Functional Assemblages of Collembola Determine Soil Microbial Communities and Associated Functions

Abstract

Soil processes such as decomposition are mainly performed by soil biota. Although soils worldwide are extremely biodiverse, the relationship between decomposers (fauna and microorganisms), and ecosystem function is poorly understood. Collembola are abundant and ubiquitous microarthropods that are found in terrestrial ecosystems. They can affect the amount of biomass and the activity of microbial communities, either directly through selectively feeding on fungi and bacteria, or indirectly by dissemination of microbial propagules, and the alteration of nutrient availability. However, despite the functional role they play in belowground food webs, the interactions between natural assemblages of soil microbes and Collembola receive little attention. This study, conducted in microcosm conditions, examines the effects of two distinct natural assemblages of functional groups of Collembola (ep-and euedaphic) upon microbial communities using PLFA markers and their associated soil functions (e.g., enzymatic activities and C mineralization rate) over a 2-month period. Our principal objective was to determine whether different functional groups of Collembola had varying effects on microbial soil community abundance, structure and activity, resulting in potentially important effects on ecosystem processes. Our findings show that the interactions of the functional groups of Collembola with microbial communities vary significantly whether they are alone or combined. A distinct response in the composition of the microbial communities was found at the end of the 2-month period. The communities were significantly different from each other in terms of PLFA marker composition. We found that the epedaphic species were related to and promoted Gram+ bacteria whereas euedaphic species were related to Gram-bacterial markers. This had further repercussions on soil function, such as nutrient recycling. Combining both functional groups did not lead to a complementary effect on soil microbial properties, with a drastically different outcome between the first and the second month of the experiment. Additional research dealing with the interactions between decomposers using natural assemblages will help to predict the functional outcomes of soil biota structure and composition.

Protists and collembolans alter microbial community composition, C dynamics and soil aggregation in simplified consumer–prey systems

“…In fact, the composition of the bacterial community was significantly modified by collembolans. Presumably, these changes were due to selective feeding of H. nitidus on certain bacterial strains and/or through modifications in competitive interactions between certain bacterial strains and C. globosum (Lussenhop, 1992;Coulibaly et al, 2019;Thakur and Geisen, 2019). In addition, other non-consumptive effects may have occurred.…”

“…Soil microbial communities have long been thought to be mainly structured by abiotic filters (Griffiths et al, 2011) and plant inputs (bottom-up regulation;Myers et al, 2001), whereas the importance of higher trophic levels has so far only been seen as a major but understudied factor (Thakur and Geisen, 2019) of crucial importance for C cycling (Crowther et al, 2015;Filser et al, 2016;Grandy et al, 2016;Morriën et al, 2017). Several soil organisms can consume bacteria and fungi, including protists, nematodes and collembolans.…”

“…Several soil organisms can consume bacteria and fungi, including protists, nematodes and collembolans. These consumers often modify the biomass and the composition of the microbial community (Rønn et al, 2002;Djigal et al, 2004;Rosenberg et al, 2009;Perez et al, 2013;Jiang et al, 2017;Geisen et al, 2018;Coulibaly et al, 2019). Such modifications are thought to result directly from consumptive effects, i.e.…”

“…However, other non-consumptive effects are also at stake (Bradford, 2016) as indicated by experimental evidence. For example, the release of N by protists and nematodes (Griffiths and Bardgett, 1997) and the excretion of urine or faeces by microarthropods (Cragg and Bardgett, 2001;Milcu et al, 2006), as well as their necromass (Coleman et al, 2002), modify the quality of organic matter processed by soil microorganisms, with expected effects on their biomass and composition. The comminution of plant debris (Lussenhop, 1992) as well as the transport of microbes on the body of soil microarthropods (Griffiths and Bardgett, 1997;Bardgett et al, 1998;Gormsen et al, 2004) is also assumed to contribute to non-consumptive effects of microarthropods on soil microbial communities.…”

“…Further, consumers of soil microorganisms can modify microbial activity and physiology, such as the production of bacterial EPSs (Matz and Kjelleberg, 2005;Queck et al, 2006) and antibiotic compounds (Jousset and Bonkowski, 2010). Variations in enzymatic activity of wood-decomposing fungi in the presence of microbivores have also been reported (Crowther et al, 2015). Overall, the influence of trophic interactions on the structure and activity of soil microbial communities is an active research topic (Jiang et al, 2017;Thakur and Geisen, 2019;Lucas et al, 2020).…”