Hydrogen transfer between methanogens and fermentative heterotrophs in hyperthermophilic cocultures

Abstract

Abstract:Interactions involving hydrogen transfer were studied in a coculture of two hyperthermophilic microorganisms: Thermotoga maritima, an anaerobic heterotroph, and Methanococcus jannaschii, a hydrogenotrophic methanogen. Cell densities of T. maritima increased 10-fold when cocultured with M. jannaschii at 85°C, and the methanogen was able to grow in the absence of externally supplied H 2 and CO 2 . The coculture could not be established if the two organisms were physically separated by a dialysis membrane, suggesting the importance of spatial proximity. The significance of spatial proximity was also supported by cell cytometry, where the methanogen was only found in cell sorts at or above 4.5 µm in samples of the coculture in exponential phase. An unstructured mathematical model was used to compare the influence of hydrogen transport and metabolic properties on mesophilic and hyperthermophilic cocultures. Calculations suggest the increases in methanogenesis rates with temperature result from greater interactions between the methanogenic and fermentative organisms, as evidenced by the sharp decline in H 2 concentration in the proximity of a hyperthermophilic methanogen. The experimental and modeling results presented here illustrate the need to consider the interactions within hyperthermophilic consortia when choosing isolation strategies and evaluating biotransformations at elevated temperatures.

The Thermotoga maritima Phenotype Is Impacted by Syntrophic Interaction with Methanococcus jannaschii in Hyperthermophilic Coculture

“…One such example in certain anaerobic niches is the association between fermentative H 2 producers and methanogenic H 2 consumers, whereby the inhibitory H 2 formed as the by-product of sugar or peptide metabolism serves as an energy source for the generation of methane (26). This syntrophy can be found in niches ranging from the mammalian digestive tract (24) to anaerobic digesters used for domestic waste treatment (12).…”

“…Molecular hydrogen is also a key chemical species in hydrothermal environments (1) and likely supports this form of syntrophy; indeed, the pairing of hyperthermophilic fermentative anaerobes and methanogens in laboratory cocultures leads to higher growth rates and higher biomass yields of heterotrophs compared to monocultures (5). Furthermore, the growth rates of certain hyperthermophilic methanogens appear to be contingent upon the supply of available H 2 that can be maximized through close spatial proximity with fermentative anaerobes (26).…”

“…In syntrophic coculture with a hydrogenotrophic methanogen, such as Methanococcus jannaschii (7), this inhibition is relieved and cell population density is enhanced through the interspecies transfer of hydrogen (26). In addition to the utilization of sugars as carbon and energy sources (8,28), T. maritima also has been shown to produce exopolysaccharides (EPS) that serve as the basis for biofilms (35,36).…”

“…In addition to the utilization of sugars as carbon and energy sources (8,28), T. maritima also has been shown to produce exopolysaccharides (EPS) that serve as the basis for biofilms (35,36). In fact, when grown to high cell densities through coculture with the hyperthermophilic methanogen M. jannaschii, T. maritima produces EPS that leads to formation of stable cellular aggregates, which presumably facilitate interspecies H 2 transfer (26). Cellular aggregation was found to occur initially during mid-log phase in high-cell-density cocultures, apparently driven, at least in part, by quorum sensing and cyclic di-GMP regulation (18,37).…”

Positive, Neutral and Negative Interactions in Cocultures between Pyrococcus furiosus and Different Methanogenic Archaea

“…infernus cocultures both species benefit from the presence of the partner and propose a mutualistic interspecies relationship relying on the transfer of intermediate H 2 . This type of interaction has been also described in the cases of a Bacterium and a methanogenic Archaeon (eg, P. thermopropionicum and M. thermoautotrophicus or Thermotoga maritima and M. jannaschii) 16,27 and of two Archaea (P. furiosus and M. kandleri). 17 Considering the other cocultures of P. furiosus and the methanogens, an unanticipated finding was that the partners did not always benefit from each other.…”