Coaggregation Facilitates Interspecies Hydrogen Transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus

Abstract

A thermophilic syntrophic bacterium, Pelotomaculum thermopropionicum strain SI, was grown in a monoculture or coculture with a hydrogenotrophic methanogen, Methanothermobacter thermautotrophicus strain ⌬H. Microscopic observation revealed that cells of each organism were dispersed in a monoculture independent of the growth substrate. In a coculture, however, these organisms coaggregated to different degrees depending on the substrate; namely, a large fraction of the cells coaggregated when they were grown on propionate, but relatively few cells coaggregated when they were grown on ethanol or 1-propanol. Field emission-scanning electron microscopy revealed that flagellum-like filaments of SI cells played a role in making contact with ⌬H cells. Microscopic observation of aggregates also showed that extracellular polymeric substance-like structures were present in intercellular spaces. In order to evaluate the importance of coaggregation for syntrophic propionate oxidation, allowable average distances between SI and ⌬H cells for accomplishing efficient interspecies hydrogen transfer were calculated by using Fick's diffusion law. The allowable distance for syntrophic propionate oxidation was estimated to be approximately 2 m, while the allowable distances for ethanol and propanol oxidation were 16 m and 32 m, respectively. Considering that the mean cell-to-cell distance in the randomly dispersed culture was approximately 30 m (at a concentration in the mid-exponential growth phase of the coculture of 5 ؋ 10 7 cells ml ؊1 ), it is obvious that close physical contact of these organisms by coaggregation is indispensable for efficient syntrophic propionate oxidation.In anaerobic digestors, organic matter is converted to methane and CO 2 via various intermediates (1, 27). Among the most important intermediate metabolites are volatile fatty acids (VFAs), such as acetate, propionate, and butyrate, and it has been reported that accumulation of VFAs results in a significant decrease in the methane production efficiency in such digestors (16,17,37,38). VFAs are, however, unfavorable substrates for anaerobes, since oxidation of these substrates to H 2 and CO 2 (or formate) is endoergonic under standard conditions (i.e., the changes in the Gibbs free energy are positive [⌬G°Ј Ͼ 0]) (Table 1) and is thermodynamically feasible only when the H 2 partial pressure (or formate concentration) is kept low (3,11,29,34). For instance, thermodynamic estimation has predicted that H 2 partial pressures as low as 10 Pa and 100 Pa are necessary for the oxidation of propionate and butyrate, respectively (29, 34). Since H 2 and formate are scavenged mainly by the carbonate respiration of methanogenic archaea, syntrophic association of VFA-oxidizing bacteria (called syntrophs) and methanogenic archaea is considered indispensable for efficient VFA oxidation (27, 36).As described previously, syntrophic VFA oxidation depends on interspecies electron (as H 2 and formate) transfer. Researchers have suggested that close physical contact between syntro...

Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms

“…SEM images revealed that P. thermopropionicum produced pilus-like filaments when it was grown in monocultures on fumarate and in cocultures with Methanothermobacter thermoautotropicus on propionate (Fig. 4C), as described (12). STM images and tunneling spectroscopy confirmed that these filaments were highly electrically conductive and were composed of bundles of individual electrically conductive filaments, each measuring between Ϸ10 and 20 nm in diameter (Fig.…”

Straw- and slurry-associated prokaryotic communities differ during co-fermentation of straw and swine manure

“…NH 4 + -N in the supernatant was quantified using indophenol blue method as previously described (Tzollas et al 2010). VFAs were detected by a GC equipped with a polar capillary column (DB-FFAP, 30 m×0.25 mm×0.25 μm) and a flame ionization detector (FID) as previously described (Ishii et al 2005). The chemical compositions of the straw at initiation stage and peak II were analyzed as described previously (Hess et al 2011).…”

Rumen prokaryotic communities of ruminants under different feeding paradigms on the Qinghai-Tibetan Plateau

“…For VFAs and NH 3 -N measurements, the rumen fluid was centrifuged at 13,000 × g for 10 min. VFAs were analysed by an Agilent 6850 gas chromatograph (Agilent Technologies Inc., Santa Clara, CA, USA) equipped with a polar capillary column (HP-FFAP, 30 m × 0.25 mm × 0.25 m) and a flame ionization detector (FID), as previously described [29]. NH 3 -N in the supernatant was quantified using a continuous flow analyser (SKALAR San++, Skalar Co., Netherlands).…”