Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort
Abstract Background Bacteria colonizing the nasopharynx play a key role as gatekeepers of respiratory health. Yet, dynamics of early life nasopharyngeal (NP) bacterial profiles remain understudied in low- and middle-income countries (LMICs), where children have a high prevalence of risk factors for...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-06-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01563-5 |
| _version_ | 1797806592985399296 |
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| author | Shantelle Claassen-Weitz Sugnet Gardner-Lubbe Yao Xia Kilaza S. Mwaikono Stephanie Harris Mounaud William C. Nierman Lesley Workman Heather J. Zar Mark P. Nicol |
| author_facet | Shantelle Claassen-Weitz Sugnet Gardner-Lubbe Yao Xia Kilaza S. Mwaikono Stephanie Harris Mounaud William C. Nierman Lesley Workman Heather J. Zar Mark P. Nicol |
| author_sort | Shantelle Claassen-Weitz |
| collection | DOAJ |
| description | Abstract Background Bacteria colonizing the nasopharynx play a key role as gatekeepers of respiratory health. Yet, dynamics of early life nasopharyngeal (NP) bacterial profiles remain understudied in low- and middle-income countries (LMICs), where children have a high prevalence of risk factors for lower respiratory tract infection. We investigated longitudinal changes in NP bacterial profiles, and associated exposures, among healthy infants from low-income households in South Africa. Methods We used short fragment (V4 region) 16S rRNA gene amplicon sequencing to characterize NP bacterial profiles from 103 infants in a South African birth cohort, at monthly intervals from birth through the first 12 months of life and six monthly thereafter until 30 months. Results Corynebacterium and Staphylococcus were dominant colonizers at 1 month of life; however, these were rapidly replaced by Moraxella- or Haemophilus-dominated profiles by 4 months. This succession was almost universal and largely independent of a broad range of exposures. Warm weather (summer), lower gestational age, maternal smoking, no day-care attendance, antibiotic exposure, or low height-for-age z score at 12 months were associated with higher alpha and beta diversity. Summer was also associated with higher relative abundances of Staphylococcus, Streptococcus, Neisseria, or anaerobic gram-negative bacteria, whilst spring and winter were associated with higher relative abundances of Haemophilus or Corynebacterium, respectively. Maternal smoking was associated with higher relative abundances of Porphyromonas. Antibiotic therapy (or isoniazid prophylaxis for tuberculosis) was associated with higher relative abundance of anerobic taxa (Porphyromonas, Fusobacterium, and Prevotella) and with lower relative abundances of health associated-taxa Corynebacterium and Dolosigranulum. HIV-exposure was associated with higher relative abundances of Klebsiella or Veillonella and lower relative abundances of an unclassified genus within the family Lachnospiraceae. Conclusions In this intensively sampled cohort, there was rapid and predictable replacement of early profiles dominated by health-associated Corynebacterium and Dolosigranulum with those dominated by Moraxella and Haemophilus, independent of exposures. Season and antibiotic exposure were key determinants of NP bacterial profiles. Understudied but highly prevalent exposures prevalent in LMICs, including maternal smoking and HIV-exposure, were associated with NP bacterial profiles. Video Abstract |
| first_indexed | 2024-03-13T06:09:36Z |
| format | Article |
| id | doaj.art-a3be366c074744a08e27d1b269abd271 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-13T06:09:36Z |
| publishDate | 2023-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-a3be366c074744a08e27d1b269abd2712023-06-11T11:20:20ZengBMCMicrobiome2049-26182023-06-0111112110.1186/s40168-023-01563-5Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohortShantelle Claassen-Weitz0Sugnet Gardner-Lubbe1Yao Xia2Kilaza S. Mwaikono3Stephanie Harris Mounaud4William C. Nierman5Lesley Workman6Heather J. Zar7Mark P. Nicol8Division of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape TownDepartment of Statistics and Actuarial Science, Faculty of Economic and Management Sciences, Stellenbosch UniversityMarshall Centre, Division of Infection and Immunity, School of Biomedical Sciences, University of Western AustraliaComputational Biology Group and H3ABioNet, Department of Integrative Biomedical Sciences, University of Cape TownJ. Craig Venter InstituteJ. Craig Venter InstituteDepartment of Paediatrics and Child Health, Red Cross War Memorial Children’s HospitalDepartment of Paediatrics and Child Health, Red Cross War Memorial Children’s HospitalDivision of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape TownAbstract Background Bacteria colonizing the nasopharynx play a key role as gatekeepers of respiratory health. Yet, dynamics of early life nasopharyngeal (NP) bacterial profiles remain understudied in low- and middle-income countries (LMICs), where children have a high prevalence of risk factors for lower respiratory tract infection. We investigated longitudinal changes in NP bacterial profiles, and associated exposures, among healthy infants from low-income households in South Africa. Methods We used short fragment (V4 region) 16S rRNA gene amplicon sequencing to characterize NP bacterial profiles from 103 infants in a South African birth cohort, at monthly intervals from birth through the first 12 months of life and six monthly thereafter until 30 months. Results Corynebacterium and Staphylococcus were dominant colonizers at 1 month of life; however, these were rapidly replaced by Moraxella- or Haemophilus-dominated profiles by 4 months. This succession was almost universal and largely independent of a broad range of exposures. Warm weather (summer), lower gestational age, maternal smoking, no day-care attendance, antibiotic exposure, or low height-for-age z score at 12 months were associated with higher alpha and beta diversity. Summer was also associated with higher relative abundances of Staphylococcus, Streptococcus, Neisseria, or anaerobic gram-negative bacteria, whilst spring and winter were associated with higher relative abundances of Haemophilus or Corynebacterium, respectively. Maternal smoking was associated with higher relative abundances of Porphyromonas. Antibiotic therapy (or isoniazid prophylaxis for tuberculosis) was associated with higher relative abundance of anerobic taxa (Porphyromonas, Fusobacterium, and Prevotella) and with lower relative abundances of health associated-taxa Corynebacterium and Dolosigranulum. HIV-exposure was associated with higher relative abundances of Klebsiella or Veillonella and lower relative abundances of an unclassified genus within the family Lachnospiraceae. Conclusions In this intensively sampled cohort, there was rapid and predictable replacement of early profiles dominated by health-associated Corynebacterium and Dolosigranulum with those dominated by Moraxella and Haemophilus, independent of exposures. Season and antibiotic exposure were key determinants of NP bacterial profiles. Understudied but highly prevalent exposures prevalent in LMICs, including maternal smoking and HIV-exposure, were associated with NP bacterial profiles. Video Abstracthttps://doi.org/10.1186/s40168-023-01563-516S rRNA geneBirth cohortMicrobiomeHigh-throughput sequencingInfantLongitudinal |
| spellingShingle | Shantelle Claassen-Weitz Sugnet Gardner-Lubbe Yao Xia Kilaza S. Mwaikono Stephanie Harris Mounaud William C. Nierman Lesley Workman Heather J. Zar Mark P. Nicol Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort Microbiome 16S rRNA gene Birth cohort Microbiome High-throughput sequencing Infant Longitudinal |
| title | Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort |
| title_full | Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort |
| title_fullStr | Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort |
| title_full_unstemmed | Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort |
| title_short | Succession and determinants of the early life nasopharyngeal microbiota in a South African birth cohort |
| title_sort | succession and determinants of the early life nasopharyngeal microbiota in a south african birth cohort |
| topic | 16S rRNA gene Birth cohort Microbiome High-throughput sequencing Infant Longitudinal |
| url | https://doi.org/10.1186/s40168-023-01563-5 |
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