An ecological framework to understand the efficacy of fecal microbiota transplantation

Xiao, Yandong; Angulo, Marco Tulio; Lao, Songyang; Weiss, Scott T.; Liu, Yang‐Yu

doi:10.1038/s41467-020-17180-x

Cited by 71 publications

(54 citation statements)

References 107 publications

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“…For the transplantation, the stool is mixed with saline or medium, homogenized and filtrated, and the supernatant is transferred into the patient’s colon by means of a colonoscopy, nasogastric tube or enema. To increase the chance of recovery, the transfer of microorganisms as well as other molecules, e.g., short-chain fatty acids, is required [ 19 , 20 ]. Then, the success of FMT has been shown to result in recovery rates of up to 90% [ 21 , 22 , 23 ].…”

Section: Introductionmentioning

confidence: 99%

Establishment of an In Vitro System of the Human Intestinal Microbiota: Effect of Cultivation Conditions and Influence of Three Donor Stool Samples

2021

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Fecal microbiota transplantation (FMT) is an alternative method for the treatment of gastrointestinal diseases with a high recovery rate. Disadvantages are ethical concerns, high donor requirements and the low storability of stool samples. The cultivation of an in vitro microbiota in a continuous bioreactor was established as an alternative to FMT to overcome these problems. In this study, the influence of the system parameters and donor stool characteristics was investigated. Each continuous colonic fermentation system was inoculated with feces from three different donors until a stable state was established. The influence of the fermentation conditions on the system’s behavior regarding cell count, metabolic activity, short-chain fatty acid profile and microbiota composition as well as richness and diversity was assessed. Cultivation conditions were found to affect the microbial system: the number of cells and the production of short-chain fatty acids increased. The abundance of Actinobacteria and Firmicutes decreased, Bacteroidetes increased, while Proteobacteria and Verrucomicrobia remained largely unaffected. Diversity in the in vitro system decreased, but richness was unaffected. The cultivation of stool from different donors revealed that the performance of the created in vitro system was similar and comparable, but unique characteristics of the composition of the original stool remained.

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Section: Introductionmentioning

confidence: 99%

Establishment of an In Vitro System of the Human Intestinal Microbiota: Effect of Cultivation Conditions and Influence of Three Donor Stool Samples

2021

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“…More broadly, changes in the network structure of the microbiota could have a significant impact on how a host responds to subsequent perturbations such as antibiotic treatment or infection with a pathogen. For example, Xiao et al demonstrated that bacterial microbiota network structure could be used to predict FMT efficacy for treatment of recurrent infection by Clostridioides difficile by comparing the microbiota networks of donors and recipients ( 38 ). In the next set of experiments, we examined whether the differences in microbiota composition and network structure of uncolonized or C. albicans - colonized mice affected the ecological resistance of the bacterial communities.…”

Section: Resultsmentioning

confidence: 99%

Decreased Ecological Resistance of the Gut Microbiota in Response to Clindamycin Challenge in Mice Colonized with the Fungus Candida albicans

Markey

Pugliese

Tian

et al. 2021

mSphere

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The mammalian gut microbiota is a complex community of microorganisms which typically exhibits remarkable stability. As the gut microbiota has been shown to affect many aspects of host health, the molecular keys to developing and maintaining a “healthy” gut microbiota are highly sought after. Yet, the qualities that define a microbiota as healthy remain elusive. We used the ability to resist change in response to antibiotic disruption, a quality we refer to as ecological resistance, as a metric for the health of the bacterial microbiota. Using a mouse model, we found that colonization with the commensal fungus Candida albicans decreased the ecological resistance of the bacterial microbiota in response to the antibiotic clindamycin such that increased microbiota disruption was observed in C. albicans-colonized mice compared to that in uncolonized mice. C. albicans colonization resulted in decreased alpha diversity and small changes in abundance of bacterial genera prior to clindamycin challenge. Strikingly, co-occurrence network analysis demonstrated that C. albicans colonization resulted in sweeping changes to the co-occurrence network structure, including decreased modularity and centrality and increased density. Thus, C. albicans colonization resulted in changes to the bacterial microbiota community and reduced its ecological resistance. IMPORTANCE Candida albicans is the most common fungal member of the human gut microbiota, yet its ability to interact with and affect the bacterial gut microbiota is largely uncharacterized. Previous reports showed limited changes in microbiota composition as defined by bacterial species abundance as a consequence of C. albicans colonization. We also observed only a few bacterial genera that were significantly altered in abundance in C. albicans-colonized mice; however, C. albicans colonization significantly changed the structure of the bacterial microbiota co-occurrence network. Additionally, C. albicans colonization changed the response of the bacterial microbiota ecosystem to a clinically relevant perturbation, challenge with the antibiotic clindamycin.

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“…Heterologous FMT is the most widely used gut microbiome intervention in clinical settings. Most research so far has focused on the efficacy and safety of FMT (Baruch et al, 2021; Davar et al, 2021; Ding et al, 2019; Tabbaa et al, 2018; Xiao et al, 2020). Several studies reported that heterochronic FMT could result in the transfer of some physiological properties from the donor to the recipient, including lifespan and healthspan (Bárcena et al, 2019; Smith et al, 2017), the germinal center reaction (Keeney et al, 2014), and neurogenesis and behavior (D’Amato et al, 2020; Rinninella et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Establishment and Resilience of Transplanted Gut Microbiota in Aged Mice

Wang

Tang

et al. 2021

Preprint

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Fecal microbiota transplantation (FMT), a procedure in which fecal material is transferred from a donor to a recipient, has been increasingly used as a treatment to restore healthy gut microbiota. There is a substantial difference in the composition of gut microbiota between young and aged hosts, but little is known about whether age matching between the FMT donor and recipient affects microbiota restoration and long-term maintenance. In the present investigation, we aimed to study the establishment and resilience of transplanted gut microbiota in aged recipients. We treated naturally aged mice (20 months old) with a broad-spectrum antibiotic cocktail and monitored the restoration of gut microbiota over 8 weeks. The diversity of gut microbiota in aged mice failed to reach the baseline level via spontaneous recovery; in contrast, FMT from either (age-)matched or unmatched donors facilitated the recovery of gut microbiota diversity. The microbiota transplanted from different donors successfully established in the aged recipients and had long-term effects on the gene expression profiles of the host colon. Finally, we evaluated the long-term maintenance of transplanted microbiota via intentional disruption of gut homeostasis. We found that lack of age matching between FMT donors and recipients may decrease the resilience of transplanted gut microbiota against colonic inflammation. The results from our study systematically examining the effects of FMT on the gut homeostasis of aged hosts suggest that the compatibility between donors and recipients should be taken into account when implementing FMT.

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An ecological framework to understand the efficacy of fecal microbiota transplantation

Cited by 71 publications

References 107 publications

Establishment of an In Vitro System of the Human Intestinal Microbiota: Effect of Cultivation Conditions and Influence of Three Donor Stool Samples

Establishment of an In Vitro System of the Human Intestinal Microbiota: Effect of Cultivation Conditions and Influence of Three Donor Stool Samples

Decreased Ecological Resistance of the Gut Microbiota in Response to Clindamycin Challenge in Mice Colonized with the Fungus Candida albicans

Establishment and Resilience of Transplanted Gut Microbiota in Aged Mice

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