Syntrophobacteraceae‐affiliated species are major propionate‐degrading sulfate reducers in paddy soil

Abstract

Methane is an important greenhouse gas and propionate is next to acetate the main intermediate (average 23%) of the carbon flow to CH in paddy fields. Sulfate (e.g., gypsum) application can reduce CH emissions up to 70%. However, the effect of gypsum application on propionate degradation and the microbial communities involved are not well understood. Therefore, we studied propionate-dependent sulfate reduction in anoxic microcosms of paddy soils from Italy and the Philippines, combining 16S rRNA and dissimilatory sulfite reductase (dsrB) gene profiling and co-occurrence network analysis. Sulfate was stoichiometrically reduced in treatments with propionate addition, while CH production was partially suppressed. Methane production but not sulfate reduction were suppressed and acetate accumulated after addition of methyl fluoride or fluoroacetate. With methyl fluoride in the presence of sulfate, the accumulated acetate was consumed after the depletion of propionate. Simultaneously, the relative abundances of Syntrophobacteraceae and Desulfovibrionaceae were significantly enhanced, while fluoroacetate repressed Desulfobulbaceae in both soils. Syntrophobacter 16S rRNA and dsrB gene copy numbers were also remarkably increased with gypsum amendment. Network analysis of both 16S rRNA and dsrB genes illustrated a strong co-occurrence of operational taxonomic units belonging to Syntrophobacteraceae, Desulfovibrionaceae and Desulfobulbaceae. In summary, Syntrophobacteraceae affiliated species were identified as the major propionate-dependent sulfate reducers in paddy soil. They (together with Desulfobulbaceae) oxidized propionate directly to acetate and CO , or coupled the oxidation syntrophically to H /formate-utilizing Desulfovibrionaceae. The transiently accumulating acetate was preferentially consumed by acetoclastic Methanosarcinaceae.

Identification of Syntrophobacteraceae as major acetate‐degrading sulfate reducing bacteria in Italian paddy soil

“…), indicating that SRB capable of acetate utilization were gradually activated and eventually outcompeted acetoclastic methanogens for the limited acetate. This observation agrees with previous studies on paddy soil (Achtnich et al ., ; Denier van der Gon et al ., ; Lueders and Friedrich, ; Gauci et al ., ; Liu and Conrad, ). Acetate was applied at a concentration of 5.5 mM, which is commonly reached in rice field soil (Glissmann and Conrad, ; Penning and Conrad, ; Rui et al ., ).…”

“…However, it was speculated that Desulfovirga spp. oxidize propionate preferentially to acetate and CO 2 , and oxidize the accumulated acetate only after the depletion of propionate (Liu and Conrad, ). Excretion of acetate has also been observed for other completely oxidizing SRB, but the excreted acetate may subsequently be oxidized further if other substrates are limiting (Rabus et al ., ).…”

“…Most likely, acetate‐utilizing SRB were initially present at low numbers or as spores and became active only after germination. However, in some studies, SRB and methanogens apparently did not compete for acetate (Nozoe, ; Scheid et al ., ; Liu and Conrad, ). This was probably the case, when organic substrates were available that SRB preferentially used instead of acetate.…”

“…A large diversity of SRB has been detected in paddy soil (Wind et al ., ; Scheid et al ., ; Stubner, ; He et al ., ; Wörner et al ., ; Liu and Conrad, ). The species of SRB, which are known to use acetate as electron donor mainly belong to Desulfobacteraceae and the genus Desulfotomaculum .…”

“…However, the taxonomic identity of these novel lineages and their functions with regard to sulfate reduction and acetate degradation in paddy soils remain unclear. Also Syntrophobacteraceae have been identified as SRB in rice field soil (He et al ., ; Wörner et al ., ; Liu and Conrad, ) and other freshwater environments (Pester et al ., ), but they have not been proposed being acetotrophic.…”