Thermodynamics shapes the biogeography of propionate-oxidizing syntrophs in paddy field soils.

Abstract

Soil biogeochemical processes are not only gauged by the dominant taxa in the microbiome but also depend on the critical functions of its rare biosphere members. Here, we evaluated the biogeographical pattern of rare biosphere propionate-oxidizing syntrophs in 113 paddy soil samples collected across China. The relative abundance, activity and growth potential of propionate-oxidizing syntrophs were analysed 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, propionate degradation was faster in the low latitude soils compared with the high latitude soils. The low rate of propionate degradation in the high latitude soils resulted in a greater increase of the total syntroph relative abundance, probably due to their initial low relative abundances and the longer incubation time for propionate consumption. The mean annual temperature (MAT) is the most important factor shaping the biogeographical pattern of propionate-oxidizing syntrophs, with the next factor being the soil s total sulfur content (TS). We suggest that the effect of MAT is related to the thermodynamic conditions, in which the endergonic constraint of propionate oxidation is leveraged with the increase of MAT. The TS effect is likely due to the ability of some propionate syntrophs to facultatively perform sulfate respiration.