Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection

Seshadri, Rekha; Leahy, Sinead C.; Attwood, Graeme T.; Teh, Koon Hoong; Lambie, Suzanne C.; Cookson, Adrian L.; Eloe‐Fadrosh, Emiley A.; Pavlopoulos, Georgios A.; Hadjithomas, Michalis; Varghese, Neha; Páez-Espino, David; Perry, Rechelle; Henderson, Gemma; Creevey, Christopher J.; Terrapon, Nicolas; Lapébie, Pascal; Drula, Élodie; Lombard, Vincent; Rubin, Edward M.; Kyrpides, Nikos C.; Henrissat, Bernard; Woyke, Tanja; Ivanova, Natalia; Kelly, William J.

doi:10.1038/nbt.4110

Cited by 454 publications

(587 citation statements)

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“…Improving our understanding of the rumen microbiota provides opportunities for knowledgebased strategies aiming at enhancing efficacy in ruminant production while minimizing its negative effect on the environment. Great advances on microbiota functions in the rumen has been obtained by extensive genome sequencing of cultured rumen bacteria and archaea (Hungate1000 project) [5] and by assembling of draft genomes from metagenomic data [6,7].…”

Section: Abstract: Rumen; Metagenome; Herbivory; Carbohydrate-activementioning

confidence: 99%

“…For the bacterial MAGs, 39% could be annotated to the order level but only 2.5% (8 MAGs) to the genus level; all belonging to Prevotella. These rumen MAGs were compared to the Hungate1000 genomes [5] and to the 913 MAGs reported from Scottish cattle [6] Ninety-six (30%) out of 324…”

Section: Construction Of a Bovine Rumen Prokaryotic Gene Catalogmentioning

confidence: 99%

“…The 324 MAGs were present in all four diet groups from our validation cohort; about 10% of reads from the 77 cattle dataset mapped to these MAGs. For genomes from the Hungate1000 project [5,9], which are representative of the diversity of cultured rumen bacteria and archaea, the mapping rate was 5.4%, whereas the mapping rate for the largest MAGs collection of Stewart et al [6] was around 13%. In contrast, only 0.1% of reads mapped to the 15 metagenomic species described by Hess et al [14] ( Figure 1c).…”

Section: Construction Of a Bovine Rumen Prokaryotic Gene Catalogmentioning

confidence: 99%

“…This expands the size of the CAZyme set of Stewart et al by almost 8 times and represents the most extensive source of reference CAZyme sequences in the rumen niche so far. It is noted that 32,755 degradative CAZymes are present in the Hungate1000 reference genomes [5].…”

Section: Carbohydrate Active Enzymes In the Bovine Rumen Metagenomementioning

confidence: 99%

“…Mapping ratios of 77 samples to 913 genomes were calculated based on [6]. Mapping ratios of 77 samples to Hungate1000 isolates were calculated based on [5].…”

Section: Figure Legendsmentioning

confidence: 99%

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A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment

Huang

Ramayo-Caldas

et al. 2018

Preprint

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BackgroundThe rumen microbiota provides essential services to its host and, through its role in ruminant production, contributes to human nutrition and food security. A thorough knowledge of the genetic potential of rumen microbes will provide opportunities for improving the sustainability of ruminant production systems. The availability of gene reference catalogs from gut microbiomes has advanced the understanding of the role of the microbiota in health and disease in humans and other mammals. In this work, we established a catalog of reference prokaryote genes from the bovine rumen. ResultsUsing deep metagenome sequencing we identified 13,825,880 non-redundant prokaryote genes from the bovine rumen. Compared to human, pig and mouse gut metagenome catalogs, the rumen is larger and richer in functions and microbial species associated with the degradation of plant cell wall material and production of methane. Genes encoding enzymes catalyzing the breakdown of plant polysaccharides showed a particularly high richness that is otherwise impossible to infer from available genomes or shallow metagenomics sequencing.The catalog expands by several folds the dataset of carbohydrate-degrading enzymes described in the rumen. Using an independent dataset from a group of 77 cattle fed 4 common dietary regimes, we found that only <0.1% of genes were shared by all animals, which contrast with a large overlap for functions, i.e. 63% for KEGG functions. Different diets induced differences in the relative abundance rather than the presence or absence of genes explaining the great adaptability of cattle to rapidly adjust to dietary changes. Conclusions

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Section: Abstract: Rumen; Metagenome; Herbivory; Carbohydrate-activementioning

confidence: 99%

Section: Construction Of a Bovine Rumen Prokaryotic Gene Catalogmentioning

confidence: 99%

Section: Construction Of a Bovine Rumen Prokaryotic Gene Catalogmentioning

confidence: 99%

Section: Carbohydrate Active Enzymes In the Bovine Rumen Metagenomementioning

confidence: 99%

“…Mapping ratios of 77 samples to 913 genomes were calculated based on [6]. Mapping ratios of 77 samples to Hungate1000 isolates were calculated based on [5].…”

Section: Figure Legendsmentioning

confidence: 99%

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A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment

Huang

Ramayo-Caldas

et al. 2018

Preprint

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Rumen

Mackie¹,

McSweeney²,

Aminov³

2022

Encyclopedia of Life Sciences

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The rumen is a large pregastric fermentation compartment (foregut) which maintains a diverse but concentrated population of anaerobic bacteria, protozoa and fungi that are responsible for a variety of degradative and fermentative reactions. During this process, biodegradable organic matter, mainly plant cell wall polymers, are converted into volatile fatty acids and microbial biomass which supply energy and protein to the host (ruminant) animal. An important reason for the evolution of foregut fermentation is detoxification of phytotoxins (of plant origin) and mycotoxins (of fungal origin). The concept of interspecies hydrogen transfer in which the mutually beneficial unidirectional transfer of hydrogen from a hydrogen‐producing to a hydrogen‐utilising bacteria in a coupled reaction that maintains low partial pressures makes the transfer process thermodynamically feasible is important in ruminal methanogenesis. Currently, modern ‘Omics’ technologies are being applied to the study of rumen microbial ecology, genomics, (meta)genomics and (meta)transcriptomics. Key Concepts The ruminant is a specialised model of foregut fermentation. The most obvious feature of ruminants is rumination that enables reduction in particle size and exposure of maximal surface area to microbial attack in the large foregut fermentation tank called the rumen. In the rumen, biodegradable organic matter, mainly plant cell wall polymers, are converted into volatile fatty acids and microbial biomass which supply energy and protein to the host (ruminant) animal. The rumen microbial population is characterised by its high population density, wide diversity and complexity of interactions. The rumen contains representatives of all three domains of life (Bacteria, Archaea and Eukarya). Bacteria are predominant but a variety of ciliate protozoa and anaerobic fungi are widely distributed. Fermentation of substrates in the rumen yields short‐chain volatile fatty acids (primarily acetic, propionic and butyric acids), carbon dioxide, methane, ammonia and occasionally lactic acid. Based on cultivation methods, plant cell wall hydrolysis is carried out by specialist bacteria (mainly the genera Ruminococcus and Fibrobacter ), ciliate protozoa and anaerobic fungi. However, cultivation‐independent approaches suggest other groups of uncultivated Firmicutes may also be important in fibre degradation. Protein is extensively degraded in the rumen and used to resynthesise bacterial protein. Many rumen bacteria preferentially utilise ammonia and 60–80% of bacterial protein is synthesised from this precursor. Phytotoxins occur widely in many common feeds, including grain, protein supplements and forages. An important reason for the evolution of foregut fermentation is detoxification of phytotoxins and mycotoxins. In the rumen, methanogenesis from carbon dioxide reduction by hydrogen dominates terminal electron flow. The concept of interspecies hydrogen transfer in which the mutually beneficial unidirectional transfer of hydrogen from a hydrogen‐producing to a hydrogen‐utilising bacteria in a coupled reaction that maintains low partial pressures makes the transfer process thermodynamically feasible. Methane emissions from enteric fermentation in livestock, mainly ruminants account for the single largest agricultural source of anthropogenic greenhouse gas emissions. These considerations have led to an increase in efforts to identify technologies to mitigate ruminant methane emissions. The advent of genomics (the mapping and sequencing of genomes and analysis of gene and gene function) has revolutionised the biological sciences. Currently, ‘omics’ technologies are being applied to the study of rumen microbial genomics, (meta)genomics and (meta)transcriptomics.

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