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Archaea and Fungi of the Human Gut Microbiome: Correlations with Diet and Bacterial Residents
Open accessAbstract
Diet influences health as a source of nutrients and toxins, and by shaping the composition of resident microbial populations. Previous studies have begun to map out associations between diet and the bacteria and viruses of the human gut microbiome. Here we investigate associations of diet with fungal and archaeal populations, taking advantage of samples from 98 well-characterized individuals. Diet was quantified using inventories scoring both long-term and recent diet, and archaea and fungi were characterized by deep sequencing of marker genes in DNA purified from stool. For fungi, we found 66 genera, with generally mutually exclusive presence of either the phyla Ascomycota or Basiodiomycota. For archaea, Methanobrevibacter was the most prevalent genus, present in 30% of samples. Several other archaeal genera were detected in lower abundance and frequency. Myriad associations were detected for fungi and archaea with diet, with each other, and with bacterial lineages. Methanobrevibacter and Candida were positively associated with diets high in carbohydrates, but negatively with diets high in amino acids, protein, and fatty acids. A previous study emphasized that bacterial population structure was associated primarily with long-term diet, but high Candida abundance was most strongly associated with the recent consumption of carbohydrates. Methobrevibacter abundance was associated with both long term and recent consumption of carbohydrates. These results confirm earlier targeted studies and provide a host of new associations to consider in modeling the effects of diet on the gut microbiome and human health.
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“In addition, members of the microbiome may drastically affect the growth of co-habitants (Hoffmann et al., 2013).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Hoffmann et al., 2013
In the citing paper
“carbohydrate consumption is associated with the proportion of the archaeon, Methanobrevibacter,46 in the intestinal microbiota.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [46]
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“Diet has also been associated with other types of microbes in the gut, such as archaea, fungi, and bacteriophage (Figure 2)45-47.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [46]
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“Infections with C. albicans can range from superficial mucosal and dermatological infections to life-threatening infections of the bloodstream and vital organs.”
From Molecular and genetic basis of azole antifungal resistance in the opportunistic pathogenic fungus Candida albicans (2020) · cites this paper as [1]
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1 retracted
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BackgroundHuman gut microbiota in health and disease: Unveiling the relationship
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“An increased prevalence of Methanobrevibacter spp. correlated, albeit nonsignificantly, with short-term and long-term carbohydrate ingestion (160), as was the case in anorexic patients (175), whereas the prevalence of Nitrososphaera spp. correlated, albeit…”
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BackgroundDiet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease
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BackgroundResultThe Human Microbiome and Its Impacts on Health
Ogunrinola, G. A., Oyewale, J. O., Oshamika, O. O., & Olasehinde, G. I. (2020) · International Journal of Microbiology · doi:10.1155/2020/8045646 · Cited by 482
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BackgroundThe Gut Microbiota in Immune-Mediated Inflammatory Diseases
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“Figure 1 shows a schematic illustration of the interaction between the immune system and gut microbiota in IMID.”
BackgroundArchaea and the Human Gut: New Beginning of an Old Story
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“smithii is positively associated with diets high in carbohydrates [22].”
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Gut microorganisms as promising targets for the management of type 2 diabetes
Delzenne, N. M., Cani, P. D., Everard, A., Neyrinck, A. M., & Bindels, L. B. (2015) · Diabetologia · doi:10.1007/s00125-015-3712-7 · Cited by 271
“15 he al th y in di vi du al s; cr os so ve r in te rv en tio n B re ak fa st co nt ai ni ng 6 g of A X = po st pr an di al gl yc ae m ia ,↓ po st pr an di al in su lin ae m ia [1 08 ]”
BackgroundInfluentialXu, J. (2016) · Genome · doi:10.1139/gen-2016-0046 · Cited by 277
The microbiota in inflammatory bowel disease
Sheehan, D., Moran, C. P., & Shanahan, F. (2015) · Journal of Gastroenterology · doi:10.1007/s00535-015-1064-1 · Cited by 260
Fungi as mediators linking organisms and ecosystems
Bahram, M., & Netherway, T. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab058 · Cited by 271
“Carbohydrate substrates of fungi play an important role in their fitness in the gut, as evidenced by increased abundance of Candida following the consumption of carbohydrate rich foods, whereas they respond negatively to saturated fatty acids (Hoffmann et al. 2013).”
Gut Mycobiota in Immunity and Inflammatory Disease
Li, X. V., Leonardi, I., & Iliev, I. D. (2019) · Immunity · doi:10.1016/j.immuni.2019.05.023 · Cited by 246
Fungal-Bacterial Interactions in Health and Disease
Krüger, W., Vielreicher, S., Kapitan, M., Jacobsen, I. D., & Niemiec, M. J. (2019) · Pathogens · doi:10.3390/pathogens8020070 · Cited by 234
“Defining the gut mycobiota from healthy stool identified Ascomycota and Basidiomycota as the most abundant taxa, and the dominant genera are Saccharomyces , Candida , Malassezia , and Cladosporium [53,54,205].”
Age and Gender Affect the Composition of Fungal Population of the Human Gastrointestinal Tract
Strati, F., Paola, M. D., Stefanini, I., Albanese, D., Rizzetto, L., Lionetti, P., Calabrò, A., Jousson, O., Donati, C., Cavalieri, D., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01227 · Cited by 231
“As occurs for the bacterial microbiota, the intestinal mycobiota is shaped by host’s age, gender, diet, and geographical environment (Yatsunenko et al., 2012; Hoffmann et al., 2013; David et al., 2014).”
BackgroundFungi stabilize connectivity in the lung and skin microbial ecosystems
Tipton, L., Müller, C. L., Kurtz, Z. D., Huang, L., Kleerup, E. C., Morris, A., Bonneau, R., & Ghedin, E. (2018) · Microbiome · doi:10.1186/s40168-017-0393-0 · Cited by 234
Homeostasis and dysbiosis of the gut microbiome in health and disease
Das, B., & Nair, G. B. (2019) · Journal of Biosciences · doi:10.1007/s12038-019-9926-y · Cited by 225
Impact of Diet on Human Intestinal Microbiota and Health
Salonen, A., & de Vos, W. M. (2014) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030212-182554 · Cited by 220
Analyses of Intestinal Microbiota: Culture versus Sequencing: Figure 1
Hiergeist, A., Gläsner, J., Reischl, U., & Gessner, A. (2015) · ILAR Journal · doi:10.1093/ilar/ilv017 · Cited by 221
“…least half of the gut-residing bacteria are gram-positive (Gossling and Slack 1974; Lagier, Million et al. 2012), and the commonly hardto-lyse domain of the Archaea is represented predominantly by methanogenicMethanobrevibacter spp.with a variable and overall low prevalence (Hoffmann et al. 2013).”
BackgroundThe Fungal Mycobiome and Its Interaction with Gut Bacteria in the Host
Sam, Q. H., Chang, M. W., & Chai, L. Y. A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020330 · Cited by 226
“[17] reported a strong link between consumed foods and fungal abundance in the gut.”
Mycobiota in gastrointestinal diseases
Mukherjee, P. K., Sendid, B., Hoarau, G., Colombel, J., Poulain, D., & Ghannoum, M. A. (2014) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2014.188 · Cited by 215
Microbial ‘old friends’, immunoregulation and socioeconomic status
Rook, G. A. W., Raison, C. L., & Lowry, C. A. (2014) · Clinical & Experimental Immunology · doi:10.1111/cei.12269 · Cited by 218
Diet and Inflammatory Bowel Disease: Review of Patient-Targeted Recommendations
Hou, J. K., Lee, D. Y., & Lewis, J. D. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2013.09.063 · Cited by 204
“For example, Candida may utilize starch, liberating simple carbohydrates that are used by bacteria such as Prevotella and Ruminococcus , which in turn produce substrates for fermentation that can be used by Methanobrevibacter to produce CH 4 and or CO 2 .”
The human gut mycobiome: pitfalls and potentials—a mycologist’s perspective
Haute, M. J. S. V., & Hallen‐Adams, H. E. (2015) · Mycologia · doi:10.3852/15-147 · Cited by 205
“An estimated 75% of women will suffer a yeast infection during their lifetime and roughly 20–25% of the world’s population has skin mycoses (Sobel 2007, Havlickova et al. 2008).”
BackgroundModelling approaches for studying the microbiome
Kumar, M., Ji, B., Zengler, K., & Nielsen, J. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0491-9 · Cited by 200
Norman, J. M., Handley, S. A., & Virgin, H. W. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.001 · Cited by 186
Tan, D.-X., Zheng, X., Kong, J., Manchester, L., Hardeland, R., Kim, S., Xu, X., & Reiter, R. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150915858 · Cited by 188
“Many archaea also inhabit the gastrointestinal tract of animals including that of the human [146,147].”
BackgroundStress and the gut microbiota-brain axis
Molina‐Torres, G., Rodríguez-Arrastia, M. J., Román, P., Sánchez‐Labraca, N., & Cardona, D. (2019) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000478 · Cited by 189
“Despite previous probiotic health claims having been exaggerated (Shanahan, 2002; Hoffmann et al., 2013; Sanders, 2016), it is particularly interesting to consider the possibility that probiotics can affect emotion in health and disease by modulating the GMB and confer a health benefit on the host (Dinan et al.”
Early gut mycobiota and mother-offspring transfer
Schei, K., Avershina, E., Øien, T., Rudi, K., Follestad, T., Salamati, S., & Ødegård, R. A. (2017) · Microbiome · doi:10.1186/s40168-017-0319-x · Cited by 179
“These fungi consume nutrients and may facilitate nutrient extraction and assist in digestion through enzyme and vitamin production [7, 8].”
BackgroundReview article: the gut microbiome in inflammatory bowel disease—avenues for microbial management
Mcilroy, J. R., Ianiro, G., Mukhopadhya, I., Hansen, R., & Hold, G. L. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14384 · Cited by 178
Viral communities of the human gut: metagenomic analysis of composition and dynamics
Aggarwala, V., Liang, G., & Bushman, F. D. (2017) · Mobile DNA · doi:10.1186/s13100-017-0095-y · Cited by 185
Fungi of the human gut microbiota: Roles and significance
Pérez, J. C. (2021) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2021.151490 · Cited by 189
Meta'omic Analytic Techniques for Studying the Intestinal Microbiome
Morgan, X. C., & Huttenhower, C. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.01.049 · Cited by 181
Intestinal mycobiota in health and diseases: from a disrupted equilibrium to clinical opportunities
Wu, X., Xia, Y., He, F., Zhu, C., & Ren, W. (2021) · Microbiome · doi:10.1186/s40168-021-01024-x · Cited by 177
Fungi inhabiting the healthy human gastrointestinal tract: a diverse and dynamic community
Hallen‐Adams, H. E., Kachman, S. D., Kim, J., Legge, R. M., & Martínez, I. (2015) · Fungal ecology · doi:10.1016/j.funeco.2015.01.006 · Cited by 169
“…it is expected that the role of human-associated eukaryotes will come under increasing scrutiny in the next several years, and papers are just beginning to address the role of organisms other than bacteria in the healthy human ( Andersen et al., 2013, Gouba et al., 2013 and Hoffmann et al., 2013).”
InfluentialShuai, M., Fu, Y., Zhong, H., Gou, W., Jiang, Z., Liang, Y., Miao, Z., Xu, J., Huynh, T., Wahlqvist, M. L., et al. (2022) · Gut · doi:10.1136/gutjnl-2021-326298 · Cited by 161
Cross-Domain and Viral Interactions in the Microbiome
Rowan-Nash, A. D., Korry, B. J., Mylonakis, E. E., & Belenky, P. A. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00044-18 · Cited by 173
“A few groups have used ITS sequencing in humans to identify potential members of a core oral mycobiome, including Candida, Cladosporium, Alternaria, Aspergillus, Fusarium, Cryptococcus, and Aureobasidium (211–213).”
BackgroundInfluentialVemuri, R., Shankar, E. M., Chieppa, M., Eri, R., & Kavanagh, K. (2020) · Microorganisms · doi:10.3390/microorganisms8040483 · Cited by 162
“For example, Candida abundance is found to be strongly associated with the recent ingestion of carbohydrates [100].”
BackgroundYeasts as probiotics: Mechanisms, outcomes, and future potential
Sen, S., & Mansell, T. J. (2020) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2020.103333 · Cited by 169
Mycobiome in the Gut: A Multiperspective Review
Chin, V. K., Yong, P. V. C., Chong, P. P., Nordin, S. A., Basir, R., & Abdullah, M. (2020) · Mediators of Inflammation · doi:10.1155/2020/9560684 · Cited by 161
“Although this study has identified various fungal communities in the gut, one of the concerns raised in this study is whether these fungal mycobiota identified are permanent residents in the gut or just transient species [19].”
BackgroundKumar, S., Indugu, N., Vecchiarelli, B., & Pitta, D. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00781 · Cited by 161
“The resulting amplified PCR products were bead purified using a Beckman Coulter Agencourt AMPure XP Beads (Beckman-Coulter, Pasadena, CA, USA) as described by Hoffmann et al. (2013).”
MethodMycobiome: Approaches to analysis of intestinal fungi
Tang, J., Iliev, I. D., Brown, J. S., Underhill, D. M., & Funari, V. A. (2015) · Journal of Immunological Methods · doi:10.1016/j.jim.2015.04.004 · Cited by 157
“While most studies of the gastrointestinal microbiota focus on commensal and pathogenic bacteria, we and others have recently begun to explore the fungi that are also present in these communities (Scupham et al., 2006; Iliev et al., 2012; Dollive et al., 2013; Hoffmann et al., 2013).”
BackgroundThe role of the microbiome in nonhealing diabetic wounds
Kalan, L., & Brennan, M. B. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13926 · Cited by 162
Archaea: Essential Inhabitants of the Human Digestive Microbiota
Nkamga, V. D., Henrissat, B., & Drancourt, M. (2017) · Human Microbiome Journal · doi:10.1016/j.humic.2016.11.005 · Cited by 141
“A higher intake of carbohydrates correlated with Methanobrevibacterpositive samples [59].”
BackgroundStructural diversity, functional aspects and future therapeutic applications of human gut microbiome
Ghosh, S., & Pramanik, S. (2021) · Archives of Microbiology · doi:10.1007/s00203-021-02516-y · Cited by 158
Temporal dynamics in the ruminal microbiome of dairy cows during the transition period
Pitta, D., Kumar, S., Vecchiarelli, B., Shirley, D. J., Bittinger, K. L., Baker, L. D., Ferguson, J. D., & Thomsen, N. K. (2014) · Journal of Animal Science · doi:10.2527/jas.2014-7621 · Cited by 154
The Human MycobiomePreprint
Seed, P. C. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019810 · Cited by 149
“The investigators suggest that Candida, Prevotella, Ruminococcus, and Methanobrevibacter may form a syntrophic guild with Candida providing metabolisms of complex carbohydrates, whereas Prevotella and Ruminococcus ferment the more simple sugars liberated by Candida.”
BackgroundMethodInfluentialBittinger, K. L., Charlson, E. S., Loy, E., Shirley, D. J., Haas, A. R., Laughlin, A. L., Yi, Y., Wu, G. D., Lewis, J. D., Frank, I., et al. (2014) · Genome biology · doi:10.1186/s13059-014-0487-y · Cited by 149
“However, fungal-bacterial interactions have not been studied extensively using culture-independent sequencebased methods (for a few examples see [5-9]).”
BackgroundHuman Gut Microbiota: Toward an Ecology of Disease
Selber‐Hnatiw, S., Rukundo, B., Ahmadi, M., Akoubi, H., Al-Bizri, H., Aliu, A. F., Ambeaghen, T. U., Avetisyan, L., Bahar, I., Baird, A., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01265 · Cited by 151
“Human-associated Archaea, among which Methanobrevibacter smithii found in almost 96% of healthy subjects, synthesize methane from H2 produced by bacterial catabolism (Hoffmann et al., 2013; Lurie-Weinberger and Gophna, 2015).”
BackgroundInfluentialGeurden, I., Mennigen, J. A., Plagnes‐Juan, E., Véron, V., Cerezo, T., Mazurais, D., Zambonino‐Infante, J., Gatesoupe, F.-J., Cassy, S., & Panserat, S. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.106062 · Cited by 145
Metadata
- Authors
- Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., Wu, G. D., Lewis, J. D., & Bushman, F. D.
- Affiliations
- Universidade Federal de Goiás (BR)
- University of Pennsylvania (US)
- Harvard University (US)
- Corresponding author
- Wu, Gary D.
- Lewis, James D.
- Bushman, Frederic D.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-06-17
- Volume
- 8
- Issue
- 6
- Pages
- e66019
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3684604
- OpenAlex
- W2110345840
- Cited by
- 808
- References
- 62
- Citations by year
- 2026: 38 · 2025: 56 · 2024: 73 · 2023: 59 · 2022: 86 · 2021: 85 · 2020: 87 · 2019: 76 · 2018: 60 · 2017: 62 · 2016: 36 · 2015: 45 · 2014: 40 · 2013: 4
- FWCI
- 18.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Pennsylvania Department of Health
- University of Pennsylvania (UL1 RR024134)
- National Institutes of Health (and K24, DK050306)
- National Institute of Diabetes and Digestive and Kidney Diseases (K24DK078228, DK 089472, R01DK089472, UH2/3 DK083981, UH3DK083981, UH2DK083981, P30DK050306)
- National Center for Research Resources (UL1RR024134, S10RR024525)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- gut microbiota, archaea, fungi, diet, Methanobrevibacter, Candida, Ascomycota, carbohydrate intake, long-term diet, microbial co-occurrence, human health
- MeSH terms
- Archaea, Bacteria, Diet, Fungi, Humans, Intestines, Microbiota
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