Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk

Exclusive breastfeeding is recommended to newborns during the first 6 months of life, whereas dairy-based infant formula is an alternative nutrition source offered to infants. Several studies demonstrated that breastfed infants have a different gut bacterial composition relative to formula-fed infan...

Full description

Bibliographic Details
Main Authors: Ahmed Elolimy, Fernanda Rosa, Patricia Tripp, Mohamed Zeineldin, Anne K. Bowlin, Christopher Randolph, Michael S. Robeson, Laxmi Yeruva
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.801854/full
_version_ 1811260791628759040
author Ahmed Elolimy
Ahmed Elolimy
Fernanda Rosa
Fernanda Rosa
Fernanda Rosa
Patricia Tripp
Mohamed Zeineldin
Anne K. Bowlin
Anne K. Bowlin
Christopher Randolph
Michael S. Robeson
Laxmi Yeruva
Laxmi Yeruva
author_facet Ahmed Elolimy
Ahmed Elolimy
Fernanda Rosa
Fernanda Rosa
Fernanda Rosa
Patricia Tripp
Mohamed Zeineldin
Anne K. Bowlin
Anne K. Bowlin
Christopher Randolph
Michael S. Robeson
Laxmi Yeruva
Laxmi Yeruva
author_sort Ahmed Elolimy
collection DOAJ
description Exclusive breastfeeding is recommended to newborns during the first 6 months of life, whereas dairy-based infant formula is an alternative nutrition source offered to infants. Several studies demonstrated that breastfed infants have a different gut bacterial composition relative to formula-fed infants. In addition, animal models have shown that human milk (HM)–fed piglets had a distinct intestinal bacterial composition compared with milk formula (MF)–fed piglets. However, the gut fungal composition and the interactions with the bacterial community in breastfed compared with formula-fed infants remain to be investigated. In an attempt to evaluate such differences, we used an animal model to perform a shotgun metagenomics analysis on the cecal and distal colon contents of neonatal piglets fed with pasteurized HM or a dairy-based infant formula (MF) during the first 21 days of life. At postnatal day 21 (PND 21), a subset of piglets from each diet group (n = 11 per group) was euthanized. The remaining piglets in each group were weaned to a solid diet and euthanized at PND 51 (n = 13 per group). Large intestine contents (i.e., cecum and distal colon) were subjected to shotgun metagenomics analysis. The differential taxonomic composition of bacteria and fungi and the predicted functional gene profiling were evaluated. Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria are the most abundant bacterial phyla observed in piglets at PND 21 and PND 51. In the large intestine at PND 21 and PND 51, Proteobacteria phylum was significantly higher in MF-fed group, and species Burkholderiales bacterium of phyla was significantly higher in MF group relative to HM group. In addition, in HM group, several Lactobacillus spp. and Bacteroides spp. were higher relative to MF group in the large intestine at PND 21 and PND 51. Fungal genus Aspergillus was higher in MF, whereas Malassezia was lower relative to HM group. Persistent effects of the neonatal diets were observed at PND 51, where alpha- and beta-diversity differences were detected for bacterial and fungal species in the large intestine. Overall, our findings indicate that neonatal diet affects the large intestinal microbial community during the exclusive milk-feeding period, as well as after the introduction of the complementary food.
first_indexed 2024-04-12T18:51:50Z
format Article
id doaj.art-51eae416c9b34a6e854a387da26d184a
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-12T18:51:50Z
publishDate 2022-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-51eae416c9b34a6e854a387da26d184a2022-12-22T03:20:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-03-011310.3389/fmicb.2022.801854801854Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human MilkAhmed Elolimy0Ahmed Elolimy1Fernanda Rosa2Fernanda Rosa3Fernanda Rosa4Patricia Tripp5Mohamed Zeineldin6Anne K. Bowlin7Anne K. Bowlin8Christopher Randolph9Michael S. Robeson10Laxmi Yeruva11Laxmi Yeruva12Arkansas Children’s Nutrition Center, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Little Rock, AR, United StatesDepartment of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesArkansas Children’s Nutrition Center, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Little Rock, AR, United StatesDepartment of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesSchool of Veterinary Medicine, Texas Tech University, Amarillo, TX, United StatesArkansas Children’s Nutrition Center, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Little Rock, AR, United StatesDepartment of Animal Medicine, College of Veterinary Medicine, Benha University, Banha, EgyptArkansas Children’s Nutrition Center, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Little Rock, AR, United StatesDepartment of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesCenter for Translational Pediatric Research, Arkansas Children’s Research Institute, Little Rock, AR, United StatesDepartment of Biomedical Informatics, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesArkansas Children’s Nutrition Center, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Little Rock, AR, United StatesDepartment of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesExclusive breastfeeding is recommended to newborns during the first 6 months of life, whereas dairy-based infant formula is an alternative nutrition source offered to infants. Several studies demonstrated that breastfed infants have a different gut bacterial composition relative to formula-fed infants. In addition, animal models have shown that human milk (HM)–fed piglets had a distinct intestinal bacterial composition compared with milk formula (MF)–fed piglets. However, the gut fungal composition and the interactions with the bacterial community in breastfed compared with formula-fed infants remain to be investigated. In an attempt to evaluate such differences, we used an animal model to perform a shotgun metagenomics analysis on the cecal and distal colon contents of neonatal piglets fed with pasteurized HM or a dairy-based infant formula (MF) during the first 21 days of life. At postnatal day 21 (PND 21), a subset of piglets from each diet group (n = 11 per group) was euthanized. The remaining piglets in each group were weaned to a solid diet and euthanized at PND 51 (n = 13 per group). Large intestine contents (i.e., cecum and distal colon) were subjected to shotgun metagenomics analysis. The differential taxonomic composition of bacteria and fungi and the predicted functional gene profiling were evaluated. Bacteroidetes, Firmicutes, Proteobacteria, and Actinobacteria are the most abundant bacterial phyla observed in piglets at PND 21 and PND 51. In the large intestine at PND 21 and PND 51, Proteobacteria phylum was significantly higher in MF-fed group, and species Burkholderiales bacterium of phyla was significantly higher in MF group relative to HM group. In addition, in HM group, several Lactobacillus spp. and Bacteroides spp. were higher relative to MF group in the large intestine at PND 21 and PND 51. Fungal genus Aspergillus was higher in MF, whereas Malassezia was lower relative to HM group. Persistent effects of the neonatal diets were observed at PND 51, where alpha- and beta-diversity differences were detected for bacterial and fungal species in the large intestine. Overall, our findings indicate that neonatal diet affects the large intestinal microbial community during the exclusive milk-feeding period, as well as after the introduction of the complementary food.https://www.frontiersin.org/articles/10.3389/fmicb.2022.801854/fullhuman milkmilk formuladistal gutbacteriafungi
spellingShingle Ahmed Elolimy
Ahmed Elolimy
Fernanda Rosa
Fernanda Rosa
Fernanda Rosa
Patricia Tripp
Mohamed Zeineldin
Anne K. Bowlin
Anne K. Bowlin
Christopher Randolph
Michael S. Robeson
Laxmi Yeruva
Laxmi Yeruva
Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
Frontiers in Microbiology
human milk
milk formula
distal gut
bacteria
fungi
title Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
title_full Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
title_fullStr Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
title_full_unstemmed Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
title_short Bacterial and Fungal Adaptations in Cecum and Distal Colon of Piglets Fed With Dairy-Based Milk Formula in Comparison With Human Milk
title_sort bacterial and fungal adaptations in cecum and distal colon of piglets fed with dairy based milk formula in comparison with human milk
topic human milk
milk formula
distal gut
bacteria
fungi
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.801854/full
work_keys_str_mv AT ahmedelolimy bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT ahmedelolimy bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT fernandarosa bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT fernandarosa bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT fernandarosa bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT patriciatripp bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT mohamedzeineldin bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT annekbowlin bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT annekbowlin bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT christopherrandolph bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT michaelsrobeson bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT laxmiyeruva bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk
AT laxmiyeruva bacterialandfungaladaptationsincecumanddistalcolonofpigletsfedwithdairybasedmilkformulaincomparisonwithhumanmilk