Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia
ABSTRACT Bronchopulmonary dysplasia (BPD) is a common chronic lung condition in preterm infants that results in abnormal lung development and leads to considerable morbidity and mortality, making BPD one of the most common complications of preterm birth. We employed RNA sequencing and 16S rRNA gene...
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American Society for Microbiology
2019
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oai:doaj.org-article:8f95692957334507bf7d34c0ff0e5d822021-12-02T18:15:44ZChanges in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia10.1128/mSystems.00484-192379-5077https://doaj.org/article/8f95692957334507bf7d34c0ff0e5d822019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00484-19https://doaj.org/toc/2379-5077ABSTRACT Bronchopulmonary dysplasia (BPD) is a common chronic lung condition in preterm infants that results in abnormal lung development and leads to considerable morbidity and mortality, making BPD one of the most common complications of preterm birth. We employed RNA sequencing and 16S rRNA gene sequencing to profile gene expression in blood and the composition of the fecal microbiota in infants born at <29 weeks gestational age and diagnosed with BPD in comparison to those of preterm infants that were not diagnosed with BPD. 16S rRNA gene sequencing, performed longitudinally on 255 fecal samples collected from 50 infants in the first months of life, identified significant differences in the relative levels of abundance of Klebsiella, Salmonella, Escherichia/Shigella, and Bifidobacterium in the BPD infants in a manner that was birth mode dependent. Transcriptome sequencing (RNA-Seq) analysis revealed that more than 400 genes were upregulated in infants with BPD. Genes upregulated in BPD infants were significantly enriched for functions related to red blood cell development and oxygen transport, while several immune-related pathways were downregulated. We also identified a gene expression signature consistent with an enrichment of immunosuppressive CD71+ early erythroid cells in infants with BPD. Intriguingly, genes that were correlated in their expression with the relative abundances of specific taxa in the microbiota were significantly enriched for roles in the immune system, suggesting that changes in the microbiota might influence immune gene expression systemically. IMPORTANCE Bronchopulmonary dysplasia (BPD) is a serious inflammatory condition of the lung and is the most common complication associated with preterm birth. A large body of evidence now suggests that the gut microbiota can influence immunity and inflammation systemically; however, the role of the gut microbiota in BPD has not been evaluated to date. Here, we report that there are significant differences in the gut microbiota of infants born at <29 weeks gestation and subsequently diagnosed with BPD, which are particularly pronounced when infants are stratified by birth mode. We also show that erythroid and immune gene expression levels are significantly altered in BPD infants. Interestingly, we identified an association between the composition of the microbiota and immune gene expression in blood in early life. Together, these findings suggest that the composition of the microbiota may influence the risk of developing BPD and, more generally, may shape systemic immune gene expression.Feargal J. RyanDamian P. DrewChloe DouglasLex E. X. LeongMax MoldovanMiriam LynnNaomi FinkAnastasia SribnaiaIrmeli PenttilaAndrew J. McPheeCarmel T. CollinsMaria MakridesRobert A. GibsonGeraint B. RogersDavid J. LynnAmerican Society for MicrobiologyarticleBPDRNA-SeqVLBWfecal organismsmicrobiotaneonatesMicrobiologyQR1-502ENmSystems, Vol 4, Iss 5 (2019) |
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BPD RNA-Seq VLBW fecal organisms microbiota neonates Microbiology QR1-502 |
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BPD RNA-Seq VLBW fecal organisms microbiota neonates Microbiology QR1-502 Feargal J. Ryan Damian P. Drew Chloe Douglas Lex E. X. Leong Max Moldovan Miriam Lynn Naomi Fink Anastasia Sribnaia Irmeli Penttila Andrew J. McPhee Carmel T. Collins Maria Makrides Robert A. Gibson Geraint B. Rogers David J. Lynn Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| description |
ABSTRACT Bronchopulmonary dysplasia (BPD) is a common chronic lung condition in preterm infants that results in abnormal lung development and leads to considerable morbidity and mortality, making BPD one of the most common complications of preterm birth. We employed RNA sequencing and 16S rRNA gene sequencing to profile gene expression in blood and the composition of the fecal microbiota in infants born at <29 weeks gestational age and diagnosed with BPD in comparison to those of preterm infants that were not diagnosed with BPD. 16S rRNA gene sequencing, performed longitudinally on 255 fecal samples collected from 50 infants in the first months of life, identified significant differences in the relative levels of abundance of Klebsiella, Salmonella, Escherichia/Shigella, and Bifidobacterium in the BPD infants in a manner that was birth mode dependent. Transcriptome sequencing (RNA-Seq) analysis revealed that more than 400 genes were upregulated in infants with BPD. Genes upregulated in BPD infants were significantly enriched for functions related to red blood cell development and oxygen transport, while several immune-related pathways were downregulated. We also identified a gene expression signature consistent with an enrichment of immunosuppressive CD71+ early erythroid cells in infants with BPD. Intriguingly, genes that were correlated in their expression with the relative abundances of specific taxa in the microbiota were significantly enriched for roles in the immune system, suggesting that changes in the microbiota might influence immune gene expression systemically. IMPORTANCE Bronchopulmonary dysplasia (BPD) is a serious inflammatory condition of the lung and is the most common complication associated with preterm birth. A large body of evidence now suggests that the gut microbiota can influence immunity and inflammation systemically; however, the role of the gut microbiota in BPD has not been evaluated to date. Here, we report that there are significant differences in the gut microbiota of infants born at <29 weeks gestation and subsequently diagnosed with BPD, which are particularly pronounced when infants are stratified by birth mode. We also show that erythroid and immune gene expression levels are significantly altered in BPD infants. Interestingly, we identified an association between the composition of the microbiota and immune gene expression in blood in early life. Together, these findings suggest that the composition of the microbiota may influence the risk of developing BPD and, more generally, may shape systemic immune gene expression. |
| format |
article |
| author |
Feargal J. Ryan Damian P. Drew Chloe Douglas Lex E. X. Leong Max Moldovan Miriam Lynn Naomi Fink Anastasia Sribnaia Irmeli Penttila Andrew J. McPhee Carmel T. Collins Maria Makrides Robert A. Gibson Geraint B. Rogers David J. Lynn |
| author_facet |
Feargal J. Ryan Damian P. Drew Chloe Douglas Lex E. X. Leong Max Moldovan Miriam Lynn Naomi Fink Anastasia Sribnaia Irmeli Penttila Andrew J. McPhee Carmel T. Collins Maria Makrides Robert A. Gibson Geraint B. Rogers David J. Lynn |
| author_sort |
Feargal J. Ryan |
| title |
Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| title_short |
Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| title_full |
Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| title_fullStr |
Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| title_full_unstemmed |
Changes in the Composition of the Gut Microbiota and the Blood Transcriptome in Preterm Infants at Less than 29 Weeks Gestation Diagnosed with Bronchopulmonary Dysplasia |
| title_sort |
changes in the composition of the gut microbiota and the blood transcriptome in preterm infants at less than 29 weeks gestation diagnosed with bronchopulmonary dysplasia |
| publisher |
American Society for Microbiology |
| publishDate |
2019 |
| url |
https://doaj.org/article/8f95692957334507bf7d34c0ff0e5d82 |
| work_keys_str_mv |
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