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Earthworms are ecological engineers that can contribute to the displacement of biological control agents such as the entomopathogenic nematodes (EPNs) and fungi (EPF). However, a previous study showed that the presence of cutaneous excreta (CEx) and feeding behavior of the earthworm species Eisenia fetida (Haplotaxida: Lumbricidae) compromise the biocontrol efficacy of certain EPN species by reducing, for example, their reproductive capability. Whether this phenomenon is a general pattern for the interaction of earthworms-entomopathogens is still unknown. We hypothesized that diverse earthworm species might differentially affect EPN and EPF infectivity and reproductive capability. Here we investigated the interaction of different earthworm species (Eisenia fetida, Lumbricus terrestris, and Perionyx excavatus) (Haplotaxida) and EPN species (Steinernema feltiae, S. riojaense, and Heterorhabditis bacteriophora) (Rhabditida) or EPF species (Beauveria bassiana and Metarhizium anisopliae) (Hypocreales), in two independent experiments. First, we evaluated the application of each entomopathogen combined with earthworms or their CEx in autoclaved soil. Hereafter, we studied the impact of the earthworms' CEx on entomopathogens applied at two different concentrations in autoclaved sand. Overall, we found that the effect of earthworms on entomopathogens was species-specific. For example, E. fetida reduced the virulence of S. feltiae, resulted in neutral effects for S. riojaense, and increased H. bacteriophora virulence. However, the earthworm P. excavates increased the virulence of S. feltiae, reduced the activity of H. bacteriophora, at least at specific timings, while S. riojaense remained unaffected. Finally, none of the EPN species were affected by the presence of L. terrestris. Also, the exposure to earthworm CEx resulted in a positive, negative or neutral effect on the virulence and reproduction capability depending on the earthworm-EPN species interaction. Concerning EPF, the impact of earthworms was also differential among species. Thus, E. fetida was detrimental to M. anisopliae and B. bassiana after eight days post-exposure, whereas Lumbricus terrestris resulted only detrimental to B. bassiana. In addition, most of the CEx treatments of both earthworm species decreased B. bassiana virulence and growth. However, the EPF M. anisopliae was unaffected when exposed to L. terrestris CEx, while the exposure to E. fetida CEx produced contrasting results. We conclude that earthworms and their CEx can have positive, deleterious, or neutral impacts on entomopathogens that often coinhabit soils, and that we must consider the species specificity of these interactions for mutual uses in biological control programs. Additional studies are needed to verify these interactions under natural conditions., MC is supported by a Moroccan scholarship of the Ministry of National Education, Vocational Training, Higher Education and Scientific Research, and the travel assistance associated with the grant CSIC ICOOP + 2018 grant (COOPA20231). RBP is financed with an FPI contract (CAR-2018) by the Department of Economic Development and Innovation of The Government of La Rioja (Spain). IVD is supported with an FPI-UR fellowship by the Universidad de La Rioja (Spain). RCH is awarded by Ramon y Cajal contract award (RYC-2016-19939) of the Government of Spain. This study is supported by CSIC I-COOP + 2018 grant (COOPA20231).

Earthworms are considered as a rich microhabitat for the growth and proliferation of diverse soil microorganisms. Hence, earthworms' associated bacteria attracted interest due to their high metabolic profiles and benefits to soil fertility and plant growth. In this study, we aimed to isolate for the first-time aerobic bacteria present in the chloragogenous tissue of the earthworm Apporectodea molleri and test their Plant Growth-Promoting abilities and their resistance to heavy metals (Mn, Zn, Cu, Cd, and Ni). The 16S rRNA gene sequencing revealed the affiliation of the fifteen isolates to six main bacterial genera: Enterobacter, Citrobacter, Aeromonas, Pseudomonas, Bacillus, Terribacillus. These strains displayed different plant growth promoting traits (e.g., indole-3-acetic acid IAA, siderophores, nitrogen fixation, phosphate, and potassium solubilization), in addition, they were able to resist differently to heavy metals. Bacillus strains were most effective as three strains, namely B. subtilis strain TC34; B. circulans strain TC7 and Bacillus sp. strain TC10, were positive to all PGP traits and resisted to all heavy metals. This study illustrates the potential of bacteria from the chloragogenous tissue to exhibit multiple properties, which can be related to the functional feature of this tissue to stock metabolites and neutralize toxic elements.

In vitro application of total gross extract of earthworms (Lumbricus terrestris) in diverse dilutions stimulates rhizogenesis in young bean plants (Phaseolus vulgaris). The observed effect is similar to that of indol acetic acid, a well-known growth enhancer in plants, used here as a control in various concentrations. Fragmentation of worm extract by column chromatography results in three groups of fractions. Only the polar group of fractions has a significant rhizogenous effect, which is, however, inferior to that observed in the presence of total gross extract of worms or of indol acetic acid. Gross extract analyses using thin layer chromatography, with appropriate chromatography systems and reagents, revealed that indol acetic acid is not present, but is probably replaced by other indol-derived substances that have a neutral to basic chromatographic behaviour. These presumed indol-derived substances are identified as methyl-tryptophane, serotonin, and hydroxy-indol acetic acid. Analyses using mass spectrometry combined with gas chromatography, following fragmentation and purification of the group of rhyzogenous fractions, have revealed the presence of hydroxy-indol carboxylic acid, which seems to take the form of several isomeres.[Journal translation]