Thermodynamic Control on Biogeography and Functioning of Rare-Biosphere Propionate Syntrophs in Paddy Field Soils

Abstract

Background Global biogeochemical processes are not only gauged by dominant taxa of soil microbiome but also depend on the critical functions of “rare biosphere” members. Here we evaluated the biogeographical pattern of “rare biosphere” propionate-oxidizing syntrophs in 113 paddy soil samples collected across eastern China. Results The relative abundance, functioning capacity and growth potential of propionate-oxidizing syntrophs were analyzed to provide a panoramic view of syntroph biogeographical distribution at the continental scale. The relative abundances of four syntroph genera, Syntrophobacter, Pelotomaculum, Smithella and Syntrophomonas were significantly greater at the warm low latitudes than at the cool high latitudes. Correspondingly, the functioning potential of propionate degradation was greater in the low latitude soils compared with the high latitude soils. The slow rate of propionate degradation in high latitude soils resulted in a greater fold change in increase of the relative abundance, probably due to the growth rate-yield tradeoff relationship. The mean annual temperature (MAT) is the most important factor shaping the biogeographical pattern of propionate-oxidizing syntrophs, with the next factor to be the total S content (TS) in soil. Conclusions We suggest that the effect of MAT is related to the Gibbs free energy change, in which the endergonic tension of propionate oxidation is leveraged with the increase of MAT. The TS effect is likely due to that some propionate syntrophs can facultatively perform sulfate respiration.

Syntrophic propionate-oxidizing bacteria in methanogenic systems

“…In one study on rice field soil, Syntrophbacter was the most active SPOB at 15°C, whereas at 30°C Pelotomaculum and Smithella were also involved in degradation of propionate (Gan et al 2012). A biogeographical study spanning temperature zones demonstrated a correlation between higher temperature and higher propionate degradation rates and higher relative abundance of SPOB (Jin et al 2021). In Arctic peat, syntrophic propionate oxidation has been identified as the rate-limiting step for methane production at temperatures below 7°C, whereas at higher temperatures the propionate pool is depleted at a higher rate (Tveit et al 2015).…”

“…As these oxidized sulfur species are energetically more favorable electron acceptors than CO 2 , methanogens will be outcompeted. In habitats with restricted availability of electron acceptors other than CO 2 , such as biogas reactors, rice fields, peatlands, and oil reservoirs, propionate will instead be converted to methane (Chen et al 2020;Jin et al 2021;Kaspar and Wuhrmann 1978;Schmidt et al 2016). In these methanogenic ecosystems, propionate degradation proceeds through a closely interlinked multispecies cooperation between syntrophic propionate-oxidizing bacteria (SPOB) and hydrogen (H 2 )/formate-and acetate-utilizing methanogens (Stams 1994) (Fig.…”