Metatranscriptomics uncovers diet-driven structural, ecological, and functional adaptations in the rumen microbiome linked to feed efficiency

TL;DR

This study shows how diet influences the rumen microbiome structure and function, linking specific microbes to improved feed efficiency in cattle.

Contribution

The study introduces the concept of 'efficient host-mediated microbial amplification' and identifies diet-specific microbial lineages associated with high feed efficiency.

Findings

High-feed-efficiency cattle showed strong positive selection for diet-responsive microbes like Fibrobacter and UBA1067.

Selected microbes encoded carbohydrate-binding modules that enhance substrate adhesion and degradation.

Low-feed-efficiency cattle had more random microbial structures and less functional specialization.

Abstract

The rumen microbiome plays a pivotal role in modulating feed efficiency in ruminants, yet the ecological mechanisms mediating the active interactions among microbial adaptations, dietary inputs, and host feed efficiency within the rumen remain poorly understood. To address this gap, we analyzed 120 metatranscriptomic datasets obtained from 30 purebred Angus bulls (each sampled four times) classified as high-feed-efficiency or low-feed-efficiency based on feed conversion ratio, and fed either forage-based (n = 15) or grain-based (n = 15) diets. We constructed a comprehensive active gene catalog comprising 1 744 067 non-redundant genes and compiled a reference set of 25 115 ruminant microbial genomes. Using integrated Neutral Community Model analysis and carbohydrate-active enzyme profiling, we examined how ecological processes and functional capacities differed across host phenotypes and diets. Neutral Community Model fits revealed that stochastic processes broadly governed rumen microbial community structures (R2 = 0.779 for high-feed-efficiency; R2 = 0.781 for low-feed-efficiency). Within the predominantly stochastic processes, however, high-feed-efficiency bulls exhibited strong positive selection for diet-responsive microbial lineages: Fibrobacter spp. (positively selected species-level genome bins: 61.3%–76.0%; negatively selected: 0%–1.3%), Butyrivibrio spp. (positively selected: 13.3%–46.0%; negatively selected: 1.0%–11.2%) under forage feeding, and UBA1067 spp. (positively selected: 33.3%–48.5%; negatively selected: 0%–8.3%) under grain feeding. These lineages encoded catalytic domains appended with carbohydrate-binding modules, such as tandem carbohydrate-binding modules linked to glycoside hydrolases, thereby enhancing substrate adhesion and degradation. In contrast, low-feed-efficiency bulls showed more random community structures and reduced functional specialization. Therefore, these suggest that cattle hosts with higher feed efficiency promote microbial populations functionally aligned with dietary inputs, a process we define as efficient host-mediated microbial amplification. These findings offer new insight into how ecological assembly and functional adaptation of the microbiome contribute to feed efficiency and lay the foundation for microbiome-informed strategies to enhance ruminant production sustainability.

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