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

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...

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Autores principales: DeBruyn, Jennifer M., Hoeland, Katharina M., Taylor, Lois S., Stevens, Jessica D., Moats, Michelle A., Bandopadhyay, Sreejata, Dearth, Stephen P., Castro, Hector F., Hewitt, Kaitlin K., Campagna, Shawn R., Dautartas, Angela M., Vidoli, Giovanna M., Mundorff, Amy Z., Steadman, Dawnie W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838218/
https://www.ncbi.nlm.nih.gov/pubmed/33519758
http://dx.doi.org/10.3389/fmicb.2020.608856
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author DeBruyn, Jennifer M.
Hoeland, Katharina M.
Taylor, Lois S.
Stevens, Jessica D.
Moats, Michelle A.
Bandopadhyay, Sreejata
Dearth, Stephen P.
Castro, Hector F.
Hewitt, Kaitlin K.
Campagna, Shawn R.
Dautartas, Angela M.
Vidoli, Giovanna M.
Mundorff, Amy Z.
Steadman, Dawnie W.
author_facet DeBruyn, Jennifer M.
Hoeland, Katharina M.
Taylor, Lois S.
Stevens, Jessica D.
Moats, Michelle A.
Bandopadhyay, Sreejata
Dearth, Stephen P.
Castro, Hector F.
Hewitt, Kaitlin K.
Campagna, Shawn R.
Dautartas, Angela M.
Vidoli, Giovanna M.
Mundorff, Amy Z.
Steadman, Dawnie W.
author_sort DeBruyn, Jennifer M.
collection PubMed
description 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.
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spelling pubmed-78382182021-01-28 Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles DeBruyn, Jennifer M. Hoeland, Katharina M. Taylor, Lois S. Stevens, Jessica D. Moats, Michelle A. Bandopadhyay, Sreejata Dearth, Stephen P. Castro, Hector F. Hewitt, Kaitlin K. Campagna, Shawn R. Dautartas, Angela M. Vidoli, Giovanna M. Mundorff, Amy Z. Steadman, Dawnie W. Front Microbiol Microbiology 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. Frontiers Media S.A. 2021-01-13 /pmc/articles/PMC7838218/ /pubmed/33519758 http://dx.doi.org/10.3389/fmicb.2020.608856 Text en Copyright © 2021 DeBruyn, Hoeland, Taylor, Stevens, Moats, Bandopadhyay, Dearth, Castro, Hewitt, Campagna, Dautartas, Vidoli, Mundorff and Steadman. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
DeBruyn, Jennifer M.
Hoeland, Katharina M.
Taylor, Lois S.
Stevens, Jessica D.
Moats, Michelle A.
Bandopadhyay, Sreejata
Dearth, Stephen P.
Castro, Hector F.
Hewitt, Kaitlin K.
Campagna, Shawn R.
Dautartas, Angela M.
Vidoli, Giovanna M.
Mundorff, Amy Z.
Steadman, Dawnie W.
Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title_full Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title_fullStr Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title_full_unstemmed Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title_short Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles
title_sort comparative decomposition of humans and pigs: soil biogeochemistry, microbial activity and metabolomic profiles
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838218/
https://www.ncbi.nlm.nih.gov/pubmed/33519758
http://dx.doi.org/10.3389/fmicb.2020.608856
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