microbiome living microorganisms in comparison [1 ].to Fungi bacteria, are formingmicroeukaryotes the so-called and “human constitute mycobiome” a smaller part [2–4]. of theFungal human communities microbiome can in be comparison found in differentto bacteria, anatomic forming sites the of so-called the human “human body, mycobiome” as depicted [in2– Figure4]. Fungal 1. communities can be found in different anatomic sites of the human body, as depicted in Figure1. FigureFigure 1. 1. MostMost common common genera genera of of fung fungii found found in in different different human body sites under physiologic conditions. (All (All images images originateoriginate from from the the free medical website http://smart.servier.com/ (accessed (accessed on on 25 25 May May 2021) 2021) by by Servier Servier licensed licensed under under a a CreativeCreative Commons Commons Attributio Attributionn 3.0 3.0 Unported Unported License). License). 14 TheThe number number of of human human microbiota microbiota has has been been determined determined to to be be 10 14, ,about about 10 10 times times greatergreater than than the the number number of of human human cells. cells. Also Also,, the the quantity quantity of microbial of microbial genes genes is about is about 100 times100 times more more than thanthe corresponding the corresponding quantity quantity of human of human genes. genes. The Thehuman human mycobiome mycobiome ac- countsaccounts for forapproximately approximately 0.001% 0.001% to 0.1% to 0.1% of the of microbial the microbial community community in the ingut the [5,6]. gut Over [5,6]. theOver last the years, last years,fungi have fungi been have the been subject the subject of intense of intense investigation, investigation, with a withparticular a particular focus onfocus their on contribution their contribution to human to human disorders, disorders, especially especially among among immune-compromised immune-compromised pa- tientspatients [7]. [ 7However,]. However, as asmost most fungi fungi are are not not easi easilyly cultured, cultured, even even in in specific specific cultural cultural media, media, theirtheir study study has has been been limited limited until until today, today, due due mainly mainly to to the the unavailability unavailability of of methods methods used used forfor their their detection. Nevertheless,Nevertheless, genomicgenomic methodology methodology in in fungi fungi research research may may broaden broaden our knowledge in their contribution to health and disease [2–4]. High-throughput sequencing our knowledge in their contribution to health and disease [2–4]. High-throughput se- (HTS) analysis of fungi is reshaping the area of the fungal community [1]. quencing (HTS) analysis of fungi is reshaping the area of the fungal community [1]. In the gut, bacteria outnumber fungi, but we cannot overlook the fact that fungal taxa may merely be determined with modern sophisticated, non-culture-based methods. Despite the fact that the gut mycobiome is less analyzed than the bacteriome, it seems Cancers 2021, 13, 3149 3 of 21 likely that fungi are primarily spread intra-uterinally to the fetus [8]. Recent studies have suggested that fungi are found in the gut microflora of young children via transmission from their mother, siblings and environmental exposure; nevertheless, diet may be the most significant factor [9]. Dietary intake plays a key role, as fungi colonize the gut by food digestion. Fungi which colonize the intestines via dietary intake could be part of the gut flora or be rejected [3]. Despite the paucity of studies, the importance of dietary intake in the content of the intestinal mycobiome is confirmed by the fact that vegetarians present dissimilarities in the mycobiotic composition in comparison to those following a Western-style nutrition [3,10]. The interplay of intestinal mycobiome with bacteriome and virome is a hot topic of research, especially in the field of mycobiome-associated diseases. Current scientific evidence has supported the contribution of the intestinal mycobiome in affecting immune response, with an impact on regional and systemic disease [11]. Notably, a considerable number of pathogenic fungi are “pathobionts”, i.e., residents in the organism that are not implicated in the pathogenesis
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