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Frontiers in Microbiology 2023Production of methane by methanogenic archaea, or methanogens, in the rumen of ruminants is a thermodynamic necessity for microbial conversion of feed to volatile fatty... (Review)
Review
Production of methane by methanogenic archaea, or methanogens, in the rumen of ruminants is a thermodynamic necessity for microbial conversion of feed to volatile fatty acids, which are essential nutrients for the animals. On the other hand, methane is a greenhouse gas and its production causes energy loss for the animal. Accordingly, there are ongoing efforts toward developing effective strategies for mitigating methane emissions from ruminant livestock that require a detailed understanding of the diversity and ecophysiology of rumen methanogens. Rumen methanogens evolved from free-living autotrophic ancestors through genome streamlining involving gene loss and acquisition. The process yielded an oligotrophic lifestyle, and metabolically efficient and ecologically adapted descendants. This specialization poses serious challenges to the efforts of obtaining axenic cultures of rumen methanogens, and consequently, the information on their physiological properties remains in most part inferred from those of their non-rumen representatives. This review presents the current knowledge of rumen methanogens and their metabolic contributions to enteric methane production. It also identifies the respective critical gaps that need to be filled for aiding the efforts to mitigate methane emission from livestock operations and at the same time increasing the productivity in this critical agriculture sector.
PubMed: 38029083
DOI: 10.3389/fmicb.2023.1296008 -
Frontiers in Microbiology 2023
PubMed: 37346751
DOI: 10.3389/fmicb.2023.1223885 -
Environmental Research Jul 2023Ruminant animals house a dense and diverse community of microorganisms in their rumen, an enlarged compartment in their stomach, which provides a supportive environment... (Review)
Review
Ruminant animals house a dense and diverse community of microorganisms in their rumen, an enlarged compartment in their stomach, which provides a supportive environment for the storage and microbial fermentation of ingested feeds dominated by plant materials. The rumen microbiota has acquired diverse and functionally overlapped enzymes for the degradation of plant cell wall polysaccharides. In rumen Bacteroidetes, enzymes involved in degradation are clustered into polysaccharide utilization loci to facilitate coordinated expression when target polysaccharides are available. Firmicutes use free enzymes and cellulosomes to degrade the polysaccharides. Fibrobacters either aggregate lignocellulose-degrading enzymes on their cell surface or release them into the extracellular medium in membrane vesicles, a mechanism that has proven extremely effective in the breakdown of recalcitrant cellulose. Based on current metagenomic analyses, rumen Bacteroidetes and Firmicutes are categorized as generalist microbes that can degrade a wide range of polysaccharides, while other members adapted toward specific polysaccharides. Particularly, there is ample evidence that Verrucomicrobia and Spirochaetes have evolved enzyme systems for the breakdown of complex polysaccharides such as xyloglucans, peptidoglycans, and pectin. It is concluded that diversity in degradation mechanisms is required to ensure that every component in feeds is efficiently degraded, which is key to harvesting maximum energy by host animals.
Topics: Animals; Metagenome; Rumen; Lignin; Bacteria; Polysaccharides; Bacteroidetes
PubMed: 37086884
DOI: 10.1016/j.envres.2023.115925 -
JDS Communications May 2024The rumen microbiome digests plant feedstuff that would be otherwise indigestible and provides most of the metabolizable energy and protein the host animals need. Until... (Review)
Review
The rumen microbiome digests plant feedstuff that would be otherwise indigestible and provides most of the metabolizable energy and protein the host animals need. Until recently, research efforts have primarily been directed to bacteria and archaea, leaving the protozoa, fungi, and viruses much less understood. Protozoa contribute to feed digestion and fermentation, but as predators, they affect the microbiome and its function by regulating the abundance and activities of other rumen microbes both in a top-down (by directly killing the prey) and bottom-up (by affecting the metabolism of other microbes) manner. Rumen viruses (or phages, used interchangeably below) are diverse and abundant but the least understood. They are also predators (intracellular "predators") because of their lytic lifecycle, although they can co-exist peacefully with their hosts and reprogram host metabolism, buttressing host ecological fitness. In doing so, rumen viruses also affect the rumen microbiome in both a top-down and a bottom-up manner. Here we review the recent advancement in understanding both types of predators, focusing on their potential impact on the rumen microbiome and functions.
PubMed: 38646576
DOI: 10.3168/jdsc.2023-0433 -
Animal Nutrition (Zhongguo Xu Mu Shou... Dec 2023Enterotypes, which are defined as bacterial clusters in the gut microbiome, have been found to have a close relationship to host metabolism and health. However, this...
Enterotypes, which are defined as bacterial clusters in the gut microbiome, have been found to have a close relationship to host metabolism and health. However, this concept has never been used in the rumen, and little is known about the complex biological relationships between ruminants and their rumen bacterial clusters. In this study, we used young goats ( = 99) as a model, fed them the same diet, and analyzed their rumen microbiome and corresponding bacterial clusters. The relationships between the bacterial clusters and rumen fermentation and growth performance in the goats were further investigated. Two bacterial clusters were identified in all goats: the P-cluster (dominated by genus , = 38) and R-cluster (dominated by , = 61). Compared with P-cluster goats, R-cluster goats had greater growth rates, concentrations of propionate, butyrate, and 18 free amino acids¸ and proportion of unsaturated fatty acids, but lower acetate molar percentage, acetate to propionate ratio, and several odd and branched chain and saturated fatty acids in rumen fluid ( < 0.05). Several members of Firmicutes, including , , and were significantly higher in the R-cluster, whereas Prevotellaceae members, such as and were significantly higher in P-cluster ( < 0.01). Co-occurrence networks showed that R-cluster enriched bacteria had significant negative correlations with P-cluster enriched bacteria ( < 0.05). Moreover, we found the concentrations of propionate, butyrate and free amino acids, and the proportions of unsaturated fatty acids were positively correlated with R-cluster enriched bacteria ( < 0.05). The concentrations of acetate, acetate to propionate ratio, and the proportion of odd and branched chain and saturated fatty acids were positively correlated with P-cluster enriched bacteria ( < 0.05). Overall, our results indicated that rumen bacterial clusters can influence rumen fermentation and growth performance of young goats, which may shed light on modulating the rumen microbiome in early life to improve the growth performance of ruminant animals.
PubMed: 37771855
DOI: 10.1016/j.aninu.2023.05.013 -
Frontiers in Microbiology 2023The calf stage is a critical period for the development of heifers. Newborn calves have low gastrointestinal barrier function and immunity before weaning, making them... (Review)
Review
The calf stage is a critical period for the development of heifers. Newborn calves have low gastrointestinal barrier function and immunity before weaning, making them highly susceptible to infection by various intestinal pathogens. Diarrhea in calves poses a significant threat to the health of young ruminants and may cause serious economic losses to livestock farms. Antibiotics are commonly used to treat diarrhea and promote calf growth, leading to bacterial resistance and increasing antibiotic residues in meat. Therefore, finding new technologies to improve the diarrhea of newborn calves is a challenge for livestock production and public health. The operation of the gut microbiota in the early stages after birth is crucial for optimizing immune function and body growth. Microbiota colonization of newborn animals is crucial for healthy development. Early intervention of the calf gastrointestinal microbiota, such as oral probiotics, fecal microbiota transplantation and rumen microbiota transplantation can effectively relieve calf diarrhea. This review focuses on the role and mechanisms of oral probiotics such as , and in relieving calf diarrhea. The aim is to develop appropriate antibiotic alternatives to improve calf health in a sustainable and responsible manner, while addressing public health issues related to the use of antibiotics in livestock.
PubMed: 37362944
DOI: 10.3389/fmicb.2023.1181545 -
The ISME Journal Jul 2023Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the entodiniomorphs (order: Entodiniomorphida) and holotrichs (order:...
Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the entodiniomorphs (order: Entodiniomorphida) and holotrichs (order: Vestibuliferida) are consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the apparent core role that protozoal species exert, their major biological and metabolic contributions to rumen function remain largely undescribed in vivo. Here, we have leveraged (meta)genome-centric metaproteomes from rumen fluid samples originating from both cattle and goats fed diets with varying inclusion levels of lipids and starch, to detail the specific metabolic niches that protozoa occupy in the context of their microbial co-habitants. Initial proteome estimations via total protein counts and label-free quantification highlight that entodiniomorph species Entodinium and Epidinium as well as the holotrichs Dasytricha and Isotricha comprise an extensive fraction of the total rumen metaproteome. Proteomic detection of protozoal metabolism such as hydrogenases (Dasytricha, Isotricha, Epidinium, Enoploplastron), carbohydrate-active enzymes (Epidinium, Diplodinium, Enoploplastron, Polyplastron), microbial predation (Entodinium) and volatile fatty acid production (Entodinium and Epidinium) was observed at increased levels in high methane-emitting animals. Despite certain protozoal species having well-established reputations for digesting starch, they were unexpectedly less detectable in low methane emitting-animals fed high starch diets, which were instead dominated by propionate/succinate-producing bacterial populations suspected of being resistant to predation irrespective of host. Finally, we reaffirmed our abovementioned observations in geographically independent datasets, thus illuminating the substantial metabolic influence that under-explored eukaryotic populations have in the rumen, with greater implications for both digestion and methane metabolism.
Topics: Animals; Cattle; Rumen; Proteomics; Ciliophora; Ruminants; Starch; Methane
PubMed: 37169869
DOI: 10.1038/s41396-023-01407-y -
Biology Apr 2024The rumen plays an essential role in the physiology and production of agriculturally important ruminants such as cattle. Functions of the rumen include fermentation,... (Review)
Review
The rumen plays an essential role in the physiology and production of agriculturally important ruminants such as cattle. Functions of the rumen include fermentation, absorption, metabolism, and protection. Cattle are, however, not born with a functional rumen, and the rumen undergoes considerable changes in size, histology, physiology, and transcriptome from birth to adulthood. In this review, we discuss these changes in detail, the factors that affect these changes, and the potential molecular and cellular mechanisms that mediate these changes. The introduction of solid feed to the rumen is essential for rumen growth and functional development in post-weaning calves. Increasing evidence suggests that solid feed stimulates rumen growth and functional development through butyric acid and other volatile fatty acids (VFAs) produced by microbial fermentation of feed in the rumen and that VFAs stimulate rumen growth and functional development through hormones such as insulin and insulin-like growth factor I (IGF-I) or through direct actions on energy production, chromatin modification, and gene expression. Given the role of the rumen in ruminant physiology and performance, it is important to further study the cellular, molecular, genomic, and epigenomic mechanisms that control rumen growth and development in postnatal ruminants. A better understanding of these mechanisms could lead to the development of novel strategies to enhance the growth and development of the rumen and thereby the productivity and health of cattle and other agriculturally important ruminants.
PubMed: 38666881
DOI: 10.3390/biology13040269 -
Nature Communications Aug 2023The diverse rumen virome can modulate the rumen microbiome, but it remains largely unexplored. Here, we mine 975 published rumen metagenomes for viral sequences, create...
The diverse rumen virome can modulate the rumen microbiome, but it remains largely unexplored. Here, we mine 975 published rumen metagenomes for viral sequences, create a global rumen virome database (RVD), and analyze the rumen virome for diversity, virus-host linkages, and potential roles in affecting rumen functions. Containing 397,180 species-level viral operational taxonomic units (vOTUs), RVD substantially increases the detection rate of rumen viruses from metagenomes compared with IMG/VR V3. Most of the classified vOTUs belong to Caudovirales, differing from those found in the human gut. The rumen virome is predicted to infect the core rumen microbiome, including fiber degraders and methanogens, carries diverse auxiliary metabolic genes, and thus likely impacts the rumen ecosystem in both a top-down and a bottom-up manner. RVD and the findings provide useful resources and a baseline framework for future research to investigate how viruses may impact the rumen ecosystem and digestive physiology.
Topics: Humans; Animals; Virome; Rumen; Microbiota; Caudovirales; Databases, Factual
PubMed: 37644066
DOI: 10.1038/s41467-023-41075-2 -
Frontiers in Veterinary Science 2023This study explores if promoting a complex rumen microbiota represents an advantage or a handicap in the current dairy production systems in which ruminants are...
INTRODUCTION
This study explores if promoting a complex rumen microbiota represents an advantage or a handicap in the current dairy production systems in which ruminants are artificially reared in absence of contact with adult animals and fed preserved monophyte forage.
METHODS
In order to promote a different rumen microbial diversity, a total of 36 newborn goat kids were artificially reared, divided in 4 groups and daily inoculated during 10 weeks with autoclaved rumen fluid (AUT), fresh rumen fluid from adult goats adapted to forage (RFF) or concentrate (RFC) diets, or absence of inoculation (CTL). At 6 months of age all animals were shifted to an oats hay diet to determine their ability to digest a low quality forage.
RESULTS AND DISCUSSION
Early life inoculation with fresh rumen fluid promoted an increase in the rumen overall microbial diversity which was detected later in life. As a result, at 6 months of age RFF and RFC animals had higher bacterial (+50 OTUs) and methanogens diversity (+4 OTUs) and the presence of a complex rumen protozoal community (+32 OTUs), whereas CTL animals remained protozoa-free. This superior rumen diversity and presence of rumen protozoa had beneficial effects on the energy metabolism allowing a faster adaptation to the forage diet, a higher forage digestion (+21% NDF digestibility) and an energetically favourable shift of the rumen fermentation pattern from acetate to butyrate (+92%) and propionate (+19%) production. These effects were associated with the presence of certain rumen bacterial taxa and a diverse protozoal community. On the contrary, the presence of rumen protozoa (mostly ) had a negative impact on the N metabolism leading to a higher bacterial protein breakdown in the rumen and lower microbial protein flow to the host based on purine derivatives urinary excretion (-17% to -54%). The inoculation with autoclaved rumen fluid, as source of fermentation products but not viable microbes, had smaller effects than using fresh inoculum. These findings suggest that enhancing rumen microbial diversity represents a desirable attribute when ruminants are fed forages in which the N supply does not represent a limiting factor for the rumen microbiota.
PubMed: 38179333
DOI: 10.3389/fvets.2023.1272835