Soil microbial communities in microaggregates are less affected by top-down effects of collembolans than those in macroaggregates

Trophic regulation of microbial communities is receiving growing interest in soil ecology. Most studies investigated the effect of higher trophic levels on microbial communities at the bulk soil level. However, microbes are not equally accessible to consumers. They may be hidden in small pores and thus protected from consumers, suggesting that trophic regulation may depend on the localization of microbes within the soil matrix. As microaggregates (< 250 µm) usually are more stable than macroaggregates (> 250 µm) and embedded in the latter, we posit that they will be less affected by trophic regulations than larger aggregates. We quantified the effect of four contrasting species of collembolans (Ceratophysella denticulata, Protaphorura fimata, Folsomia candida, Sinella curviseta) on the microbial community composition in macro- (250 µm – 2mm) and microaggregates (50 – 250 µm). To do so, we re-built consumer-prey systems comprising remaining microbial background (post-autoclaving), fungal prey (Chaetomium globosum), and collembolan species (added as single species or combined). After three months, we quantified microbial community composition using phospholipid fatty acid markers (PLFAs). We found that the microbial communities in macroaggregates were more affected by the addition of collembolans than the communities in microaggregates. In particular, the fungal-to-bacterial (F:B) ratio significantly decreased in soil macroaggregates in the presence of collembolans. In the microaggregates, the F:B ratio remained lower and unaffected by collembolan inoculation. Presumably, fungal hyphae were more abundant in macroaggregates because they offered more habitat space for them, and the collembolans reduced fungal abundance because they consumed them. On the contrary, microaggregates presumably contained microbial communities protected from consumers. In addition, collembolans increased the formation of macroaggregates but did not influence their stability, despite their negative effect on fungal abundance, a well-known stabilizing agent. Overall, we show that trophic interactions between microbial communities and collembolans depend on the aggregate size class considered and, in return, soil macroaggregation is affected by these trophic interactions.