Microbiota succession influences nematode physiology in a beetle microcosm ecosystem

• Published in: Nature communications Vol. 15; no. 1; pp. 5137 - 11
• Main Authors: Lo, Wen-Sui, Sommer, Ralf J., Han, Ziduan
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 15.06.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 38; 45/23; 45/91; 631/326/2565/2134; 631/326/2565/2142; Animals; Bacteria; Bacteria - classification; Bacteria - genetics; Bacteria - metabolism; Beetles; Cellulases - genetics; Cellulases - metabolism; Coleoptera - microbiology; Coleoptera - physiology; Decay; Ecological niches; Ecosystem; Genes; Humanities and Social Sciences; Insects; Lipids; Metagenomics; Microbiota; Microbiota - physiology; Microorganisms; multidisciplinary; Nematoda - microbiology; Nematoda - physiology; Nematodes; Nutrients; Physiology; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-49513-5

Unravelling the multifaceted and bidirectional interactions between microbiota and host physiology represents a major scientific challenge. Here, we utilise the nematode model, Pristionchus pacificus , coupled to a laboratory-simulated decay process of its insect host, to mimic natural microbiota succession and investigate associated tripartite interactions. Metagenomics reveal that during initial decay stages, the population of vitamin B-producing bacteria diminishes, potentially due to a preferential selection by nematodes. As decay progresses to nutrient-depleted stages, bacteria with smaller genomes producing less nutrients become more prevalent. Lipid utilisation and dauer formation, representing key nematode survival strategies, are influenced by microbiota changes. Additionally, horizontally acquired cellulases extend the nematodes’ reproductive phase due to more efficient foraging. Lastly, the expressions of Pristionchus species-specific genes are more responsive to natural microbiota compared to conserved genes, suggesting their importance in the organisms’ adaptation to its ecological niche. In summary, we show the importance of microbial successions and their reciprocal interaction with nematodes for insect decay in semi-artificial ecosystems. This study uses decomposing beetle grubs to replicate the natural microbial habitat of a nematode model organism. The approach enables exploration of interactions between nematodes and their microbiota and was used to show the importance of microbial successions and their reciprocal interaction with nematodes for insect decay.