Variations in bacterial taxonomic profiles and potential functions in response to the gut transit of earthworms (Eisenia fetida) feeding on cow manure

Abstract

Earthworms play an important role in the organic matter decomposition in terrestrial ecosystems. Earthworms interact directly with the microorganisms to affect the organic matter decomposition via gut transit, i.e., the digestion and assimilation of organic matter in the foregut and midgut and its excretion by the hindgut. However, how the microbial community ingested by earthworms respond to the transit processes in different gut segments of earthworms is not clear. We used composted cow manure to feed earthworms and sampled vermicompost and the contents of foregut, midgut and hindgut for bacterial 16S rRNA gene sequencing analysis. We observed that earthworm gut transit decreased the abundances of the dominant phyla Proteobacteria and Bacteroidetes but increased Actinobacteria, Chloroflexi and Acidobacteria. The alpha diversity of bacterial community in midgut was the lowest of the different gut segments, and the bacterial community structure of the foregut was significantly different from the midgut and hindgut. The enrichment analysis results revealed different selective stimulatory and inhibitory effects on the ingested bacterial community in the different gut segments, which extended to vermicompost. The FAPROTAX data indicated that C and N metabolic microbes were enriched in the earthworm gut. Microbes involved in fermentation and methanogenesis were enriched in the hindgut, and denitrification microbes were enriched in the foregut. The N metabolism microbes in vermicompost were significantly enriched after the stimulation of earthworm gut transit (P < 0.05), and the pathogenic microbes of animals and plants were inhibited. Combined with the results of subsequent correlation and biochemical analyses, earthworm gut transit significantly altered the structure and function of the bacterial community to accelerate the degradation and mineralization of organic matter and the enrichment of phosphorus and potassium. Our study suggests that the gut transit process of earthworms plays an important role in regulating organic matter dynamics in terrestrial ecosystems.