Regulation of soil organic matter dynamics and microbial activity by endogeic earthworms

Earthworms are among the most important members of the soil invertebrate fauna in temperate ecosystems. Through burrow construction, mixing of organic matter and mineral soil, comminution of organic matter and casting they beneficially affect soil structure and chemical properties, and thus the biomass, activity and community composition of microorganisms. Microorganisms, particularly bacteria and fungi, are the primarily decomposers of organic matter in soils. Since earthworms control the microbial community they also affect the fate of soil organic matter which may lead either to its mobilization or stabilization. This study investigates the role of different factors presumably controlling the interaction of earthworms and microorganisms with regard to the stabilization and mobilization of soil organic matter. The effect of endogeic earthworms (Octolasion tyrtaeum (Savigny)) and the availability of clay on the mobilization and stabilization of 14C-labelled catechol mixed into an arable and a forest soil was investigated. Production of 14CO2 and accumulation of 14C in humic fractions of casts and the non-processed soils were determined. Octolasion tyrtaeum did not affect 14CO2-C production in the forest soil, but increased it early in the arable soil; clay counteracted the effect of O. tyrtaeum in the arable soil. Clay and O. tyrtaeum did not affect integration of 14C into the humic fractions of the forest soil. In contrast, in the arable soil O. tyrtaeum increased the amount of 14C in the labile fractions, whereas clay increased it in the humin fraction, indicating that endogeic earthworms and clay are only of little importance in soils with high organic matter content, high clay content and high microbial biomass, but contrarily affect phenolic compounds in poor soils. Endogeic earthworms strongly increase microbial activity and thus mineralization of phenolic compounds, whereas clay decreases it by binding phenolic compounds when passing through the earthworm gut. The effect of cutting of shoots of white clover (Trifolium repens L.) and perennial ryegrass (Lolium perenne L.) on the availability of soluble carbon in the rhizosphere, and on the biomass and activity of soil microorganisms and juveniles of the endogeic earthworm species O. tyrtaeum (Savigny) and Aporrectodea caliginosa (Savigny) were studied. Both plant species increased microbial biomass in the soil, but microbial activity remained unaffected. Although defoliation increased the availability of carbon in the rhizosphere as indicated by the increase in microbial biomass, the biomass of both earthworm species decreased during the experiment, suggesting that earthworms were unable to exploit the microbial carbon pool in soil, rather, rhizosphere microorganisms appeared to have effectively competed with endogeic earthworms and exploited root carbon exudates. The interaction of saprophytic fungi and O. tyrtaeum on the translocation and stabilization of litter derived carbon (13C/15N labelled rye leaves) into the upper layer of an arable soil was investigated in a microcosm experiment. Phospholipid fatty acids and ergosterol were used as marker molecules to determine the effects of earthworms on bacterial and fungal abundance and microbial community composition. The results indicate that saprophytic fungi translocate and stabilize litter derived carbon in their mycelial network in the upper mineral soil. Endogeic earthworms reduce fungal biomass by grazing and thereby counteract the fungal stabilization of carbon. In addition, earthworms reduce bacterial biomass in the soil while mainly competing with Gram-negative bacteria for labile carbon resources. The flux of bacterial carbon (13C labelled Serratia marcescens cells) through the soil microbial community as affected by the passage through the gut of endogeic earthworms A. caliginosa was investigated by means of terminal-restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA gene fragments and rRNA stable isotope probing (SIP). Production of 13CO2-C was strongly increased in presence of A. caliginosa and in casts compared to the soil. Microbial communities in casts and soil after one day of incubation were almost similar and consist of eleven different bacterial lineages, with Proteobacteria and Actinobacteria being the most abundant; however they differed in the abundance of Acidobacteria, Firmicutes and Planctomycetes. After six days microbial community in the soil was almost similar to that of casts at day one. The clone library of the casts, in contrast, consisted of only five different lineages and was dominated by members of the phylum Firmicutes, predominantly Staphylococcus spp. , indicating that the passage through the gut of endogeic earthworms considerably changes the activity and composition of the microbial community, and the mineralization and incorporation of bacterial carbon. The results of the present study document that endogeic earthworms increase the mineralization of soil organic matter by promoting, feeding on or competing with specific microorganisms in the soil. The effect, however, also depends on abiotic soil conditions such as soil texture.