Editorial: Xenobiotics from diet and health: impact on microbiome
David Ríos-Covian1 
Maria Carmen Collado2 
Carina Venter3 
Carlos Gómez-Gallego4 
Clara G. de los Reyes-Gavilán5,6 
Sonia González6,7*- 1Equipe Interactions des Micro-organismes Commensaux et Probiotiques avec l'Hôte, Institute MICALIS, National Research Institute for Agriculture, Food and the Environment, Univ Paris Saclay, Paris, France
- 2Department of Biotechnology, Institute of Agrochemistry and Food Technology-National Research Council, Valencia, Spain
- 3Section of Allergy and Immunology, Department of Pediatrics, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, CO, United States
- 4Department of Pediatrics, Institute of Public Health and Clinical Nutrition, University of Eastern Finland, Kuopio, Finland
- 5Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias (IPLA-Spanish National Research Council), Villaviciosa, Spain
- 6Diet, Microbiota, and Health Group, Instituto de Investigación Sanitaria del Principado de Asturias (DIMISA, Health Research Institute of Asturias), Oviedo, Spain
- 7Department of Functional Biology, Faculty of Medicine, University of Oviedo, Oviedo, Spain
Editorial on the Research Topic
Xenobiotics from diet and health: impact on microbiome
Introduction
This Research Topic collects studies that assess the impact of different dietary components on the composition of the gut microbiota. Although sensu stricto the term “xenobiotic” refers to a chemical substance found in an organism that is not naturally produced or expected to be present in that organism, it is also commonly applied to substances with possible toxic or carcinogenic action, such as environmental pollutants or pesticides (1). It has been estimated that humans are exposed to 1–3 million xenobiotics during their lifetime, so this plethora of compounds makes this an attractive and emerging field of study (1).
The majority of the substances that fall under the term xenobiotic have become relevant because of the changes in our dietary patterns over the past few years, with a remarkable increase in food processing, but also as a result of the application of certain techniques that enhance the palatability of foodstuffs. This is the case of heterocyclic amines (HA), polycyclic aromatic hydrocarbons (PAH), acrylamides generated by cooking food at high temperatures, or glycation end products (AGEs) (2–4). The latter are formed by non-enzymatic reactions between carbonyl groups of reducing sugars and free amino groups in foods cooked at high temperatures or stored for long periods (5). The increase in the concentration of these compounds in the body is directly associated with the degree of inflammation, the formation of free radicals, insulin resistance, and metabolic disturbances (4). In this regard, the article by Park et al. evaluates the impact of a strain of Lactococcus lactis isolated from kimchi (LL-KF140) on the toxicokinetics of Nε-(carboxymethyl)lysine (CML), one of the most abundant glycosylation end products in foods. The paper includes data from an in vitro assay to test the efficacy of eight enzymes produced by strain LL-KF140 in reducing CML after 24 h of incubation, an in vivo study in a rat model treated with CML as a casein-lactose reaction product, and the bacteria administered for 14 d. These researchers also carried out a clinical trial in humans, who received the bacteria for 26 d together with CML administered in 40 g of parmesan cheese. The results presented in this work contribute to expanding the still-limited knowledge about the role of Lactobacilli as detoxifiers of compounds that may be harmful to human health.
Similarly, Zapico et al. have evaluated the impact of exposure to various food cooking by-products in the diet of a sample of socially vulnerable individuals on the composition and activity of the gut microbiota. The regular diet of the subjects leads to the intake of a variety of heterocyclic amines, nitrates, nitrites, nitrosocompounds, polycyclic aromatic hydrocarbons, and acrylamide. A comparison of xenobiotic intake with fecal microbiota composition revealed that the Pseudomonadota and Verrucomicrobiota phyla showed significant correlations with the intake of some xenobiotics (heterocyclic amines, polycyclic aromatic hydrocarbons, and nitrates). In addition, MelQx had a negative association with the microbial families Lachnospiraceae and Eggerthellaceae, while PhIP was related to the relative abundance of the Muribaculceae, Streptococcaceae, and Eubacterium coprostanoligenes groups. These results support the possible association between xenobiotics derived from food processing and gut microbiota composition.
The work of Liu et al. addresses another important aspect of this complex relationship between diet and microbiota. Several studies in recent years have found differences in the composition of the microbiota according to gender (6). However, these researchers go a step further by studying the different responses in terms of microbiota composition after the administration of the macromolecular polysaccharide Inonotus obliquus polysaccharide (IOP) in male and female rats (Liu et al.). For this purpose, they determined the molecular weight and purity of IOP by high-performance gel permeation chromatography (HPGPC) and the phenol sulfuric acid method, with NMR used to confirm the chemical structure of IOP. Sex hormone [testosterone (T) and estradiol (E2)] levels and intestinal microbial changes were detected by enzyme-linked immunosorbent assay (ELISA) and 16S rRNA, respectively, after IOP (100 mg/kg) gavage in male and female Sprague-Dawley (SD) rats. It was observed that IOP induced apoptosis in a dose-dependent manner, with 46.19% of apoptosis occurring at high doses. In the rat model, the administration of IOP was associated with an increase in the levels of the hormone E2 in male rats with respect to the control. IOP was associated with the increased abundance of Lactobacillus, Roseburia, and Clostridia_UGC-014 in female rats, whereas in male rats, the genera Prevotella, Alistipes, and Clostridia_UGC-014 were increased. Thus, this study supports the existing knowledge of the IOP structure and elucidates the modifications that occur in the intestinal microbiota following IOP administration in rats of both sexes.
The present Research Topic and special edition are concluded with a review by Muratore et al. on nutritional modulation of the microbiome in recipients of allogeneic hematopoietic stem cell transplantation. Allogeneic hematopoietic stem cell transplantation (allo-HSCT), used as a treatment for various oncologic and non-oncologic diseases, is associated with high morbidity and mortality. In this work, the authors propose that intestinal dysbiosis may lead to complications that could increase the risk of mortality. This reinforces the interest in identifying different nutritional strategies to improve the quality of life in cancer patients and reduce the risk of mortality through modulation of the intestinal microbiota. In this article, a complete overview of how the pre-transplant diet could affect the composition of the microbiome and its ability to resist the alterations that occur during transplantation is provided. This emphasizes the importance of enteral or parenteral nutrition (7, 8).
Conclusion
The results reported in this Research Topic, together with those that will be developed from them, will allow the discovery of different compounds with the ability to modulate the intestinal microbiota and decipher the mechanisms that explain this interaction. This will be the first step toward the development of new dietary strategies capable of counteracting the potential adverse effects that these compounds may have. This compendium of work highlights the importance of future assessment of the relationship between xenobiotic intake and microbiota composition, as recently reported by the European Food Safety Agency (9).
Author contributions
DR-C: Writing – review & editing. MC: Writing – review & editing. CV: Writing – review & editing. CG-G: Writing – review & editing. CR-G: Conceptualization, Writing – review & editing. SG: Conceptualization, Writing – original draft, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was funded by Project RTI2018-098288-B-I00 (acronym MIXED), financed by MCIN/AEI/10.13039/501100011033/FEDER, “Una manera de hacer Europa” and the Grant PID2022-140410OB-I00, funded by MCIN/AEI/10.13039/501100011033/FEDER “A way of making Europe”.
Acknowledgments
We deeply thank all the authors and reviewers who have participated in this Research Topic. We also thank the editorial board for their support.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
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References
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Keywords: xenobiotics, detoxicant, probiotics, Lactobacillus, nitrosocompounds, macromolecular polysaccharide
Citation: Ríos-Covian D, Collado MC, Venter C, Gómez-Gallego C, de los Reyes-Gavilán CG and González S (2024) Editorial: Xenobiotics from diet and health: impact on microbiome. Front. Nutr. 10:1342142. doi: 10.3389/fnut.2023.1342142
Received: 21 November 2023; Accepted: 06 December 2023;
Published: 04 January 2024.
Edited and reviewed by: Christophe Lacroix, ETH Zürich, Switzerland
Copyright © 2024 Ríos-Covian, Collado, Venter, Gómez-Gallego, de los Reyes-Gavilán and González. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Sonia González, soniagsolares@uniovi.es