Investigating early life microbial and host transcriptomic dynamics in the bovine gastrointestinal tract

Eóin O'Hara
There is increasing concern surrounding the ability of livestock industries to meet the needs of the rising global population. The gastrointestinal microbiota of ruminants plays a critical role in feed degradation, host energy supply, but is also a substantial source of anthropogenic greenhouse gas emissions. It is proposed that dietary intervention during the first weeks of life may offer an opportunity to permanently manipulate microbial colonisation patterns of the rumen, with a view to
more » ... cing host performance whilst mitigating climatic impacts. However, the optimum window for intervention remains to be elucidated. Despite the close relationship between the rumen and its microbes, understanding of the molecular controls of rumen development during early life is limited. In mature animals, microbial fermentation in the rumen is the principle host energy source, but the hindgut and its microbiome may play of increased importance while the rumen develops during early life. However, little is known of the hindgut microbiota and its contribution to animal growth. Study 1 investigated the temporal dynamics of the rumen microbiota in beef calves during early life using 16S rRNA sequencing, to characterise the patterns of microbial establishment in the rumen and identify the most favourable timeframe for dietary manipulation. The microbial community displayed an ordered pattern of succession during the first 3 weeks of life, but settled by day 21, indicating that this may be the limit of any timeframe for early life manipulation. Study 1 also revealed a substantial farm effect on the colonisation of certain microbial groups, including Methanobrevibacter smithii (P<0.05) and Dialister (P<0.05). Such an effect has not been reported previously and may have substantial implications in future manipulation efforts. Study 2 characterised the transcriptomic profile of rumen tissue from birth to post weaning, revealing significant enrichment in immune related genes (e.g. TLR5, LAP, TAP) and processes following birth (P<0.05). This was not associated with any depression in known tight junction genes (P>0.05), indicating that rumen permeability was not compromised. Further exploring the relationship between microbial colonisation and rumen immune function may offer an opportunity to manipulate the establishment of certain taxa. Solid iii feed allocation was associated with enhanced expression of genes involved in Volatile Fatty Acid (VFA) absorption (MCT1; P<0.05) and metabolism (BDH1, ACAT; P<0.05). Understanding the mechanistic control of VFA absorption and how it changes during the life-cycle of the animal will be key for the design of optimal calf nutrition strategies. Study 3 characterised the hindgut microbiota of young ruminants, and its response to fortification of milk replacer with sodium butyrate (SB). The trophic effect of butyrate on calf growth and feed efficiency (P<0.1) was associated with increased concentrations of total VFA, propionate and acetate (P<0.05) in the hindgut. Native butyrogenic bacteria Butyrivibrio and Shuttleworthia were decreased by SB (P<0.05), while the proportion of the propionate producer Phascolarctobacterium was higher (P<0.05). Mogibacterium is associated with impaired gut health and was reduced in the cecum of SB calves (P<0.05). These data show that the beneficial effects of SB on growth and performance occur in tandem with changes in the abundance of important SCFA producing and health-associated bacteria in the hindgut in milk-fed calves, and that SB supplementation may suppress butyrate biosynthesis in the gut. Therefore, efforts to improve animal performance via early life manipulation should also consider the hindgut compartments, as this may offer a method to improve animal performance during the milk-feeding period. In summary, the data presented in this thesis contributes to understanding of rumen microbial composition and molecular development during early life and shows that enhanced activity of the hindgut microbiota may contribute to early life calf growth. iv Preface This thesis is an original work by Eóin O'Hara and is part of a collaborative initiative between Prof. Leluo Guan at the University of Alberta and Dr. Sinéad Waters of Teagasc, Ireland.
doi:10.7939/r3-gpj3-5m35 fatcat:mbug2fnn3ffrnebobcggbshnpy