A conserved interdomain microbial network underpins cadaver decomposition despite environmental variables

Zachary M Burcham; Aeriel D Belk; Bridget B McGivern; Amina Bouslimani; Parsa Ghadermazi; Cameron Martino; Liat Shenhav; Anru R Zhang; Pixu Shi; Alexandra Emmons; Heather L Deel; Zhenjiang Zech Xu; Victoria Nieciecki; Qiyun Zhu; Michael Shaffer; Morgan Panitchpakdi; Kelly C Weldon; Kalen Cantrell; Asa Ben-Hur; Sasha C Reed; Greg C Humphry; Gail Ackermann; Daniel McDonald; Siu Hung Joshua Chan; Melissa Connor; Derek Boyd; Jake Smith; Jenna M S Watson; Giovanna Vidoli; Dawnie Steadman; Aaron M Lynne; Sibyl Bucheli; Pieter C Dorrestein; Kelly C Wrighton; David O Carter; Rob Knight; Jessica L Metcalf

doi:10.1038/s41564-023-01580-y

A conserved interdomain microbial network underpins cadaver decomposition despite environmental variables

Nat Microbiol. 2024 Mar;9(3):595-613. doi: 10.1038/s41564-023-01580-y. Epub 2024 Feb 12.

Authors

Zachary M Burcham^{1

2}, Aeriel D Belk^{1

3}, Bridget B McGivern⁴, Amina Bouslimani⁵, Parsa Ghadermazi⁶, Cameron Martino⁷, Liat Shenhav^{8

9

10}, Anru R Zhang^{11

12}, Pixu Shi¹¹, Alexandra Emmons¹, Heather L Deel¹³, Zhenjiang Zech Xu¹⁴, Victoria Nieciecki^{1

13}, Qiyun Zhu^{7

15

16}, Michael Shaffer⁴, Morgan Panitchpakdi⁵, Kelly C Weldon⁵, Kalen Cantrell¹⁷, Asa Ben-Hur¹⁸, Sasha C Reed¹⁹, Greg C Humphry⁷, Gail Ackermann⁷, Daniel McDonald⁷, Siu Hung Joshua Chan⁶, Melissa Connor²⁰, Derek Boyd^{21

22}, Jake Smith^{21

23}, Jenna M S Watson²¹, Giovanna Vidoli²¹, Dawnie Steadman²¹, Aaron M Lynne²⁴, Sibyl Bucheli²⁴, Pieter C Dorrestein⁵, Kelly C Wrighton⁴, David O Carter²⁵, Rob Knight^{7

17

26

27}, Jessica L Metcalf^{28

29

30}

Affiliations

¹ Department of Animal Sciences, Colorado State University, Fort Collins, CO, USA.
² Department of Microbiology, University of Tennessee, Knoxville, TN, USA.
³ Department of Animal Sciences, Auburn University, Auburn, AL, USA.
⁴ Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, USA.
⁵ Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, San Diego, CA, USA.
⁶ Department of Chemical and Biological Engineering, Colorado State University, Fort Collins, CO, USA.
⁷ Department of Pediatrics, University of California San Diego, La Jolla, California, USA.
⁸ Center for Studies in Physics and Biology, Rockefeller University, New York, NY, USA.
⁹ Institute for Systems Genetics, New York Grossman School of Medicine, New York University, New York, NY, USA.
¹⁰ Department of Computer Science, New York University, New York, NY, USA.
¹¹ Department of Biostatistics and Bioinformatics, Duke University, Durham, NC, USA.
¹² Department of Computer Science, Duke University, Durham, NC, USA.
¹³ Graduate Program in Cell and Molecular Biology, Colorado State University, Fort Collins, CO, USA.
¹⁴ School of Food Science and Technology, Nanchang University, Nanchang, Jiangxi, China.
¹⁵ School of Life Sciences, Arizona State University, Tempe, AZ, USA.
¹⁶ Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ, USA.
¹⁷ Department of Computer Science and Engineering, University of California San Diego, La Jolla, CA, USA.
¹⁸ Department of Computer Science, Colorado State University, Fort Collins, CO, USA.
¹⁹ U.S. Geological Survey, Southwest Biological Science Center, Moab, UT, USA.
²⁰ Forensic Investigation Research Station, Colorado Mesa University, Grand Junction, CO, USA.
²¹ Forensic Anthropology Center, Department of Anthropology, University of Tennessee, Knoxville, TN, USA.
²² Department of Social, Cultural, and Justice Studies, University of Tennessee at Chattanooga, Chattanooga, TN, USA.
²³ Mid-America College of Funeral Service, Jeffersonville, IN, USA.
²⁴ Department of Biological Sciences, Sam Houston State University, Huntsville, TX, USA.
²⁵ Laboratory of Forensic Taphonomy, Forensic Sciences Unit, School of Natural Sciences and Mathematics, Chaminade University of Honolulu, Honolulu, HI, USA.
²⁶ Center for Microbiome Innovation, University of California San Diego, La Jolla, CA, USA.
²⁷ Department of Bioengineering, University of California San Diego, La Jolla, CA, USA.
²⁸ Department of Animal Sciences, Colorado State University, Fort Collins, CO, USA. [email protected].
²⁹ Graduate Program in Cell and Molecular Biology, Colorado State University, Fort Collins, CO, USA. [email protected].
³⁰ Humans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada. [email protected].

Abstract

Microbial breakdown of organic matter is one of the most important processes on Earth, yet the controls of decomposition are poorly understood. Here we track 36 terrestrial human cadavers in three locations and show that a phylogenetically distinct, interdomain microbial network assembles during decomposition despite selection effects of location, climate and season. We generated a metagenome-assembled genome library from cadaver-associated soils and integrated it with metabolomics data to identify links between taxonomy and function. This universal network of microbial decomposers is characterized by cross-feeding to metabolize labile decomposition products. The key bacterial and fungal decomposers are rare across non-decomposition environments and appear unique to the breakdown of terrestrial decaying flesh, including humans, swine, mice and cattle, with insects as likely important vectors for dispersal. The observed lockstep of microbial interactions further underlies a robust microbial forensic tool with the potential to aid predictions of the time since death.

MeSH terms

Animals
Bacteria
Cadaver
Cattle
Humans
Metagenome
Mice
Microbial Consortia*
Soil Microbiology*
Swine

Abstract

MeSH terms

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