Interspecies distances between propionic acid degraders and methanogens in syntrophic consortia for optimal hydrogen transfer

Abstract

A mixed culture from an anaerobic biowaste digester was enriched on propionate and used to investigate interspecies hydrogen transfer in dependence of spatial distances between propionate degraders and methanogens. From 20.3 mM propionate, 20.8 mM acetate and 15.5 mM methane were formed. Maximum specific propionate oxidation and methane formation rates were 49 and 23 mmol mg(-1) day(-1), respectively. Propionate oxidation was inhibited by only 20 mM acetate by about 50 %. Intermediate formate formation during inhibited methanogensis was observed. The spatial distribution and the biovolume fraction of propionate degraders and of methanogens in relation to the total population during aggregate formation were determined. Measurements of interbacterial distances were conducted with fluorescence in situ hybridization by application of group-specific 16S rRNA-targeted probes and 3D image analyses. With increasing incubation time, floc formation and growth up to 54 μm were observed. Propionate degraders and methanogens were distributed randomly in the flocs. The methanogenic biovolume fraction was high at the beginning and remained constant over 42 days, whereas the fraction of propionate degraders increased with time during propionate feeding. Interbacterial distances between propionate degraders and methanogens decreased with time from 5.30 to 0.29 μm, causing an increase of the maximum possible hydrogen flux from 1.1 to 10.3 nmol ml(-1) min(-1). The maximum possible hydrogen flux was always higher than the hydrogen formation and consumption rate, indicating that reducing the interspecies distance by aggregation is advantageous in complex ecosystems.

Efficient Metabolic Exchange and Electron Transfer within a Syntrophic Trichloroethene-Degrading Coculture of Dehalococcoides mccartyi 195 and Syntrophomonas wolfei

“…Previous studies reported that the syntrophic coculture of a propionate degrader and a hydrogenotrophic methanogen could form cell aggregates while growing on propionate for optimal hydrogen transfer (27,56). A similar phenomenon was also observed in mixed cultures containing propionate degraders and methanogens enriched from an anaerobic biowaste digester where flocs formed showing that reducing the interspecies distances by aggregation was advantageous in complex ecosystems (57). In engineered dechlorinating systems, D. mccartyi species have been observed in biofilms within a membrane bioreactor (58) and in bioflocs maintained in a continuous flow bioreactor fed with butyrate (13).…”

Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation

“…Recently, Felchner-Zwirello et al (2013) measured interbacterial distances between the propionate degraders and methanogens in syntrophic associations within granules that increased in size with time after inoculation of the growth media. According to these authors, the two microbial types find each other (probably by quorum sensing) and the aggregates increase in size over time, while the interspecies distances decrease from 5.30 to 0.29 mm.…”

Interspecies electron transfer in syntrophic methanogenic consortia: From cultures to bioreactors

“…Felchner-Zwirello et al [29] even observed that the interbacterial distances between propionate degraders and methanogens decreased from 5.30 to 0.29 μm when these microorganisms formed aggregates of up to 54 μm, causing an increase of the maximum possible H 2 flux from 1.1 to 10.3 nmol ml À 1 min À 1 . Therefore, reducing the interspecies distance by aggregation is supposedly advantageous in complex methanogenic system.…”

“…Besides, the formation of granules is advantageous for interspecies H 2 transfer. In granules, microbes are densely packed together, and the small distance between cells facilitates H 2 diffusion [29]. Intact granules display high methanogenic activities with fatty acids as substrates.…”

“…For formate, lower diffusivity, but higher solubility means that even bacteria farther away can still access it before it escapes the system or that unaggregated bacteria may be able to access the formate when cells get close enough during random motion. This may explain why in anaerobic granules, usually more evidences for interspecies hydrogen transfer rather than formate transfer have been found, and vice versa in anaerobic flocs, where the interspecies distance may have been larger [29,37]. Also, in some cases, when H 2 transfer is inhibited, the microbes involved would switch to formate transfer instead [29,59].…”