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Distribution of Bacterial 1,3-Galactosyltransferase Genes In Distribution of Bacterial α1,3-Galactosyltransferase Genes in the Human Gut Microbiome Emmanuel Montassier, Gabriel Al-Ghalith, Camille Mathé, Quentin Le Bastard, Venceslas Douillard, Abel Garnier, Rémi Guimon, Bastien Raimondeau, Yann Touchefeu, Emilie Duchalais, et al. To cite this version: Emmanuel Montassier, Gabriel Al-Ghalith, Camille Mathé, Quentin Le Bastard, Venceslas Douillard, et al.. Distribution of Bacterial α1,3-Galactosyltransferase Genes in the Human Gut Microbiome. Frontiers in Immunology, Frontiers, 2020, 10, pp.3000. 10.3389/fimmu.2019.03000. inserm-02490517 HAL Id: inserm-02490517 https://www.hal.inserm.fr/inserm-02490517 Submitted on 25 Feb 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. ORIGINAL RESEARCH published: 13 January 2020 doi: 10.3389/fimmu.2019.03000 Distribution of Bacterial α1,3-Galactosyltransferase Genes in the Human Gut Microbiome Emmanuel Montassier 1,2,3, Gabriel A. Al-Ghalith 4, Camille Mathé 5,6, Quentin Le Bastard 1,3, Venceslas Douillard 5,6,7, Abel Garnier 5,6,7, Rémi Guimon 5,6,7, Bastien Raimondeau 5,6, Yann Touchefeu 8,9, Emilie Duchalais 8,9, Nicolas Vince 5,6, Sophie Limou 5,6, Pierre-Antoine Gourraud 5,6,7, David A. Laplaud 5,10, Arnaud B. Nicot 5,6, Jean-Paul Soulillou 5,6*† and Laureline Berthelot 5,6*† 1 Microbiota Hosts Antibiotics and bacterial Resistances (MiHAR), Université de Nantes, Nantes, France, 2 Laboratoire EA3826 Thérapeutiques cliniques et expérimentales des infections IRS2 Nantes Biotech, Université de Nantes, Nantes, France, 3 Department of Emergency Medicine, CHU de Nantes, Nantes, France, 4 Bioinformatics and Computational Biology, University of Minnesota, Minneapolis, MN, United States, 5 Centre de Recherche en Transplantation et Immunologie UMR 6 Edited by: 1064, INSERM, Université de Nantes, Nantes, France, Institut de Transplantation Urologie Néphrologie (ITUN), CHU de 7 Jia Sun, Nantes, Nantes, France, CHU de Nantes, CIC 1413, Pôle Hospitalo-Universitaire 11 Santé Publique, Clinique des données, 8 9 Jiangnan University, China Nantes, France, Institut des Maladies de l’Appareil Digestif, CHU Nantes, Nantes, France, INSERM U1235, Nantes, France, 10 Neurology department, CIC Neurology, CHU de Nantes, Nantes, France Reviewed by: Runmin Wei, University of Texas MD Anderson Because of a loss-of-function mutation in the GGTA1 gene, humans are unable to Cancer Center, United States synthetize α1,3-Galactose (Gal) decorated glycans and develop high levels of circulating Xi Ma, China Agricultural University anti-α1,3-Galactose antibodies (anti-Gal Abs). Anti-Gal Abs have been identified as a (CAU), China major obstacle of organ xenotransplantation and play a role in several host-pathogen *Correspondence: relationships including potential susceptibility to infection. Anti-Gal Abs are supposed Jean-Paul Soulillou [email protected] to stem from immunization against the gut microbiota, an assumption derived from Laureline Berthelot the observation that some pathogens display α1,3-Gal and that antibiotic treatment [email protected] decreases the level of anti-Gal. However, there is little information to date concerning †These authors have contributed the microorganisms producing α1,3-Gal in the human gut microbiome. Here, available equally to this work α1,3-Galactosyltransferase (GT) gene sequences from gut bacteria were selectively Specialty section: quantified for the first time in the gut microbiome shotgun sequences of 163 adult This article was submitted to individuals from three published population-based metagenomics analyses. We showed Nutritional Immunology, that most of the gut microbiome of adult individuals contained a small set of bacteria a section of the journal Frontiers in Immunology bearing α1,3-GT genes. These bacteria belong mainly to the Enterobacteriaceae family, Received: 25 June 2019 including Escherichia coli, but also to Pasteurellaceae genera, Haemophilus influenza and Accepted: 06 December 2019 Lactobacillus species. α1,3-Gal antigens and α1,3-GT activity were detected in healthy Published: 13 January 2020 stools of individuals exhibiting α1,3-GT bacterial gene sequences in their shotgun data. Citation: Montassier E, Al-Ghalith GA, Mathé C, Keywords: intestinal microbiome, α1,3-Galactosyltransferase, α1,3-Gal antigen, shotgun data, enterobacteriaceae Le Bastard Q, Douillard V, Garnier A, Guimon R, Raimondeau B, Touchefeu Y, Duchalais E, Vince N, INTRODUCTION Limou S, Gourraud P-A, Laplaud DA, Nicot AB, Soulillou J-P and Human beings and old-world primates are unable to express the α1,3-Galactose epitope because of Berthelot L (2020) Distribution of α Bacterial α1,3-Galactosyltransferase a loss-of-function mutation in the GGTA1 gene (Glycoprotein 1,3-Galactosyltransferase 1) coding Genes in the Human Gut Microbiome. α1,3GalactosylTransferase [see (1) for review]. As such, humans develop anti-α1,3-Galactose Front. Immunol. 10:3000. (anti-Gal) antibodies (Abs) supposed to result from an immune response to gut microbiota within doi: 10.3389/fimmu.2019.03000 the first year of life (2, 3). Frontiers in Immunology | www.frontiersin.org 1 January 2020 | Volume 10 | Article 3000 Montassier et al. α1,3-Galactosyltransferase in Gut Microbiome Humans have high levels of circulating Abs directed against We also analyzed data of a second and more recent shotgun- the α1,3-Gal epitope, with more than 1% of B-cells exhibiting a sequencing project from the LifeLines-DEEP cohort. The raw membrane receptor devoted to α1,3-Gal recognition (4). Anti- sequence data from this Dutch population-based cohort are Gal Abs have been identified in the 1980s as the main barrier to available from the European genome-phenome archive (https:// vascularized organ xeno-transplantation, where they act as the www.ebi.ac.uk/ega) at accession number EGAS00001001704. major etiological component of hyper-acute vascular xenograft We randomly selected 57 individuals in the database and rejection (5), which does not occur if the transplant comes analyzed raw sequences downloaded from the EGA. We then from GGTA1 KO pigs (6). Anti-Gal Abs in humans have also analyzed a shotgun metagenomic DNA sequencing dataset of been proposed as protective against a variety of Gal-positive 20 samples from Hmong in Thailand (n = 15), Karen in microorganisms (7, 8) or viruses budding from non-human Thailand (n = 5) from a multi-generational Asian American host cells (9) and likely contribute to several host-pathogen cohort (21). relationships, also including potential infection susceptibility. Anti-Gal may also play a role in some auto-immune processes. α Patients with multiple sclerosis, with lower circulating titers of 1,3-GalactosylTransferase Gene anti-Gal Abs (10) and with dysbiosis of the gut microbiota, may Sequences lack bacteria able to synthetize the α1,3-Gal epitope in their The gene sequences encoding α1,3-GalactosylTransferase microbiota (11). (α1,3GT) enzymes were collected from the Bioinformatics Importantly, presence of the α1,3-Gal epitope has been Resource Portal ExPASy (https://enzyme.expasy.org/EC/2.4. detected in engineered animal devices such as porcine or bovine 1.87). We also collected all gene sequences corresponding to biological heart valves (BHV) (12), and anti-Gal Abs may play a α1,3GT among the 4,800 described genomes of bacteria in the role in late valve deterioration, a major limitation of the success Kyoto Encyclopedia of Genes and Genomes (KEGG) (https:// of BHV implantation in young adults. Thus, the level and type of www.genome.jp/kegg/) and the gene sequences coding α1,3GT microbiota able to synthetize the α1,3-Gal epitope may represent proteins in UniProt (https://www.uniprot.org/). Evolution has a key environmental factor controlling several pathological provided a high diversity of enzymes able to create the branched processes. The knowledge of the micro-organisms producing the α1,3 position in galactose, which can stimulate an immune α1,3-Gal antigens eliciting and maintaining blood anti-Gal levels response in humans. Supplementary Table 1 (also commented may allow for the design of strategies to accordingly modulate in the result section) provides the final list of sequences submitted antibody titers in some pathological states. for bioinformatics analysis. It is known that several bacteria are able to synthetize α1,3- Gal sugars (13) such as Klebsiella pneumonia (14), Escherichia α coli (15), Salmonella (16), or Serratia marcescens (17) and that 1,3GalactosylTransferase Phylogenic Tree antibiotics can decrease the levels of blood anti-Gal in an Building experimental model (18). Yet, there is little information on which We retrieved 193 bacterial gene sequences of the α1,3GT from the α1,3-Gal positive bacteria in the human gut microbiome initiate KEGG and UniProt databases by using α1,3GT-related keywords the primary response against the α1,3-Gal epitope in the first year and manually curated the obtained list (Supplementary Table 1). of life, or which bacteria likely sustain the high level of anti-Gal We found 55 duplicates of nucleotide sequences, 45 of which antibodies in adults (19). In this paper, we analyzed for the first coming from different strains of E. Coli; the 10 remaining time the spectrum of α1,3GalactosylTransferase (α1,3GT) gene sequences were duplicates from the same genus except one, sequences in bacteria from human gut microbiome samples of Acidaminococcus intestinis and Campylobacter lari. We removed 163 healthy adults using shotgun metagenomic analysis. the duplicates to conduct the alignment and the tree building as advised for these algorithms; the alignment was performed MATERIALS AND METHODS using Clustal Omega from the EMBL-EBI website (22, 23).
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