The soil microbial food web revisited: Predatory myxobacteria as keystone taxa?

AbstractTrophic interactions in the microbial food web of soils are crucial for nutrient and carbon cycling. Traditionally, protozoa are considered the major micropredators of bacteria in soil. However, some prokaryotes, such as Myxobacteria and Bdellovibrio are also famous for bacterivorous life style. Until recently, it was impossible to assess the abundance of pro- and eukaryotic micropredators in soils simultaneously. Using a metatranscriptomic three-domain profiling of small subunit ribosomal RNA we investigated the abundance of bacterivores in 28 datasets from eleven European mineral and organic soils of different climatic zones. In all soils, Myxobacteria comprised a significant proportion from 4 – 19% of prokaryotic 16S rRNA transcripts and more than 60% of all bacterivores in most soils. Haliangiaceae and Polyangiaceae were most abundant, while the name-giving Myxococcaceae were barely present. Other bacterial predators like Bdellovibrio were low abundant. Also Protozoan micropredator 18S rRNA transcripts, e.g. from Cercozoa, Amoebozoa and Ciliophora, were on average less abundant, especially in mineral soils. Nematodes were even less abundant. In addition, we applied a longitudinal approach to identify bacterivores during beech litter colonisation. Here, Myxobacteria showed prey-dependent, protozoa-like community dynamics during colonisation. Thus, their broad prey range and high abundance suggests a major influence of Myxobacteria on structuring the prokaryotic community composition in soil, and might warrant their classification as keystone taxon. Our results suggest the presence of an ecologically important “bacterial loop” in soil food webs, independent of protozoa and nematodes.

There is widespread concern that cessation of grazing in historically grazed ecosystems is causing biotic homogenization and biodiversity loss. Here, we used 12 montane grassland sites along an 800-km north-south gradient across the United Kingdom, to test whether cessation of grazing affects local ɑ- and β-diversity of belowground food webs. We show that cessation of grazing leads to strongly decreased ɑ-diversity of both soil microbial and faunal diversity. In contrast, the β-diversity varied between groups of soil organisms. While soil microbial communities exhibited increased homogenization after cessation of grazing, we observed decreased homogenization for soil fauna after cessation of grazing. Overall, our results indicate that grazer exclusion from historically grazed montane grasslands has far-ranging consequences for the diversity and composition of belowground food webs, and underscore the importance of grazers for maintaining the diversity of belowground communities, which play a central role in ecosystem functioning.

ABSTRACT The understanding of microbial interactions and trophic networks is a prerequisite for the elucidation of the turnover and transformation of organic materials in soils. To elucidate the incorporation of biomass carbon into a soil microbial food web, we added 13C-labeled Escherichia coli biomass to an agricultural soil and identified those indigenous microbes that were specifically active in its mineralization and carbon sequestration. rRNA stable isotope probing (SIP) revealed that uncultivated relatives of distinct groups of gliding bacterial micropredators (Lysobacter spp., Myxococcales, and the Bacteroidetes) lead carbon sequestration and mineralization from the added biomass. In addition, fungal populations within the Microascaceae were shown to respond to the added biomass after only 1 h of incubation and were thus surprisingly reactive to degradable labile carbon. This RNA-SIP study identifies indigenous microbes specifically active in the transformation of a nondefined complex carbon source, bacterial biomass, directly in a soil ecosystem.

There are great concerns about the impacts of soil biodiversity loss on ecosystem functions and services such as nutrient cycling, food production, and carbon storage. A diverse community of soil organisms that together comprise a complex food web mediates such ecosystem functions and services. Recent advances have shed light on the key drivers of soil food web structure, but a conceptual integration is lacking. Here, we explore how human-induced changes in plant community composition influence soil food webs. We present a framework describing the mechanistic underpinnings of how shifts in plant litter and root traits and microclimatic variables impact on the diversity, structure, and function of the soil food web. We then illustrate our framework by discussing how shifts in plant communities resulting from land-use change, climatic change, and species invasions affect soil food web structure and functioning. We argue that unravelling the mechanistic links between plant community trait composition and soil food webs is essential to understanding the cascading effects of anthropogenic shifts in plant communities on ecosystem functions and services.