Inulin Fermentation by Lactobacilli and Bifidobacteria from Dairy Calves

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 comb. nov. (formerly 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 non-fermenter strains indicated that strain YZ050 encodes an inulinase homolog, previously linked to extracellular degradation of long-chain inulin in Lacticaseibacillus paracasei comb. nov., that was strongly induced during growth on inulin. Inulin catabolism by YZ050 also generates extracellular fructose which can serve as a growth substrate to 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, a 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 that can promote growth of other non-inulin consuming LAB strains. 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.

In vitro Selection of Synbiotics and in vivo Investigation of Growth Indices, Reproduction Performance, Survival, and Ovarian Cyp19α Gene Expression in Zebrafish Danio rerio

“…In the case of the artichoke extract, it was the dose of 100% that resulted in higher growth rates of the L. acidophilus and L. delbrueckii (see, Figures 1 , 3 ) but in the case of the mushroom extract, it was at the dose of 50% where the probiotic strain exhibited maximum growth rate ( Figures 2 , 4 ). The observed increase in the growth rate of the probionts in response to the addition of artichoke extract in the medium could be attributed to the presence of inulin-type fructans, such as inulin, fructooligosaccharide, in the artichoke extract ( Yaseen, 2018 ; Rattanakiat et al, 2020 ; Zhu et al, 2020 ). Fructans are one of the most known prebiotics that were shown to stimulate probiotics growth in several organisms, including fish ( Li et al, 2019 ; Manikandan et al, 2020 ; Ghafarifarsani et al, 2021 ; Zimmermann et al, 2021 ).…”

Isolation and Identification of a Rumen Lactobacillus Bacteria and Its Degradation Potential of Gossypol in Cottonseed Meal during Solid-State Fermentation

“…L. agilis is firstly isolated from municipal sewage in 1981, and it is commonly known as motile Lactobacillus species from sewage and chicken guts [38,39], it was demonstrated that L. agilis played a key role in the degradation of sinigrin, cholesterol, and glucosinolates [40,41]. There was limited knowledge about its function in ruminants, Zhu et al [42] had isolated several L. agilis from the feces of dairy calves, and found that these bacteria readily degraded long chain inulin. To date, this is the first time found that L. agilis presented the ability of gossypol degradation, the successful isolation of L. agilis from the rumen would be helpful for a better understanding of its detoxification mechanism of gossypol in the future.…”

Epitranscriptomic profile of Lactobacillus agilis and its adaptation to growth on inulin

“…A Lactobacillus agilis strain named YZ050 was previously isolated from dairy cow fecal samples in our lab and showed the capability to ferment inulin [13]. The stock was streaked on MRS plates.…”