Metaproteome plasticity sheds light on the ecology of the rumen microbiome and its connection to host traits

Abstract

The arsenal of genes that microbes express reflect the way in which they sense their environment. We have previously reported that the rumen microbiome composition and its coding capacity are different in animals having distinct feed efficiency states, even when fed an identical diet. Here, we reveal that many microbial populations belonging to the bacteria and archaea domains show divergent proteome production in function of the feed efficiency state. Thus, proteomic data serve as a strong indicator of host feed efficiency state phenotype, overpowering predictions based on genomic and taxonomic information. We highlight protein production of specific phylogenies associated with each of the feed efficiency states. We also find remarkable plasticity of the proteome both in the individual population and at the community level, driven by niche partitioning and competition. These mechanisms result in protein production patterns that exhibit functional redundancy and checkerboard distribution that are tightly linked to the host feed efficiency phenotype. By linking microbial protein production and the ecological mechanisms that act within the microbiome feed efficiency states, our present work reveals a layer of complexity that bears immense importance to the current global challenges of food security and sustainability.

Core microbiota for nutrient digestion remained and ammonia utilization increased after continuous batch culture of rumen microbiota in vitro

“…Previous studies reported controversial effects of urea supplementation on gas production and dry matter digestibility ( Salem et al, 2013 ; Spanghero et al, 2018 ; Muthia et al, 2021 ; Kour et al, 2023 ), and we detected that bacterial counts decreased but gas production and dry matter digestibility were stable over a 23-day continuous batch culture of rumen microbiota under high urea condition. The theory of functional redundancy in rumen microbiota might support these observations ( Wemheuer et al, 2020 ; Sasson et al, 2022 ), and we inferred that functional redundant microbes might be partially removed, while core bacteria associated with dry matter digestion might be preserved after 23 days of continuous batch culture.…”

Prevotella: A Key Player in Ruminal Metabolism

“…The authors concluded that highly efficient animals process a less diverse array of metabolites and specialize in the production of fatty acids with a concomitant reduction in methane production [ 106 ]. Further results published by the same group revealed that proteomics data are more informative to delineate the actual microbiome metabolic profile than metagenomics data, thus fueling a long-standing debate concerning the intrinsic divergence between gene content and actual protein expression in metagenomics studies [ 114 ]. Nevertheless, these and a myriad of additional studies led to the proposal of a host genetics-microbiome axis as the master control mechanism of metabolism in ruminants [ 103 , 115 ].…”

Life at the borderlands: microbiomes of interfaces critical to One Health

“…Additionally, this method enables the detection of post-translational modifications. Metaproteomic analysis can be approached through targeted or untargeted strategies (Sasson et al 2022 ).…”

“…Such data can then be interpreted in the context of the milieu of interactions in microbial communities and host and environmental interfaces (Gloag et al 2013 , Regmi et al 2022 ). For example, Sasson et al ( 2022 ) demonstrated the increased depth of insight possible with metaproteomic data paired with metagenomic data in the rumen microbiome. Their study revealed associations between protein production profiles of specific metagenome-assembled genomes (in addition to phyla) and cattle feed efficiency phenotypes.…”