Modelling thermodynamic feedback on the metabolism of hydrogenotrophic methanogens

Lynch, Thomasin; Wang, Y.; Brunt, Bruce van; Pacheco, D.; Janssen, Peter H.

doi:10.1016/j.jtbi.2019.05.018

Cited by 13 publications

(20 citation statements)

References 35 publications

(41 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…They estimated kinetic, thermodynamic, and growth parameters and predicted that in the long term only one methanogen would survive in tri-cultures. Similar conclusions were reached in another recent theoretical analysis (Lynch et al, 2019). Muñoz-Tamayo et al (2019) discussed that, as the rumen harbors a diverse community of methanogens, ecological factors such as sensitivity to pH, location in association to fluid or particles, and endosymbiosis with protozoa can contribute to explain the existence of diversity despite of thermodynamic and kinetic advantages of some methanogens over others.…”

Section: The Competition For Dihydrogensupporting

confidence: 81%

“…Pure cultures of rumen hydrogenotrophs, such as those isolated in the Hungate 1000 Project (Kelly, 2016), could be screened for kinetic parameters of H 2 incorporation and H 2 thresholds. This information could be used to predict the outcome of the competition for H 2 between methanogens and other hydrogenotrophs with models similar to the ones generated by Muñoz-Tamayo et al (2019) and Lynch et al (2019) for competition between methanogens. The ability of nonmethanogenic hydrogenotrophs to compete for H 2 could be evaluated in co-culture with methanogens if they are also fermentative H 2 producers themselves (e.g., R. flavefaciens, S. ruminantium), or in tri-cultures with methanogens and a H 2producing organism if they incorporate H 2 but do not produce it (e.g., F. succinogenes, Succinivibrio dextrinosolvens, Succinimonas amylolytica, reductive acetogens).…”

Section: Discussionmentioning

confidence: 99%

“…For example, methanogens possessing cytochromes can generate more ATP per mole of CH 4 produced and have higher growth yields when growing on elevated H 2 concentration compared to methanogens without cytochromes, but on the other hand they have greater H 2 thresholds. Methylotrophic methanogens of the order Methanosarcinales have cytochromes and they have evolved to live in environments with low H 2 concentration by acquiring the capacity of using one carbon compounds as substrates for methanogenesis (Thauer et al, 2008;Vanwonterghem et al, 2016;Lynch et al, 2019).…”

Section: Effects Of Metabolic Hydrogen Flows On Microbial Growthmentioning

confidence: 99%

See 2 more Smart Citations

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

2020

View full text Add to dashboard Cite

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.

show abstract

Section: The Competition For Dihydrogensupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Section: Effects Of Metabolic Hydrogen Flows On Microbial Growthmentioning

confidence: 99%

See 1 more Smart Citation

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

2020

View full text Add to dashboard Cite

show abstract

“…Moreover, since the motivation for this study is the behavior of hydrogenotrophs in the human GIT, substrate concentrations comparable to concentrations expected in this environment were deemed appropriate. The substrate ranges investigated were: lactate 0-25 mM h −1 (Vernia et al, 1988;Macfarlane and Macfarlane, 2012;Pham et al, 2017); sulphate 0-10 mM h −1 (Florin et al, 1991;Lewis and Cochrane, 2007); and hydrogen 0-50 mM h −1 (Carbonero et al, 2012;Wolf et al, 2016). The range of dilution rates was 0.01-0.15 h −1 , as only acetogen survival is possible above this range under current model assumptions.…”

Section: Numerical Analysis Of the Model Under Continuous Culture Conmentioning

confidence: 99%

“…There exist models for each of these functional groups in monoculture and for certain co-culture combinations. A thermodynamics-based monoculture model for SRB growth and metabolism has been published (Noguera et al, 1998) and there exist numerous models for microbial methanogenesis both in monoculture and in co-culture with a SRB (see Junicke et al, 2016;Lynch et al, 2019, andMuñoz-Tamayo et al, 2019 for recent examples). Tamayo et al (2008) and D'Hoe et al (2018) have produced models for reductive acetogens in monoculture and co-culture, respectively.…”

Section: Introductionmentioning

confidence: 99%

Competition for Hydrogen Prevents Coexistence of Human Gastrointestinal Hydrogenotrophs in Continuous Culture

et al. 2020

View full text Add to dashboard Cite

Understanding the metabolic dynamics of the human gastrointestinal tract (GIT) microbiota is of growing importance as research continues to link the microbiome to host health status. Microbial strains that metabolize hydrogen have been associated with a variety of both positive and negative host nutritional and health outcomes, but limited data exists for their competition in the GIT. To enable greater insight into the behaviour of these microbes, a mathematical model was developed for the metabolism and growth of the three major hydrogenotrophic groups: sulphate-reducing bacteria (SRB), methanogens and reductive acetogens. In batch culture simulations with abundant sulphate and hydrogen, the SRB outcompeted the methanogen for hydrogen due to having a half-saturation constant 10 6 times lower than that of the methanogen. The acetogen, with a high model threshold for hydrogen uptake of around 70 mM, was the least competitive. Under high lactate and zero sulphate conditions, hydrogen exchange between the SRB and the methanogen was the dominant interaction. The methanogen grew at 70% the rate of the SRB, with negligible acetogen growth. In continuous culture simulations, both the SRB and the methanogen were washed out at dilution rates above 0.15 h −1 regardless of substrate availability, whereas the acetogen could survive under abundant hydrogen conditions. Specific combinations of conditions were required for survival of more than one hydrogenotroph in continuous culture, and survival of all three was not possible. The stringency of these requirements and the inability of the model to simulate survival of all three hydrogenotrophs in continuous culture demonstrates that factors outside of those modelled are vital to allow hydrogenotroph coexistence in the GIT.

show abstract

Review: Towards the next-generation models of the rumen microbiome for enhancing predictive power and guiding sustainable production strategies

Muñoz-Tamayo,

Davoudkhani,

Fakih

et al. 2023

animal

View full text Add to dashboard Cite

Modelling thermodynamic feedback on the metabolism of hydrogenotrophic methanogens

Cited by 13 publications

References 35 publications

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

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

Competition for Hydrogen Prevents Coexistence of Human Gastrointestinal Hydrogenotrophs in Continuous Culture

Review: Towards the next-generation models of the rumen microbiome for enhancing predictive power and guiding sustainable production strategies

Contact Info

Product

Resources

About