Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles

Abstract

Vertebrate decomposition processes have important ecological implications and, in the case of human decomposition, forensic applications. Animals, especially domestic pigs (Sus scrofa), are frequently used as human analogs in forensic decomposition studies. However, recent research shows that humans and pigs do not necessarily decompose in the same manner, with differences in decomposition rates, patterns, and scavenging. The objective of our study was to extend these observations and determine if human and pig decomposition in terrestrial settings have different local impacts on soil biogeochemistry and microbial activity. In two seasonal trials (summer and winter), we simultaneously placed replicate human donors and pig carcasses on the soil surface and allowed them to decompose. In both human and pig decomposition-impacted soils, we observed elevated microbial respiration, protease activity, and ammonium, indicative of enhanced microbial ammonification and limited nitrification in soil during soft tissue decomposition. Soil respiration was comparable between summer and winter, indicating similar microbial activity; however, the magnitude of the pulse of decomposition products was greater in the summer. Using untargeted metabolomics and lipidomics approaches, we identified 38 metabolites and 54 lipids that were elevated in both human and pig decomposition-impacted soils. The most frequently detected metabolites were anthranilate, creatine, 5-hydroxyindoleacetic acid, taurine, xanthine, N-acetylglutamine, acetyllysine, and sedoheptulose 1/7-phosphate; the most frequently detected lipids were phosphatidylethanolamine and monogalactosyldiacylglycerol. Decomposition soils were also significantly enriched in metabolites belonging to amino acid metabolic pathways and the TCA cycle. Comparing humans and pigs, we noted several differences in soil biogeochemical responses. Soils under humans decreased in pH as decomposition progressed, while under pigs, soil pH increased. Additionally, under pigs we observed significantly higher ammonium and protease activities compared to humans. We identified several metabolites that were elevated in human decomposition soil compared to pig decomposition soil, including 2-oxo-4-methylthiobutanoate, sn-glycerol 3-phosphate, and tryptophan, suggesting different decomposition chemistries and timing between the two species. Together, our work shows that human and pig decomposition differ in terms of their impacts on soil biogeochemistry and microbial decomposer activities, adding to our understanding of decomposition ecology and informing the use of non-human models in forensic research.