Abstract

Recent evidence suggests that changes in microbial colonization of the rumen prior to weaning may imprint the rumen microbiome and impact phenotypes later in life. We investigated how dietary manipulation from birth influences growth, methane production, and gastrointestinal microbial ecology. At birth, 18 female Holstein and Montbéliarde calves were randomly assigned to either treatment or control (CONT). Treatment was 3-nitrooxypropanol (3-NOP), an investigational anti-methanogenic compound that was administered daily from birth until three weeks post-weaning (week 14). Samples of rumen fluid and faecal content were collected at weeks 1, 4, 11, 14, 23, and 60 of life. Calves were tested for methane emissions using the GreenFeed system during the post-weaning period (week 11–23 and week 56–60 of life). Calf physiological parameters (BW, ADG and individual VFA) were similar across groups throughout the trial. Treated calves showed a persistent reduction in methane emissions (g CH4/d) throughout the post-weaning period up to at least 1 year of life, despite treatment ceasing three weeks post-weaning. Similarly, despite variability in the abundance of individual taxa across weeks, the rumen bacterial, archaeal and fungal structure differed between CONT and 3-NOP calves across all weeks, as visualised using sparse-PLS-DA. Similar separation was also observed in the faecal bacterial community. Interestingly, despite modest modifications to the abundance of rumen microbes, the reductive effect of 3-NOP on methane production persisted following cessation of the treatment period, perhaps indicating a differentiation of the ruminal microbial ecosystem or a host response triggered by the treatment in the early development phase.

Highlights

  • Recent evidence suggests that changes in microbial colonization of the rumen prior to weaning may imprint the rumen microbiome and impact phenotypes later in life

  • In a study by Romero-Perez et al.[22] the effects diminished after treatment ceased, indicating that the inhibiting effects on methane are likely dependent on continuous supplementation of 3-NOP

  • Calves receiving 3-NOP showed a persistent reduction in methane emissions (g ­CH4/d) throughout the immediate postweaning period and at one year post-weaning, despite treatment ceasing at three weeks after weaning (14 weeks of life; Fig. 1)

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Summary

Introduction

Recent evidence suggests that changes in microbial colonization of the rumen prior to weaning may imprint the rumen microbiome and impact phenotypes later in life. Recent characterisations of the gastrointestinal microbiome from birth have outlined the sequential establishment of microbial d­ omains[4,5,6] This may provide a small window for effective manipulation of methanogens, as ruminal archaea reach levels similar to that of an adult by ~ 14 d of l­ife[7,8]. The effect did not persist entirely 4 months after, we considered that interventions which target both microbial establishment, and the weaning transition period, may have the potential to imprint the microbiome for reduced methane emissions persisting later into life. Strategies to alter the microbiome in favour of reduced methanogenesis include s­ aponins[14,15], tannins, nitrates and unsaturated f­ats[16,17,18,19], which exhibit an antiprotozoal effect Effects of these interventions have largely failed to persist beyond treatment application periods. We examined the effects of 3-NOP on methane production in post-weaned calves during treatment, and for up to one year post treatment to determine its ability to favour reduced methane production

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