Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk

Preterm infants have an immature intestinal environment featuring microbial dysbiosis. Human milk can improve the composition of the neonatal gut microbiome by supporting commensal species. Milk free fatty acids (FFAs) provide nutritional energy, participate in endogenous signaling, and exert antimi...

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Main Authors: Megan E. Waller, Alyssa Gutierrez, Taylor D. Ticer, Janiece S. Glover, John E. Baatz, Carol L. Wagner, Melinda A. Engevik, Katherine E. Chetta
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Journal of Functional Foods
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Online Access:http://www.sciencedirect.com/science/article/pii/S1756464625000064
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author Megan E. Waller
Alyssa Gutierrez
Taylor D. Ticer
Janiece S. Glover
John E. Baatz
Carol L. Wagner
Melinda A. Engevik
Katherine E. Chetta
author_facet Megan E. Waller
Alyssa Gutierrez
Taylor D. Ticer
Janiece S. Glover
John E. Baatz
Carol L. Wagner
Melinda A. Engevik
Katherine E. Chetta
author_sort Megan E. Waller
collection DOAJ
description Preterm infants have an immature intestinal environment featuring microbial dysbiosis. Human milk can improve the composition of the neonatal gut microbiome by supporting commensal species. Milk free fatty acids (FFAs) provide nutritional energy, participate in endogenous signaling, and exert antimicrobial effects. This study examined the growth of individual commensal and pathobiont microbes in response to unesterified unsaturated FFAs found in milk: oleic, linoleic, arachidonic, and docosahexaenoic acid. Select species of commensal and pathobiont genera (Bifidobacterium, Lactobacillus, Streptococcus, Staphylococcus, Enterococcus, Acinetobacter, Pseudomonas, Escherichia, and Klebsiella) were cultured with FFAs. The growth of all commensals, except for L. johnsonii, was significantly inhibited by the highest concentration (1 %) of all FFAs. L. johnsonii was only inhibited by arachidonic acid. In contrast, suppression of pathobionts in response to FFAs was less pronounced. Higher concentrations (0.1 %, 1 %) of docosahexaenoic acid significantly inhibited the growth of five of eight pathobionts. Meanwhile, for oleic, linoleic, and arachidonic acid, only two of eight pathobionts were significantly affected. Intriguingly, the effects for these FFAs were highly complex. For example, S. agalactiae growth was enhanced with 1 % oleic acid but suppressed at 0.01 %; however, the effects were directionally opposite for linoleic acid, i.e., suppressed at 1 % but enhanced at 0.01 %. Our genome analyses suggest that pathobiont survival may be related to the number of gene copies for fatty acid transporters. Overall, the effect of FFAs was dose-dependent and species-specific, where commensal growth was broadly inhibited while pathobionts were either unaffected or exhibited complex, bi-directional responses.
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spelling doaj-art-25aa4519cc3f4f4f8da712384196e7192025-02-09T04:59:53ZengElsevierJournal of Functional Foods1756-46462025-02-01125106664Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milkMegan E. Waller0Alyssa Gutierrez1Taylor D. Ticer2Janiece S. Glover3John E. Baatz4Carol L. Wagner5Melinda A. Engevik6Katherine E. Chetta7Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, United States; Department of Pediatrics, C.P. Darby Children's Research Institute, Medical University of South Carolina, United StatesDepartment of Regenerative Medicine & Cell Biology, Medical University of South Carolina, United StatesDepartment of Microbiology & Immunology, Medical University of South Carolina, United StatesDepartment of Regenerative Medicine & Cell Biology, Medical University of South Carolina, United StatesDepartment of Pediatrics, C.P. Darby Children's Research Institute, Medical University of South Carolina, United States; Department of Pediatrics, Division of Neonatal-Perinatal Medicine, Medical University of South Carolina, Shawn Jenkins Children's Hospital, 10 McClennan Banks Drive, MSC 915, Charleston, SC 29425, United StatesDepartment of Pediatrics, C.P. Darby Children's Research Institute, Medical University of South Carolina, United States; Department of Pediatrics, Division of Neonatal-Perinatal Medicine, Medical University of South Carolina, Shawn Jenkins Children's Hospital, 10 McClennan Banks Drive, MSC 915, Charleston, SC 29425, United StatesDepartment of Regenerative Medicine & Cell Biology, Medical University of South Carolina, United States; Department of Microbiology & Immunology, Medical University of South Carolina, United StatesDepartment of Pediatrics, C.P. Darby Children's Research Institute, Medical University of South Carolina, United States; Department of Pediatrics, Division of Neonatal-Perinatal Medicine, Medical University of South Carolina, Shawn Jenkins Children's Hospital, 10 McClennan Banks Drive, MSC 915, Charleston, SC 29425, United States; Corresponding author at: Department of Pediatrics, Division of Neonatal-Perinatal Medicine, Medical University of South Carolina, Shawn Jenkins Children's Hospital, 10 McClennan Banks Drive, MSC 915, Charleston, SC 29465, United States.Preterm infants have an immature intestinal environment featuring microbial dysbiosis. Human milk can improve the composition of the neonatal gut microbiome by supporting commensal species. Milk free fatty acids (FFAs) provide nutritional energy, participate in endogenous signaling, and exert antimicrobial effects. This study examined the growth of individual commensal and pathobiont microbes in response to unesterified unsaturated FFAs found in milk: oleic, linoleic, arachidonic, and docosahexaenoic acid. Select species of commensal and pathobiont genera (Bifidobacterium, Lactobacillus, Streptococcus, Staphylococcus, Enterococcus, Acinetobacter, Pseudomonas, Escherichia, and Klebsiella) were cultured with FFAs. The growth of all commensals, except for L. johnsonii, was significantly inhibited by the highest concentration (1 %) of all FFAs. L. johnsonii was only inhibited by arachidonic acid. In contrast, suppression of pathobionts in response to FFAs was less pronounced. Higher concentrations (0.1 %, 1 %) of docosahexaenoic acid significantly inhibited the growth of five of eight pathobionts. Meanwhile, for oleic, linoleic, and arachidonic acid, only two of eight pathobionts were significantly affected. Intriguingly, the effects for these FFAs were highly complex. For example, S. agalactiae growth was enhanced with 1 % oleic acid but suppressed at 0.01 %; however, the effects were directionally opposite for linoleic acid, i.e., suppressed at 1 % but enhanced at 0.01 %. Our genome analyses suggest that pathobiont survival may be related to the number of gene copies for fatty acid transporters. Overall, the effect of FFAs was dose-dependent and species-specific, where commensal growth was broadly inhibited while pathobionts were either unaffected or exhibited complex, bi-directional responses.http://www.sciencedirect.com/science/article/pii/S1756464625000064Human breast milkDietFormulaBifidobacteriumLactobacillusEnterobacter
spellingShingle Megan E. Waller
Alyssa Gutierrez
Taylor D. Ticer
Janiece S. Glover
John E. Baatz
Carol L. Wagner
Melinda A. Engevik
Katherine E. Chetta
Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
Journal of Functional Foods
Human breast milk
Diet
Formula
Bifidobacterium
Lactobacillus
Enterobacter
title Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
title_full Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
title_fullStr Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
title_full_unstemmed Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
title_short Profiling the response of individual gut microbes to free fatty acids (FFAs) found in human milk
title_sort profiling the response of individual gut microbes to free fatty acids ffas found in human milk
topic Human breast milk
Diet
Formula
Bifidobacterium
Lactobacillus
Enterobacter
url http://www.sciencedirect.com/science/article/pii/S1756464625000064
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