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.