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How do earthworms and soil microbial communities interact to determine the fate of organic matter amendments to soil?

Omosigho, H. O. (2021) How do earthworms and soil microbial communities interact to determine the fate of organic matter amendments to soil? PhD thesis, University of Reading

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To link to this item DOI: 10.48683/1926.00115247

Abstract/Summary

The soil ecosystem harbours most of the global ecosystem’s biodiversity. The soil ecosystem contains a dynamic complex of microorganisms such as bacteria, microfauna (such as nematodes) and macrofauna (such as earthworms) and the non-living environment interacting as one functional unit. The biodiversity of this ecosystem plays a critical role in the provision of ecosystem functions and services. These ecosystem functions and services benefit humans. However, the rise in global challenges due to the rapid increase in human population, food shortage, the increase in our ecological footprint, rapid changes in the earth’s climate, the introduction of invasive exotic organisms capable of changing ecosystem biodiversity and the increasing incidences of droughts and other natural disasters, has resulted in a ‘trade off’ of ecosystem services and a reduction in soil biodiversity that is pivotal to the ecosystem functions and services. Earthworms are dominant members of soil invertebrate communities that play a key role in soil ecosystems’ functioning directly through impacts on soil structure and through the stimulation of soil microbial decompositional activities in bipores and as a result of soil ingestion and gut passage. The earthworm gut microbiome, mainly derived from ingested soil, is hypothesised to influence host physiology, for example, by enhancing nutrition through the provision of assimilable nutrients via depolymerisation. However, few studies have examined the nature of the relationship between earthworm health and function and their soil-derived gut microbiome’s diversity and composition. Also, we must improve our understanding of soil functioning especially given the pressures on the soil to deliver the services related to addressing the global challenges and the potential feedback between soil and the climate system into the future. The overall aim of this thesis was to increase our understanding about the importance of the earthworm - earthworm microbiome relationship in supporting critical soil ecosystem process such as organic matter mineralisation, explicitly paying attention to the feedback of the presence of the earthworm microbiome to the health and function of earthworms in supporting ecosystem processes. I used a novel antibiotic-based procedure to suppress Lumbricus terrestris earthworms’ gut microbiome in the pilot study. The use of antibiotics significantly reduced the abundance of L. terrestris-associated culturable microorganisms (P < 0.05), but 16S rRNA gene amplicon analysis showed no effect on earthworm microbiome alpha diversity and only subtle effects on beta diversity despite the pronounced knockdown of bacterial colony-forming units. The influence of the earthworm microbiome (antibiotic-treated or intact) and the soil microbiome (autoclaved or intact), and their interaction on L. terrestris feeding on, and preference for, three plant species litters (Lolium multiflorum (ryegrass), Quercus robur (oak) and Fraxinus excelsior(ash)) was then investigated. Across all earthworm microbiome x soil microbiome treatments, L. terrestris showed a greater preference for ash litter (P < 0.05) when compared to ryegrass and oak litter: a preference that may relate to differences in litter quality parameters (C: N and polyphenol content). However, disruption of either the soil microbiome, earthworm microbiome or soil and earthworm microbiome resulted in significantly (P < 0.05) reduced overall consumption of litter and a shift in litter preference to consume less oak litter. Finally, in a soil microbial diversity manipulation experiment, the research attempted to examine whether an increase in OM mineralisation in the presence of earthworms would depend on soil microbial diversity and could be linked to microbial diversity impacts on earthworm health. The aim to use the created soil with a gradient of microbial richness and L. terrestris as a test species to examine whether changes in soil microbial richness influence the effect of earthworms on organic matter decomposition to respired CO2 and whether any effects were linked to earthworm health status that may feedback to ecosystem functioning. Health status was evaluated by assessment of earthworm energy reserves through lipid, carbohydrate, and protein analysis. There was no effect of microbial diversity on earthworm functional impacts on SOM mineralization or earthworm health and therefore does not support the overall hypothesis for this thesis. Taken together, the findings currently suggest that the correlated properties of the soil microbiome that are important for earthworm health and functional role are abundance (biomass) and activity rather than the richness of species present or the presence of specific species or combinations of species. The insensitivity of both earthworm health and function to bacterial species loss suggests that the nature of the function provided by the ingested soil bacterial microbiome to its host is a functionally redundant one, because the functions provided are very generic, as many other microbial groups can provide similar function.

Item Type:Thesis (PhD)
Thesis Supervisor:Shaw, L.
Thesis/Report Department:School of Archaeology, Geography & Environmental Science
Identification Number/DOI:https://doi.org/10.48683/1926.00115247
Divisions:Science > School of Archaeology, Geography and Environmental Science > Department of Geography and Environmental Science
ID Code:115247

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