Effects of feeding Saccharomyces cerevisiae fermentation postbiotic on the fecal microbial community of Holstein dairy calves

Centeno‑Martinez et al. Animal Microbiome https://doi.org/10.1186/s42523-023-00234-y (2023) 5:13 Animal Microbiome Open Access BRIEF REPORT Effects of feeding Saccharomyces cerevisiae fermentation postbiotic on the fecal microbial community of Holstein dairy calves Ruth Eunice Centeno‑Martinez1, Wenxuan Dong1, Rebecca N. Klopp1, Ilkyu Yoon2, Jacquelyn P. Boerman1 and Timothy A. Johnson1* Abstract Background The livestock industry is striving to identify antibiotic alternatives to reduce the need to use antibiotics. Postbiotics, such as Saccharomyces cerevisiae fermentation product (SCFP), have been studied and proposed as poten‑ tial non-antibiotic growth promoters due to their effects on animal growth and the rumen microbiome; however, little is known of their effects on the hind-gut microbiome during the early life of calves. The objective of this study was to measure the effect of in-feed SCFP on the fecal microbiome of Holstein bull calves through 4 months of age. Calves (n = 60) were separated into two treatments: CON (no SCFP added) or SCFP (SmartCare®, Diamond V, Cedar Rapids, IA, in milk replacer and NutriTek®, Diamond V, Cedar Rapids, IA, incorporated into feed), and were blocked by body weight and serum total protein. Fecal samples were collected on d 0, 28, 56, 84, and 112 of the study to charac‑ terize the fecal microbiome community. Data were analyzed as a completely randomized block design with repeated measures when applicable. A random-forest regression method was implemented to more fully understand commu‑ nity succession in the calf fecal microbiome of the two treatment groups. Results Richness and evenness of the fecal microbiota increased over time (P < 0.001), and SCFP calves tended to increase the evenness of the community (P = 0.06). Based on random-forest regression, calf age as predicted by microbiome composition was significantly correlated with the calf physiological age ( R2 = 0.927, P < 1 × 10−15). Twenty-two “age-discriminatory” ASVs (amplicon sequence variants) were identified in the fecal microbiome that were shared between the two treatment groups. Of these, 6 ASVs (Dorea-ASV308, Lachnospiraceae-ASV288, OscillospiraASV311, Roseburia-ASV228, Ruminococcaceae-ASV89 and Ruminoccocaceae-ASV13) in the SCFP group reached their highest abundance in the third month, but they reached their highest abundance in the fourth month in the CON group. All other shared ASVs reached their highest abundance at the same timepoint in both treatment groups. Conclusions Supplementation of SCFP altered the abundance dynamics of age discriminatory ASVs, suggesting a faster maturation of some members of the fecal microbiota in SCFP calves compared to CON calves. These results demonstrate the value of analyzing microbial community succession as a continuous variable to identify the effects of a dietary treatment. Keywords Calf, Fecal microbiome, Maturation, Saccharomyces cerevisiae fermentation product *Correspondence: Timothy A. Johnson 1 Department of Animal Science, Purdue University, 270 S Russell St., West Lafayette, IN, USA 2 Diamond V, Cedar Rapids, IA, USA © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Centeno‑Martinez et al. Animal Microbiome (2023) 5:13 Background Dairy calf feeding systems seek to provide pre-weaned calves with dietary nutrition to promote immediate growth and health, as well as future milk production. An important factor in the animal nutrition is the gut microbiome. The gut microbiota has been identified to be important for the development of the intestinal epithelium, mucosal layer, and immune cell repertoire [1]. Additionally, studies had identified a potential link between the small intestine microbiome with calf immune function, health and growth [2, 3]. As an example, a study identified that the prevalence of Faecalibacterium spp. in the fecal microbiota of neonatal calves in the first week of life was associated with higher weight gain and less diarrhea [4]. Therefore, it is important to maintain calf gut health to minimize susceptibility to enteric infections and to improve the animal health and growth. Additionally, the increasing prevalence of antibioticresistant bacteria in both animals and humans has led to the need for alternatives to antibiotics that can still promote the same positive calf health and growth benefits that antibiotics currently provide. Postbiotics can be defined as a mixture of intermediate and end products from microbial fermentation that can contribute to observed health benefits, and are currently being explored as non-antibiotic growth promoters [5]. One example of a postbiotic is Saccharomyces cerevisiae fermentation product (SCFP), which is produced during the anaerobic fermentation of Saccharomyces cerevisiae and provides a complex mixture of metabolites, including lysed cell components, amino acids, lipids, volatile fatty acids, and B vitamins [6]. In the dairy industry, SCFP has supplemented the calf diet to improve feed intake, growth, health and rumen development [7–9]. SCFP improves rumen fermentation, which can be measured by VFA concentration, blood glucose levels, ruminal pH, concentration of anaerobic and cellulolytic bacteria, and papillae length [10–12]. In cows challenged with sub-acute rumen acidosis (SARA), a health disorder in which a the rumen suffers a reversible reduction of the pH below 5.6 and 5.8 for a prolonged period [13], supplementation of 14 g·d−1 of SCFP did not cause a change in the dry matter digestibility and total tract digestibility of crude protein and phosphorus, but supplementation of 38 g·d−1 of SCFP resulted in increased digestibility of neutral detergent fiber (NDF), which includes hemicellulose, cellulose and lignin compounds [14]. In vitro studies using rumen activity modifier model (RAMM) have shown that supplementation of SCFPs increases the abundance of fibrolytic and lactate utilizing organisms compared to control [13]. A follow up metabolic challenge study in mid-lactation dairy cows showed that SCFP supplementation attenuated the negative effects Page 2 of 10 of subacute ruminal acidosis (SARA) such as reduction of richness and (...truncated)