Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Hackmann, Timothy J.; Ngugi, David Kamanda; Firkins, J.L.; Tao, Junyi

doi:10.1111/1462-2920.13929

Cited by 48 publications

(60 citation statements)

References 46 publications

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“…While it would be possible to miss this gene from an individual single-cell genome, it is highly unlikely that we would specifically miss enolases from ∼10 genomes, which constitute the metagenome. So far, only 6 rumen bacterial genomes have been described that are lacking enolase; 5 from Firmicutes and 1 from Prevotella (38,39). An alternative, the methylglyoxal shunt, has been suggested to bypass enolase, where dihydroxyacetone phosphate is converted to pyruvate or L-lactate via methylglyoxal (38).…”

Section: Discussionmentioning

confidence: 99%

Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Treitli

Kolísko

Husník

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Lower termites harbor in their hindgut complex microbial communities that are involved in the digestion of cellulose. Among these are protists, which are usually associated with specific bacterial symbionts found on their surface or inside their cells. While these form the foundations of a classic system in symbiosis research, we still know little about the functional basis for most of these relationships. Here, we describe the complex functional relationship between one protist, the oxymonad Streblomastix strix, and its ectosymbiotic bacterial community using single-cell genomics. We generated partial assemblies of the host S. strix genome and Candidatus Ordinivivax streblomastigis, as well as a complex metagenome assembly of at least 8 other Bacteroidetes bacteria confirmed by ribosomal (r)RNA fluorescence in situ hybridization (FISH) to be associated with S. strix. Our data suggest that S. strix is probably not involved in the cellulose digestion, but the bacterial community on its surface secretes a complex array of glycosyl hydrolases, providing them with the ability to degrade cellulose to monomers and fueling the metabolism of S. strix. In addition, some of the bacteria can fix nitrogen and can theoretically provide S. strix with essential amino acids and cofactors, which the protist cannot synthesize. On the contrary, most of the bacterial symbionts lack the essential glycolytic enzyme enolase, which may be overcome by the exchange of intermediates with S. strix. This study demonstrates the value of the combined single-cell (meta)genomic and FISH approach for studies of complicated symbiotic systems.

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Section: Discussionmentioning

confidence: 99%

Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Treitli

Kolísko

Husník

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…In the reduction of crotonyl-CoA to butyryl-CoA, Fd ox is simultaneously reduced by a second molecule of NADH to Fd red 2− in a process called electron bifurcation (Buckel and Thauer, 2013; Figure 3A; see also section "The Role of Dihydrogen as an Intercellular Electron Carrier"). The oxidation of Fd red 2− so formed by electron bifurcation can result in H + extrusion and ATP generation by ETLP (Hackmann and Firkins, 2015;Hackmann et al, 2017).…”

Section: Carbohydrate Metabolism and Production Of Volatile Fatty Acidsmentioning

confidence: 99%

Metabolic Hydrogen Flows in Rumen Fermentation: Principles and Possibilities of Interventions

2020

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Rumen fermentation affects ruminants productivity and the environmental impact of ruminant production. The release to the atmosphere of methane produced in the rumen is a loss of energy and a cause of climate change, and the profile of volatile fatty acids produced in the rumen affects the post-absorptive metabolism of the host animal. Rumen fermentation is shaped by intracellular and intercellular flows of metabolic hydrogen centered on the production, interspecies transfer, and incorporation of dihydrogen into competing pathways. Factors that affect the growth of methanogens and the rate of feed fermentation impact dihydrogen concentration in the rumen, which in turn controls the balance between pathways that produce and incorporate metabolic hydrogen, determining methane production and the profile of volatile fatty acids. A basic kinetic model of competition for dihydrogen is presented, and possibilities for intervention to redirect metabolic hydrogen from methanogenesis toward alternative useful electron sinks are discussed. The flows of metabolic hydrogen toward nutritionally beneficial sinks could be enhanced by adding to the rumen fermentation electron acceptors or direct fed microbials. It is proposed to screen hydrogenotrophs for dihydrogen thresholds and affinities, as well as identifying and studying microorganisms that produce and utilize intercellular electron carriers other than dihydrogen. These approaches can allow identifying potential microbial additives to compete with methanogens for metabolic hydrogen. The combination of adequate microbial additives or electron acceptors with inhibitors of methanogenesis can be effective approaches to decrease methane production and simultaneously redirect metabolic hydrogen toward end products of fermentation with a nutritional value for the host animal. The design of strategies to redirect metabolic hydrogen from methane to other sinks should be based on knowledge of the physicochemical control of rumen fermentation pathways. The application of new -omics techniques together with classical biochemistry methods and mechanistic modeling can lead to exciting developments in the understanding and manipulation of the flows of metabolic hydrogen in rumen fermentation.

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“…A recent study of the metabolic pathways present in the genomes of a number of rumen bacteria identified several non-standard metabolic pathways that are not adequately represented in current databases (Hackmann et al, 2017). Hackmann and colleagues found that the recognized pathways for metabolizing pentose and hexose sugars to short-chain fatty acids do not adequately explain the fermentation products generated by a wide range of rumen bacteria (Hackmann et al, 2017). They found that 44% of these bacteria encoded atypical metabolic pathways and identified several that are completely novel.…”

Section: Composition Of the Rumen Microbiomementioning

confidence: 99%

Invited review: Application of meta-omics to understand the dynamic nature of the rumen microbiome and how it responds to diet in ruminants

Gruninger

Ribeiro

Cameron

et al. 2019

Animal

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Ruminants are unique among livestock due to their ability to efficiently convert plant cell wall carbohydrates into meat and milk. This ability is a result of the evolution of an essential symbiotic association with a complex microbial community in the rumen that includes vast numbers of bacteria, methanogenic archaea, anaerobic fungi and protozoa. These microbes produce a diverse array of enzymes that convert ingested feedstuffs into volatile fatty acids and microbial protein which are used by the animal for growth. Recent advances in high-throughput sequencing and bioinformatic analyses have helped to reveal how the composition of the rumen microbiome varies significantly during the development of the ruminant host, and with changes in diet. These sequencing efforts are also beginning to explain how shifts in the microbiome affect feed efficiency. In this review, we provide an overview of how meta-omics technologies have been applied to understanding the rumen microbiome, and the impact that diet has on the rumen microbial community. DO 2009. Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Applied and Environmental Microbiology 75, 7115-7124. Khafipour E, Plaizier JC, Aikman PC and Krause DO 2011. Population structure of rumen Escherichia coli associated with subacute ruminal acidosis (SARA) in dairy cattle. Journal of Dairy Science 94, 351-360. Kim M and Yu Z 2014. Variations in 16S rRNA-based microbiome profiling between pyrosequencing runs and between pyrosequencing facilities. PH 2015. Buccal swabbing as a noninvasive method to determine bacterial, archaeal, and eukaryotic microbial community structures in the rumen. Applied and Environmental Microbiology 81, 7470-7483. Koetschan C, Kittelmann S, Lu J, Al-Halbouni D, Jarvis GN, Müller T, Wolf M and Janssen PH 2014. Internal transcribed spacer 1 secondary structure analysis reveals a common core throughout the anaerobic fungi (Neocallimastigomycota). PLoS One 9, e91928. Kong Y, Teather R and Forster R 2010. Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiology Ecology 74, 612-622. Kumar S, Indugu N, Vecchiarelli B and Pitta DW 2015. Associative patterns among anaerobic fungi, methanogenic archaea, and bacterial communities in response to changes in diet and age in the rumen of dairy cows. Frontiers in Microbiology 6, 781.

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Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short‐chain fatty acids

Cited by 48 publications

References 46 publications

Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics

Metabolic Hydrogen Flows in Rumen Fermentation: Principles and Possibilities of Interventions

Invited review: Application of meta-omics to understand the dynamic nature of the rumen microbiome and how it responds to diet in ruminants

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