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Neonatal gut and respiratory microbiota: coordinated development through time and space

Alex Grier, View ORCID ProfileAndrew McDavid, Bokai Wang, Xing Qiu, James Java, Sanjukta Bandyopadhyay, Hongmei Yang, Jeanne Holden-Wiltse, Haeja A. Kessler, Ann L. Gill, Heidie Huyck, Ann R. Falsey, David J. Topham, Kristin M. Scheible, Mary T. Caserta, Gloria S. Pryhuber, Steven R. Gill
doi: https://doi.org/10.1101/247122
Alex Grier
1Genomics Research Center, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Andrew McDavid
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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  • ORCID record for Andrew McDavid
Bokai Wang
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Xing Qiu
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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James Java
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Sanjukta Bandyopadhyay
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Hongmei Yang
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Jeanne Holden-Wiltse
2Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Haeja A. Kessler
3Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Ann L. Gill
3Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Heidie Huyck
4Medicine-Infectious Disease, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Ann R. Falsey
4Medicine-Infectious Disease, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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David J. Topham
3Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
5Center for Vaccine Biology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Kristin M. Scheible
6Division of Neonatology, Department of Pediatrics, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Mary T. Caserta
7Division of Infectious Disease, Department of Pediatrics, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Gloria S. Pryhuber
6Division of Neonatology, Department of Pediatrics, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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Steven R. Gill
1Genomics Research Center, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
3Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
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  • For correspondence: steven_gill@urmc.rochester.edu
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ABSTRACT

Background: Postnatal development of the microbiota in early life influences immunity, metabolism, neurodevelopment and long-term infant health. Microbiome development occurs at multiple body sites, each with distinct community compositions and functions. Associations between microbiota at multiple sites represent an unexplored influence on the infant microbiome. Here, we examined co-occurrence patterns of gut and respiratory microbiota in pre- and full-term infants over the first year of life, a period critical to neonatal development and risk of respiratory diseases.

Results: Gut and respiratory microbiota collected as longitudinal rectal, throat and nasal samples from 38 pre-term and 44 full-term infants were first clustered into community state types (CSTs) on the basis of their composition. Multiple methods were used to relate the occurrence of CSTs to several measures of infant maturity, including gestational age (GA) at birth, week of life (WOL), and post menstrual age (PMA: equal to GA plus WOL). Manifestation of CSTs followed one of three patterns with respect to infant maturity. First, chronological: independent of infant maturity (GA) at birth, and strongly associated with post-natal age (WOL). Second, idiosyncratic: primarily dependent on maturity (GA) at birth, with persistent differences in CST occurrence between pre- and full-term infants through the first year of life. Third, convergent: CSTs appear earlier in infants with greater maturity (GA) at birth, but after a sufficient post-natal interval their occurrence in pre-term infants reaches parity with full-term infants. The composition of CSTs was highly dissimilar between different body sites, but the CST of any one body site was highly predictive of the CSTs at other body sites. There were significant associations between the abundance of individual taxa at each body site and the CSTs of the other body sites, which persisted after stringent control for the non-linear effects of infant maturity. Significant canonical correlations exist between the microbiota composition at each pair of body sites, with the strongest correlations between more proximal locations.

Conclusion: Cross-body site associations of developing infant microbiota suggest the importance of research and clinical practices that focus on dynamic interactions between multiple microbial communities to elucidate and promote systemic microbiota development.

  • LIST OF ABBREVIATIONS

    GA
    gestational age
    PMA
    premenstrual age
    WOL
    week of life
    CST
    community state type
    OTU
    operational taxonomic units
    FDR
    false discovery rate
    NICU
    neonatal intensive care unit
  • Copyright 
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    Posted January 19, 2018.
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    Neonatal gut and respiratory microbiota: coordinated development through time and space
    Alex Grier, Andrew McDavid, Bokai Wang, Xing Qiu, James Java, Sanjukta Bandyopadhyay, Hongmei Yang, Jeanne Holden-Wiltse, Haeja A. Kessler, Ann L. Gill, Heidie Huyck, Ann R. Falsey, David J. Topham, Kristin M. Scheible, Mary T. Caserta, Gloria S. Pryhuber, Steven R. Gill
    bioRxiv 247122; doi: https://doi.org/10.1101/247122
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    Neonatal gut and respiratory microbiota: coordinated development through time and space
    Alex Grier, Andrew McDavid, Bokai Wang, Xing Qiu, James Java, Sanjukta Bandyopadhyay, Hongmei Yang, Jeanne Holden-Wiltse, Haeja A. Kessler, Ann L. Gill, Heidie Huyck, Ann R. Falsey, David J. Topham, Kristin M. Scheible, Mary T. Caserta, Gloria S. Pryhuber, Steven R. Gill
    bioRxiv 247122; doi: https://doi.org/10.1101/247122

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