Abstract

The positive effect of earthworms on soil processes and plant growth has been extensively documented. The capacity of earthworms to decompose organic matter has been attributed to the microbial communities that inhabit their digestive track or the structures they build, which in turn contribute to make up the drilosphere, a hotspot for microbial activity. However, how earthworms modify the structure of soil microbial communities and how these changes affect soil microbial processes is still unclear. Do earthworms reduce microbial abundance and activity because they feed on microorganisms or do they select and stimulate specific microbial groups? We hypothesise that “the effect of earthworms on nutrient cycling and plant growth is not only a direct effect but is mainly mediated indirectly, via modifications of the microbial community.” The objective of this review is to synthesize the existing literature concerning the influence of earthworms on the structure and function of soil microbial communities, as well as to understand how earthworm-induced changes in the soil microbiota would in turn impact soil processes, particularly those occurring in the rhizosphere and involved in plant growth and health. Recent reports have shown that specific bacterial groups consistently increase in soils where earthworms are present, regardless of the earthworm functional group. The extent of this increase seems to be dependent upon the type of substrate under study. Our synthesis also reveals that endogeic and anecic earthworms regularly induce an increase in soil nutrients, whilst this positive effect is not as evident in the presence of epigeic earthworms. The effect of earthworms on nutrient cycling has been further investigated with microbial functional genes, although existing reports largely focus on nitrogen cycling. Earthworms seem to enhance denitrification, most likely through the increase in organic compounds due to organic matter decomposition. By enhancing soil nutrient availability, earthworms indirectly promote plant growth, which has also been attributed to the induction of signal molecules. However, no experiment to date has been able to prove a direct causal relationship between specific signal molecules, earthworms and plant growth promotion. Finally, we propose a framework for earthworm-microbiota interactions and recommend further research.

Highlights

  • Earthworms are considered as ecosystem engineers that play an important role in shaping soil structure and cycling nutrients (Blouin et al, 2013)

  • Earthworms are known to play a critical role in ecological processes, through their improvement of soil structure, nutrient cycling and plant growth

  • Evidence shows that earthworms contribute towards the structuring of soil microbial communities, either directly through their ingestion or indirectly through a priming effect resulting from an increase of available labile substances

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Summary

Introduction

Earthworms are considered as ecosystem engineers that play an important role in shaping soil structure and cycling nutrients (Blouin et al, 2013). Earthworms promote litter decomposition, nitrogen (N) mineralisation and water infiltration, as a result of their feeding and burrowing habits (Baker, 2007), and deeply affect soil properties (Hättenschwiler and Gasser, 2005) They play a crucial role in the provision of soil ecosystem services (Lavelle et al, 2016). Earthworms are builders of habitats for other organisms, which establishes them as physical or allogenic engineers (Jones et al, 1994; Lavelle et al, 1997, 2016) These building activities constitute an input of organic matter to the soil and a pathway for the stabilization of soil organic carbon (Corg) through the formation of organomineral aggregates (Deeb et al, 2017). In addition to shaping soil structure, earthworms have an important impact on soil organic matter dynamics and microorganisms in their gut, casts and drilosphere (Andriuzzi et al, 2016) and are identified as biochemical (Lavelle et al, 2016) or autogenic ecosystem engineers (Lawton and Jones, 1995)

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