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Metabolic Interactions of a Chain Elongation Microbiome.

ABSTRACT: Carbon chain elongation (CCE), a reaction within the carboxylate platform that elongates short-chain to medium-chain carboxylates by mixed culture, has attracted worldwide interest. The present study provides insights into the microbial diversity and predictive microbial metabolic pathways of a mixed-culture CCE microbiome on the basis of a comparative analysis of the metagenome and metatranscriptome. We found that the microbial structure of an acclimated chain elongation microbiome was a highly similar to that of the original inoculating biogas reactor culture; however, the metabolic activities were completely different, demonstrating the high stability of the microbial structure and flexibility of its functions. Additionally, the fatty acid biosynthesis (FAB) pathway, rather than the well-known reverse β-oxidation (RBO) pathway for CCE, was more active and pivotal, though the FAB pathway had more steps and consumed more ATP, a phenomenon that has rarely been observed in previous CCE studies. A total of 91 draft genomes were reconstructed from the metagenomic reads, of which three were near completion (completeness, >97%) and were assigned to unknown strains of Methanolinea tarda, Bordetella avium, and Planctomycetaceae The last two strains are likely new-found active participators of CCE in the mixed culture. Finally, a conceptual framework of CCE, including both pathways and the potential participators, was proposed.IMPORTANCE Carbon chain elongation means the conversion of short-chain volatile fatty acids to medium-chain carboxylates, such as n-caproate and n-caprylate with electron donors under anaerobic condition. This bio-reaction can both expand the resource of valuable biochemicals and broaden the utilization of low-grade organic residues in a sustainable biorefinery context. Clostridium kluyveri is conventionally considered model microbe for carbon chain elongation which uses the reverse β-oxidation pathway. However, little is known about the detailed microbial structure and function of other abundant microorganism in a mixed culture (or open culture) of chain elongation. We conducted the comparative metagenomic and metatranscriptomic analysis of a chain elongation microbiome to throw light on the underlying functional microbes and alternative pathways.

SUBMITTER: Han W

PROVIDER: S-EPMC6210121 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Medium-chain carboxylates (MCC) derived from biomass biorefining are attractive biochemicals to uncouple the production of a wide array of products from the use of non-renewable sources. Biological conversion of biomass-derived lactate during secondary fermentation can be steered to produce a variety of MCC through chain elongation. We explored the effects of zero-valent iron nanoparticles (nZVI) and lactate enantiomers on substrate consumption, product formation and microbiome composition in batch lactate-based chain elongation. In abiotic tests, nZVI supported chemical hydrolysis of lactate oligomers present in concentrated lactic acid. In fermentation experiments, nZVI created favorable conditions for either chain-elongating or propionate-producing microbiomes in a dose-dependent manner. Improved lactate conversion rates and n-caproate production were promoted at 0.5-2 g nZVI⋅L-1 while propionate formation became relevant at ≥ 3.5 g nZVI⋅L-1. Even-chain carboxylates (n-butyrate) were produced when using enantiopure and racemic lactate with lactate conversion rates increased in nZVI presence (1 g⋅L-1). Consumption of hydrogen and carbon dioxide was observed late in the incubations and correlated with acetate formation or substrate conversion to elongated products in the presence of nZVI. Lactate racemization was observed during chain elongation while isomerization to D-lactate was detected during propionate formation. Clostridium luticellarii, Caproiciproducens, and Ruminococcaceae related species were associated with n-valerate and n-caproate production while propionate was likely produced through the acrylate pathway by Clostridium novyi. The enrichment of different potential n-butyrate producers (Clostridium tyrobutyricum, Lachnospiraceae, Oscillibacter, Sedimentibacter) was affected by nZVI presence and concentrations. Possible theories and mechanisms underlying the effects of nZVI on substrate conversion and microbiome composition are discussed. An outlook is provided to integrate (bio)electrochemical systems to recycle (n)ZVI and provide an alternative reducing power agent as durable control method.

Project description:The gut microbiome is a complex microbial community that has a significant influence on the host. Microbial interactions in the gut are mediated by dietary substrates, especially complex polysaccharides. In this environment, breakdown products from larger carbohydrates and short chain fatty acids are commonly shared among gut microbes. Understanding the forces that guide microbiome development and composition is important to determine its role in health and in the intervention of the gut microbiome as a therapeutic tool. Recently, modeling approaches such as genome-scale models and time-series analyses have been useful to predict microbial interactions. In this study, a bottom-up approach was followed to develop a mathematical model based on microbial growth equations that incorporate metabolic sharing and inhibition. The model was developed using experimental in vitro data from a system comprising four microorganisms of the infant gut microbiome (Bifidobacterium longum subsp. infantis, Lactobacillus acidophilus, Escherichia coli, and Bacteroides vulgatus), one substrate (fructooligosaccharides, FOS), and evaluating two metabolic products (acetate and lactate). After parameter optimization, the model accurately predicted bacterial abundance in co-cultures from mono-culture data. In addition, a good correlation was observed between the experimental data with predicted FOS consumption and acid production. B. infantis and L. acidophilus were dominant under these conditions. Further model validation included cultures with the four-species in a bioreactor using FOS. The model was able to predict the predominance of the two aforementioned species, as well as depletion of acetate and lactate. Finally, the model was tested for parameter identifiability and sensitivity. These results suggest that variations in microbial abundance and activities in the infant gut were mainly explained by metabolic interactions, and could be properly modeled using Monod kinetics with metabolic interactions. The model could be scaled to include data from larger consortia, or be applied to microbial communities where sharing metabolic resources is important in shaping bacterial abundance. Moreover, the model could be useful in designing microbial consortia with desired properties such as higher acid production.

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Project description:BackgroundRecent studies have provided insights into the persistence and succession of microbes aboard the International Space Station (ISS), notably the dominance of Klebsiella pneumoniae. However, the interactions between the various microbes aboard the ISS and how they shape the microbiome remain to be clearly understood. In this study, we apply a computational approach to predict possible metabolic interactions in the ISS microbiome and shed further light on its organization.ResultsThrough a combination of a systems-based graph-theoretical approach, and a constraint-based community metabolic modeling approach, we demonstrated several key interactions in the ISS microbiome. These complementary approaches provided insights into the metabolic interactions and dependencies present amongst various microbes in a community, highlighting key interactions and keystone species. Our results showed that the presence of K. pneumoniae is beneficial to many other microorganisms it coexists with, notably those from the Pantoea genus. Species belonging to the Enterobacteriaceae family were often found to be the most beneficial for the survival of other microorganisms in the ISS microbiome. However, K. pneumoniae was found to exhibit parasitic and amensalistic interactions with Aspergillus and Penicillium species, respectively. To prove this metabolic prediction, K. pneumoniae and Aspergillus fumigatus were co-cultured under normal and simulated microgravity, where K. pneumoniae cells showed parasitic characteristics to the fungus. The electron micrography revealed that the presence of K. pneumoniae compromised the morphology of fungal conidia and degenerated its biofilm-forming structures.ConclusionOur study underscores the importance of K. pneumoniae in the ISS, and its potential positive and negative interactions with other microbes, including potential pathogens. This integrated modeling approach, combined with experiments, demonstrates the potential for understanding the organization of other such microbiomes, unravelling key organisms and their interdependencies. Video Abstract.

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Metabolic Interactions of a Chain Elongation Microbiome.

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