Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity
ABSTRACT The gut microbiome is a potentially important mechanism that links prenatal disaster exposures with increased disease risks. However, whether prenatal disaster exposures are associated with alterations in the infant’s gut microbiome remains unknown. We established a birth cohort study named...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mSphere |
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| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00134-23 |
| _version_ | 1797651062295887872 |
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| author | Ai Zhang David de Ángel Solá Midnela Acevedo Flores Lijuan Cao Leran Wang Josh G. Kim Phillip I. Tarr Barbara B. Warner Nicolás Rosario Matos Leyao Wang |
| author_facet | Ai Zhang David de Ángel Solá Midnela Acevedo Flores Lijuan Cao Leran Wang Josh G. Kim Phillip I. Tarr Barbara B. Warner Nicolás Rosario Matos Leyao Wang |
| author_sort | Ai Zhang |
| collection | DOAJ |
| description | ABSTRACT The gut microbiome is a potentially important mechanism that links prenatal disaster exposures with increased disease risks. However, whether prenatal disaster exposures are associated with alterations in the infant’s gut microbiome remains unknown. We established a birth cohort study named Hurricane as the Origin of Later Alterations in Microbiome (HOLA) after Hurricane Maria struck Puerto Rico in 2017. We enrolled vaginally born Latino term infants aged 2 to 6 months, including n = 29 infants who were exposed in utero to Hurricane Maria in Puerto Rico and n = 34 infants who were conceived at least 5 months after the hurricane as controls. Shotgun metagenomic sequencing was performed on infant stool swabs. Infants exposed in utero to Hurricane Maria had a reduced diversity in their gut microbiome compared to the control infants, which was mainly seen in the exclusively formula-fed group (P = 0.02). Four bacterial species, including Bacteroides vulgatus, Clostridium innocuum, Bifidobacterium pseudocatenulatum, and Clostridium neonatale, were depleted in the exposure group compared to the control group. Compositional differences in the microbial community and metabolic genes between the exposure and control groups were significant, which were driven by the formula feeding group (P = 0.02 for the microbial community and P = 0.008 for the metabolic genes). Metabolic modules involved in carbohydrate metabolism were reduced in the exposure group. Prenatal maternal exposure to Hurricane Maria was associated with a reduced gut commensal and an altered microbial composition and metabolic potential in the offspring’s gut. Breastfeeding can adjust the composition of the gut microbiomes of exposed infants. IMPORTANCE Climate change is a serious issue that is affecting human health. With more frequent and intense weather disasters due to climate change, there is an urgent need to evaluate and understand the impacts of prenatal disaster exposures on the offspring. The prenatal stage is a particularly vulnerable stage for disease origination. However, the impact of prenatal weather disaster exposures on the offspring’s gut microbiome has not been evaluated. Our HOLA study starts to fill this knowledge gap and provides novel insights into the microbiome as a mechanism that links prenatal disaster exposures with elevated disease risks. Our major finding that reduced microbial diversity and altered metabolic capacity are associated with prenatal hurricane exposures warrants further studies to evaluate the impact of weather disasters on the unborn. |
| first_indexed | 2024-03-11T16:09:37Z |
| format | Article |
| id | doaj.art-c1c0fbfcc47b431d8ff0cf6315e7416d |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-03-11T16:09:37Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-c1c0fbfcc47b431d8ff0cf6315e7416d2023-10-24T16:32:15ZengAmerican Society for MicrobiologymSphere2379-50422023-10-018510.1128/msphere.00134-23Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacityAi Zhang0David de Ángel Solá1Midnela Acevedo Flores2Lijuan Cao3Leran Wang4Josh G. Kim5Phillip I. Tarr6Barbara B. Warner7Nicolás Rosario Matos8Leyao Wang9Department of Medicine, Division of Allergy and Immunology, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Pediatrics, Yale University School of Medicine , New Haven, Connecticut, USADepartment of Pediatrics and Obstetrics and Gynecology, San Juan City Hospital Research Unit, San Juan Hospital , San Juan, Puerto RicoDepartment of Medicine, Division of Allergy and Immunology, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Medicine, Division of Infectious Diseases, Edison Family Center for Genome Sciences and Systems Biology, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Medicine, Division of Allergy and Immunology, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Pediatrics, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Pediatrics, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USADepartment of Pediatrics and Obstetrics and Gynecology, San Juan City Hospital Research Unit, San Juan Hospital , San Juan, Puerto RicoDepartment of Medicine, Division of Allergy and Immunology, Washington University School of Medicine in St. Louis , St. Louis, Missouri, USAABSTRACT The gut microbiome is a potentially important mechanism that links prenatal disaster exposures with increased disease risks. However, whether prenatal disaster exposures are associated with alterations in the infant’s gut microbiome remains unknown. We established a birth cohort study named Hurricane as the Origin of Later Alterations in Microbiome (HOLA) after Hurricane Maria struck Puerto Rico in 2017. We enrolled vaginally born Latino term infants aged 2 to 6 months, including n = 29 infants who were exposed in utero to Hurricane Maria in Puerto Rico and n = 34 infants who were conceived at least 5 months after the hurricane as controls. Shotgun metagenomic sequencing was performed on infant stool swabs. Infants exposed in utero to Hurricane Maria had a reduced diversity in their gut microbiome compared to the control infants, which was mainly seen in the exclusively formula-fed group (P = 0.02). Four bacterial species, including Bacteroides vulgatus, Clostridium innocuum, Bifidobacterium pseudocatenulatum, and Clostridium neonatale, were depleted in the exposure group compared to the control group. Compositional differences in the microbial community and metabolic genes between the exposure and control groups were significant, which were driven by the formula feeding group (P = 0.02 for the microbial community and P = 0.008 for the metabolic genes). Metabolic modules involved in carbohydrate metabolism were reduced in the exposure group. Prenatal maternal exposure to Hurricane Maria was associated with a reduced gut commensal and an altered microbial composition and metabolic potential in the offspring’s gut. Breastfeeding can adjust the composition of the gut microbiomes of exposed infants. IMPORTANCE Climate change is a serious issue that is affecting human health. With more frequent and intense weather disasters due to climate change, there is an urgent need to evaluate and understand the impacts of prenatal disaster exposures on the offspring. The prenatal stage is a particularly vulnerable stage for disease origination. However, the impact of prenatal weather disaster exposures on the offspring’s gut microbiome has not been evaluated. Our HOLA study starts to fill this knowledge gap and provides novel insights into the microbiome as a mechanism that links prenatal disaster exposures with elevated disease risks. Our major finding that reduced microbial diversity and altered metabolic capacity are associated with prenatal hurricane exposures warrants further studies to evaluate the impact of weather disasters on the unborn.https://journals.asm.org/doi/10.1128/msphere.00134-23infant gut microbiomeprenatal exposureextreme weather eventclimate changemetagenomic sequencingasthma |
| spellingShingle | Ai Zhang David de Ángel Solá Midnela Acevedo Flores Lijuan Cao Leran Wang Josh G. Kim Phillip I. Tarr Barbara B. Warner Nicolás Rosario Matos Leyao Wang Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity mSphere infant gut microbiome prenatal exposure extreme weather event climate change metagenomic sequencing asthma |
| title | Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| title_full | Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| title_fullStr | Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| title_full_unstemmed | Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| title_short | Infants exposed in utero to Hurricane Maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| title_sort | infants exposed in utero to hurricane maria have gut microbiomes with reduced diversity and altered metabolic capacity |
| topic | infant gut microbiome prenatal exposure extreme weather event climate change metagenomic sequencing asthma |
| url | https://journals.asm.org/doi/10.1128/msphere.00134-23 |
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