Understanding the gut microbiome of dairy calves: Opportunities to improve early-life gut health

Abstract Background: Antibiotic resistance is an increasing threat to human health. The human gut microbiome harbors a collection of bacterial antimicrobial resistance genes (ARGs) known as the resistome. The factors associated with establishment of the resistome in early life are not well understood and clarifying these factors would inform strategies to decrease antibiotic resistance. We investigated the early-life exposures and taxonomic signatures associated with resistome development over the first year of life in a large, prospective cohort in the United States. Shotgun metagenomic sequencing was used to profile both microbial composition and ARGs in stool samples collected at 6 weeks and 1 year of age from infants enrolled in the New Hampshire Birth Cohort Study. Negative binomial regression and statistical modeling was used to examine infant factors such as sex, delivery mode, feeding method, gestational age, antibiotic exposure, and infant gut microbiome composition in relation to the diversity and relative abundance of ARGs.Results: Metagenomic sequencing was performed on paired samples from 195 full term (at least 37 weeks’ gestation) and 15 late preterm (33-36 weeks’ gestation) infants. 6-week samples compared to 1-year samples had 4.37 times (95% CI: 3.54-5.39) the rate of harboring ARGs. The majority of ARGs that were at a greater relative abundance at 6 weeks (chi-squared p < 0.01) worked through the mechanism of antibiotic efflux (i.e., by pumping antibiotics out of the cell). The overall relative abundance of the resistome was strongly correlated with Proteobacteria (Spearman correlation = 78.9%) and specifically E. coli (62.2%) relative abundance in the gut microbiome. Among infant characteristics, delivery mode was most strongly associated with the diversity and relative abundance of ARGs. Infants born via cesarean delivery had a higher risk of harboring unique ARGs [relative risk = 1.12 (95% CI: 0.97 – 1.29)] as well as a having an increased risk for overall ARG relative abundance [relative risk = 1.43 (95% CI: 1.12 – 1.84)] at 1 year compared to infants born vaginally. Additionally, 6 specific ARGs were at a greater relative abundance in infants delivered by cesarean section compared to vaginally delivered infants across both time points. Conclusions: Our findings suggest that the developing infant gut resistome may be alterable by early-life exposures. Establishing the extent to which infant characteristics and early-life exposures impact the resistome can ultimately lead to interventions that decrease the transmission of ARGs and thus the possibility of antibiotic resistant life threatening infections.

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Biotic and abiotic factors influencing channel catfish egg and gut microbiome dynamics during early life stages

Aquaculture ◽

10.1016/j.aquaculture.2018.08.073 ◽

2019 ◽

Vol 498 ◽

pp. 556-567 ◽

Cited By ~ 5

Author(s):

S. Abdul Razak ◽

M.J. Griffin ◽

C.C. Mischke ◽

B.G. Bosworth ◽

G.C. Waldbieser ◽

...

Keyword(s):

Channel Catfish ◽

Gut Microbiome ◽

Early Life ◽

Abiotic Factors ◽

Life Stages ◽

Early Life Stages ◽

Biotic And Abiotic Factors ◽

Factors Influencing

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Effects of different feed type exposure in early life on performance, rumen fermentation, and feed preference of dairy calves

Journal of Dairy Science ◽

10.3168/jds.2018-14373 ◽

2018 ◽

Vol 101 (9) ◽

pp. 8169-8181 ◽

Cited By ~ 1

Author(s):

J.X. Xiao ◽

L.Y. Guo ◽

G.M. Alugongo ◽

Y.J. Wang ◽

Z.J. Cao ◽

...

Keyword(s):

Early Life ◽

Rumen Fermentation ◽

Dairy Calves

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Diet, Environmental Chemicals, and the Gut Microbiome

10.1093/med/9780190490911.003.0006 ◽

2017 ◽

Cited By ~ 1

Author(s):

Marvin M. Singh ◽

Gerard E. Mullin

Keyword(s):

Cardiovascular Disease ◽

Metabolic Syndrome ◽

Intestinal Permeability ◽

Environmental Effects ◽

Gut Microbiome ◽

Critical Role ◽

Environmental Exposures ◽

Environmental Chemicals ◽

Gut Health ◽

Daily Lives

This chapter reviews the latest research on gut health and addresses the nutritional and environmental effects on the gut microbiome, a key player in pathogenesis of diseases such as inflammation, intestinal permeability, obesity, metabolic syndrome, diabetes, cardiovascular disease, and neurologic conditions. The 100 trillion microorganisms that cohabit within each of us play a critical role in maintaining health and preventing disease. Many factors can alter and interact with the microbiome, including nutrition, genetics, and environmental exposures. Clinicians need to understand these relationships to help patients make the informed decisions that can impact their daily lives and the health of subsequent generations.

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Early life determinants induce sustainable changes in the gut microbiome of six-year-old children

Scientific Reports ◽

10.1038/s41598-019-49160-7 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 4

Author(s):

Silvia Gschwendtner ◽

Hyena Kang ◽

Elisabeth Thiering ◽

Susanne Kublik ◽

Bärbel Fösel ◽

...

Keyword(s):

Gut Microbiome ◽

Early Life

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Inulin Fermentation by Lactobacilli and Bifidobacteria from Dairy Calves

Applied and Environmental Microbiology ◽

10.1128/aem.01738-20 ◽

2020 ◽

Vol 87 (1) ◽

Author(s):

Yuanting Zhu ◽

Jinxin Liu ◽

Julian M. Lopez ◽

David A. Mills

Keyword(s):

Lactic Acid ◽

Lactic Acid Bacteria ◽

Gut Microbiome ◽

Animal Health ◽

Dairy Calves ◽

Milk Replacer ◽

Comparative Genomic ◽

Bacterial Strains ◽

Content Type ◽

Long Chain

ABSTRACT Prebiotics are increasingly examined for their ability to modulate the neonate gut microbiota of livestock, and products such as inulin are commonly added to milk replacer used in calving. However, the ability of specific members of the bovine neonate microbiota to respond to inulin remains to be determined, particularly among indigenous lactobacilli and bifidobacteria, beneficial genera commonly enriched by inulin. Screening of Bifidobacterium and Lactobacillus isolates obtained from fresh feces of dairy calves revealed that lactobacilli had a higher prevalence of inulin fermentation capacity (58%) than bifidobacteria (17%). Several Ligilactobacillus agilis (synonym Lactobacillus agilis) isolates exhibited vigorous growth on, and complete degradation of, inulin; however, the phenotype was strain specific. The most vigorous inulin-fermenting strain, L. agilis YZ050, readily degraded long-chain inulin not consumed by bifidobacterial isolates. Comparative genomic analysis of both L. agilis fermenter and nonfermenter strains indicated that strain YZ050 encodes an inulinase homolog, previously linked to extracellular degradation of long-chain inulin in Lacticaseibacillus paracasei, that was strongly induced during growth on inulin. Inulin catabolism by YZ050 also generates extracellular fructose, which can cross-feed other non-inulin-fermenting lactic acid bacteria isolated from the same bovine feces. The presence of specific inulin-responsive bacterial strains within calf gut microbiome provides a mechanistic rationale for enrichment of specific lactobacilli and creates a foundation for future synbiotic applications in dairy calves aimed at improving health in early life. IMPORTANCE The gut microbiome plays an important role in animal health and is increasingly recognized as a target for diet-based manipulation. Inulin is a common prebiotic routinely added to animal feeds; however, the mechanism of inulin consumption by specific beneficial taxa in livestock is ill defined. In this study, we examined Lactobacillus and Bifidobacterium isolates from calves fed inulin-containing milk replacer and characterized specific strains that robustly consume long-chain inulin. In particular, novel Ligilactobacillus agilis strain YZ050 consumed inulin via an extracellular fructosidase, resulting in complete consumption of all long-chain inulin. Inulin catabolism resulted in temporal release of extracellular fructose, which can promote growth of other non-inulin-consuming strains of lactic acid bacteria. This work provides the mechanistic insight needed to purposely modulate the calf gut microbiome via the establishment of networks of beneficial microbes linked to specific prebiotics.

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Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health

Gut ◽

10.1136/gutjnl-2020-321747 ◽

2020 ◽

pp. gutjnl-2020-321747

Author(s):

Marina Fassarella ◽

Ellen E Blaak ◽

John Penders ◽

Arjen Nauta ◽

Hauke Smidt ◽

...

Keyword(s):

Environmental Factors ◽

Microbial Diversity ◽

Gut Microbiome ◽

Gut Health ◽

Stable States ◽

Host Genotype ◽

Functional Richness ◽

Microbe Interactions ◽

Host Microbe Interactions ◽

Stability And Resilience

The human gut microbiome is a complex ecosystem, densely colonised by thousands of microbial species. It varies among individuals and depends on host genotype and environmental factors, such as diet and antibiotics. In this review, we focus on stability and resilience as essential ecological characteristics of the gut microbiome and its relevance for human health. Microbial diversity, metabolic flexibility, functional redundancy, microbe–microbe and host–microbe interactions seem to be critical for maintaining resilience. The equilibrium of the gut ecosystem can be disrupted by perturbations, such as antibiotic therapy, causing significant decreases in functional richness and microbial diversity as well as impacting metabolic health. As a consequence, unbalanced states or even unhealthy stable states can develop, potentially leading to or supporting diseases. Accordingly, strategies have been developed to manipulate the gut microbiome in order to prevent or revert unhealthy states caused by perturbations, including faecal microbiota transplantation, supplementation with probiotics or non-digestible carbohydrates, and more extensive dietary modifications. Nevertheless, an increasing number of studies has evidenced interindividual variability in extent and direction of response to diet and perturbations, which has been attributed to the unique characteristics of each individual’s microbiome. From a clinical, translational perspective, the ability to improve resilience of the gut microbial ecosystem prior to perturbations, or to restore its equilibrium afterwards, would offer significant benefits. To be effective, this therapeutic approach will likely need a personalised or subgroup-based understanding of individual genetics, diet, gut microbiome and other environmental factors that might be involved.

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Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model

Applied and Environmental Microbiology ◽

10.1128/aem.02510-18 ◽

2019 ◽

Vol 85 (9) ◽

Cited By ~ 4

Author(s):

Chunlong Mu ◽

Gaorui Bian ◽

Yong Su ◽

Weiyun Zhu

Keyword(s):

Early Life ◽

Inflammatory Cytokine ◽

Immune Status ◽

Interspecific Cross ◽

Cytokine Expression ◽

Gut Health ◽

Content Type ◽

Nursing Mother ◽

Colonic Microbiota ◽

Cross Fostering

ABSTRACT Nursing mother and breed can differently regulate early-life microbiota succession in pigs. However, it remains unclear whether they affect gastrointestinal microbiota and immune status, which are critical for early-life gut health. Here, an interspecific cross-fostering piglet model was employed by fostering neonatal Yorkshire and Meishan piglets to the same or another breed of sows. Jejunal and colonic microbiotas and mucosal immune parameters were analyzed at postnatal days 14 (preweaning) and 49 (postweaning). Nursing mother affected 10 genera in the colon and 3 minor genera in the jejunum. At day 14, Meishan sow-nursed piglets had lower Streptococcus suis and higher Cloacibacillus counts in the colonic digesta and larger amounts of interleukin 10 and Foxp3-positive cells in the colonic mucosa than did Yorkshire sow-nursed piglets. At day 49, nursing mother had no significant effects on cytokine expression. Breed effects were observed; Meishan piglets had lower relative abundances of Prevotella and lower gene expression of tumor necrosis factor alpha (TNF-α) than those of Yorkshire piglets at days 14 and 49. Collectively, nursing mother mainly affected preweaning colonic microbiota and immune status, while breed effects persisted after weaning. Piglets nursed by Meishan sows had different microbiota compositions and inflammatory cytokine profiles in the colon compared with those of piglets nursed by Yorkshire sows. These results highlight the different role of nursing mother and breed in affecting early gut microenvironment. IMPORTANCE Early-life gut microbiota and immune status are pivotal for postnatal growth. By using an interspecific cross-fostering piglet model, we find that change in nursing mother transiently reshapes preweaning colon microbiota and immune status, while breed shows persistent effects both pre- and postweaning. Piglets nursed by Meishan sows had lower Streptococcus suis counts and higher anti-inflammatory cytokine expression. These results highlight the significance of nursing mother in regulating early-life gut health.

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