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Islet autoantibody seroconversion in type-1 diabetes is associated with metagenome-assembled genomes in infant gut microbiomes

Author

Listed:
  • Li Zhang

    (University of Oklahoma Health Sciences Center
    University of Oklahoma)

  • Karen R. Jonscher

    (University of Oklahoma Health Sciences Center
    University of Oklahoma Health Sciences Center)

  • Zuyuan Zhang

    (University of Oklahoma)

  • Yi Xiong

    (University of Oklahoma)

  • Ryan S. Mueller

    (Oregon State University)

  • Jacob E. Friedman

    (University of Oklahoma Health Sciences Center
    University of Oklahoma Health Sciences Center
    University of Oklahoma Health Sciences Center)

  • Chongle Pan

    (University of Oklahoma Health Sciences Center
    University of Oklahoma
    University of Oklahoma)

Abstract

The immune system of some genetically susceptible children can be triggered by certain environmental factors to produce islet autoantibodies (IA) against pancreatic β cells, which greatly increases their risk for Type-1 diabetes. An environmental factor under active investigation is the gut microbiome due to its important role in immune system education. Here, we study gut metagenomes that are de-novo-assembled in 887 at-risk children in the Environmental Determinants of Diabetes in the Young (TEDDY) project. Our results reveal a small set of core protein families, present in >50% of the subjects, which account for 64% of the sequencing reads. Time-series binning generates 21,536 high-quality metagenome-assembled genomes (MAGs) from 883 species, including 176 species that hitherto have no MAG representation in previous comprehensive human microbiome surveys. IA seroconversion is positively associated with 2373 MAGs and negatively with 1549 MAGs. Comparative genomics analysis identifies lipopolysaccharides biosynthesis in Bacteroides MAGs and sulfate reduction in Anaerostipes MAGs as functional signatures of MAGs with positive IA-association. The functional signatures in the MAGs with negative IA-association include carbohydrate degradation in lactic acid bacteria MAGs and nitrate reduction in Escherichia MAGs. Overall, our results show a distinct set of gut microorganisms associated with IA seroconversion and uncovered the functional genomics signatures of these IA-associated microorganisms

Suggested Citation

  • Li Zhang & Karen R. Jonscher & Zuyuan Zhang & Yi Xiong & Ryan S. Mueller & Jacob E. Friedman & Chongle Pan, 2022. "Islet autoantibody seroconversion in type-1 diabetes is associated with metagenome-assembled genomes in infant gut microbiomes," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31227-1
    DOI: 10.1038/s41467-022-31227-1
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    1. Christopher J. Stewart & Nadim J. Ajami & Jacqueline L. O’Brien & Diane S. Hutchinson & Daniel P. Smith & Matthew C. Wong & Matthew C. Ross & Richard E. Lloyd & HarshaVardhan Doddapaneni & Ginger A. M, 2018. "Temporal development of the gut microbiome in early childhood from the TEDDY study," Nature, Nature, vol. 562(7728), pages 583-588, October.
    2. Tommi Vatanen & Eric A. Franzosa & Randall Schwager & Surya Tripathi & Timothy D. Arthur & Kendra Vehik & Åke Lernmark & William A. Hagopian & Marian J. Rewers & Jin-Xiong She & Jorma Toppari & Anette, 2018. "The human gut microbiome in early-onset type 1 diabetes from the TEDDY study," Nature, Nature, vol. 562(7728), pages 589-594, October.
    3. Stephen Nayfach & Zhou Jason Shi & Rekha Seshadri & Katherine S. Pollard & Nikos C. Kyrpides, 2019. "New insights from uncultivated genomes of the global human gut microbiome," Nature, Nature, vol. 568(7753), pages 505-510, April.
    4. Jordan T. Russell & Luiz F. W. Roesch & Malin Ördberg & Jorma Ilonen & Mark A. Atkinson & Desmond A. Schatz & Eric W. Triplett & Johnny Ludvigsson, 2019. "Genetic risk for autoimmunity is associated with distinct changes in the human gut microbiome," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    5. Brandon Brooks & Matthew R. Olm & Brian A. Firek & Robyn Baker & Brian C. Thomas & Michael J. Morowitz & Jillian F. Banfield, 2017. "Strain-resolved analysis of hospital rooms and infants reveals overlap between the human and room microbiome," Nature Communications, Nature, vol. 8(1), pages 1-7, December.
    6. Alexandre Almeida & Alex L. Mitchell & Miguel Boland & Samuel C. Forster & Gregory B. Gloor & Aleksandra Tarkowska & Trevor D. Lawley & Robert D. Finn, 2019. "A new genomic blueprint of the human gut microbiota," Nature, Nature, vol. 568(7753), pages 499-504, April.
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