What happens to us when we die? Well, here’s the literal explanation.

Kevin Lyons

Given the day that’s in it, I thought I’d seize the opportunity to write an article about a spooky subject which blends the fields of ecology, microbiology and forensic science: namely, the role of microbes in the decomposition of dead bodies.

We often forget that a dead animal, plant, fungus, bacterium, archaeon or protist, is every bit a part of its environment as a living one. Having acquired and utilized various elements, ions and chemical compounds throughout its life – as energy sources and building-blocks for growth – the deceased organism must eventually be decomposed and its constituents recycled back into the environment to maintain the flow of energy through the ecosystem. In a typical terrestrial ecosystem, the decomposition of dead vertebrates is primarily carried out by necrophagous (i.e. corpse-eating) invertebrates such as flies and beetles (Benbow et al., 2013). However, the overall process is highly complex, and typically involves a wide range of organisms that interact with the corpse and with each other: such as avian-, mammalian- and insect scavengers; moths, wasps, slime moulds, nematodes, and microbes. The community of organisms associated with a decomposing carcass or cadaver has been collectively termed the ‘necrobiome’.

Studying the role of microbial communities in the decomposition of carcasses and cadavers, as well as the environmental consequences of this decomposition, is probably not something that every microbiologist in the academic- or industrial sphere would find especially appealing. However, there are now six major research facilities in the US (affectionately known as ‘body farms‘) which are dedicated to the study of human body decomposition in all its gory glory. These facilities typically have large plots of land, where donated bodies are allowed to decompose in a variety of different settings and scenarios, in a way that generates data which can be used to either support or refute evidence obtained in real-life criminal investigations.

Dr. Jennifer DeBruyn – Associate Professor in the Department of Biosystems Engineering and Soil Science at the University of Tennessee – leads a research group at the original ‘body farm’ in Knoxville, Tennessee. The facility, formally known as the Forensic Anthropology Center, was founded in 1987 by Prof. William “Bill” M. Bass in an attempt to improve measurements of decay and time-of-death estimates in forensic anthropology. Prof. Bass was inspired to establish the facility by an embarrassing experience he had had while working as a forensic pathologist for the Tennessee State Medical Examiners System in the 1970s. He was asked one day to determine the age of what was later found to be a well-preserved Civil War soldier (who had been dead for over a hundred years) and wrongly deduced that the man must have died “within the last six months”. No doubt this margin of error required urgent improvement, and thanks to Prof. Bass – and all who have followed his lead – a lot of progress has been made since then.

Two weeks ago, Dr. DeBruyn gave a fascinating talk, entitled The Necrobiome: Microbial Life After Death, as part of the American Society for Microbiology’s Microbes After Hours event series. Anyone looking for a great overview of this unusual area of research, would do well to watch the video recording.

The decomposition of a dead mammal typically proceeds several times faster than the decomposition of plant material, due to its relatively moist, nutrient-rich nature (Carter et al., 2006; Metcalf et al., 2015). This process releases a transient, localised pulse of carbon and nutrients into the surrounding soil which is associated with increases in soil microbial biomass, microbial activity and nematode abundance (Carter et al., 2006). Decomposition events contribute to ecosystem heterogeneity by causing direct disturbance – for example, the release of nutrients into soil – and indirect disturbance through the actions of visiting organisms. In addition, the decomposition of vertebrates enhances the biodiversity of terrestrial ecosystems by acting as a specialised habitat for a number of flies and beetles, and by promoting the growth of pioneer plant species.

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Typical mass loss curves for cadavers, plant material and faecal (dung) material (adapted from Carter et al., 2006)

Vertebrate decomposition can be divided into three major stages: bloating, active decay and advanced decay. The bloating stage is caused by the release of decomposition gases, and is associated with cadaver distension and surface rupture. Next comes the active decay stage – driven by necrophagous invertebrates and high-efficiency aerobic microbes – which results in rapid mass loss, fluid loss and elevated temperatures. Finally, when most of the available nutrients have been depleted; when oxygen levels in the decomposition fluids are low; when the temperature of the cadaver falls back to ambient levels; and when lower-efficiency anaerobic microbes begin to dominate; the cadaver is said to be undergoing advanced decay.

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A summary of the decomposition products arising from vertebrate remains. When a vertebrate dies, its cells are deprived of oxygen and burst open (cell autolysis) leading to the release of a wide range of large macromolecules. The actions of microbes break these macromolecules down into a variety of simpler substances, many of which have strong, unpleasant odours (adapted from Dr. DeBruyn’s ASM talk)

The microbial communities associated with decomposing cadavers are highly diverse in terms of taxonomy and metabolism, consisting of a wide variety of aerobes and anaerobes, which originate from the soil, as well as from visiting organisms – such as birds, mammals, ants, flies, beetles, moths and wasps – and from the internal and external surfaces of the corpse itself (Cobaugh et al., 2015). It seems that the functional and structural characteristics of these communities change significantly over time, with competition occurring between human-associated species and soil-associated species, and different taxa and metabolic lifestyles dominating at different decomposition stages.

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Changes in microbial composition of soil below cadavers throughout decomposition. Interesting to note the reduction in soil-associated Acidobacteria over time and increased abundance of mammalian-gut-associated Firmicutes. Results from soil samples collected in Advanced III stage may suggest the beginning of a slow return to a state resembling the pre-decomposition equilibrium. (Cobaugh et al., 2015)

Various high-throughput ‘-omics’ techniques (e.g. genomics, transcriptomics, proteomics, metabolomics) are now being applied to the study of decomposition in an attempt to learn more about this microbial succession, and develop methods to accurately back-calculate time-of-death from these observations (Hauther et al., 2015). One advantage of using microbes for this purpose – rather than, for example, one current method which utilizes our understanding of insect larval development – is that, assuming no preservation methods are used, decomposition by resident microbes will be observable in 100% of cases; whereas if a body is indoors and out of the reach of flies and beetles, our understanding of insect larval development will be of no use.

It has long been known that spore-forming organisms such as the Gram-positive bacterium Bacillus anthracis (producer of the anthrax toxin) can persist in the environment for long periods of time: B. anthracis spores have been detected on dead cattle, reindeer and even woolly mammoth remains, and often cause outbreaks among animals when released from melting permafrost (Revich and Podolnaya, 2015). In a recent study, the Gram-positive bacterium Erysipelothrix rhusiopathiae – a human and animal pathogen known to survive in aquatic environments, soil environments and in the vicinity of decomposing animal remains – was found to be responsible for the deaths of approximately 150 muskoxen on Banks Island, Canada (Kutz et al., 2015). Another recent study found that nucleic-acid signatures from a genus of Gram-negative obligate anaerobic bacteria, Bacteroides, could be detected in high abundances in the soil surrounding a human cadaver up to 198 days after placement (Cobaugh et al., 2015). This is especially surprising, as Bacteroides are typically associated with the low-oxygen environment of the mammalian gastrointestinal tract, and hence, would not typically be expected to survive exposure to the oxygen-rich atmosphere. All of these findings raise important questions about the survival of cadaver-derived pathogenic microbes in the environment, and their associated health risks.

Clearly the spooky and useful outcomes of ‘body farm’ research have interesting implications for ecology, microbiology, forensic science and epidemiology – as well as many other fields. With this in mind, I would encourage anyone interested in the details of decomposition to hold his/her nose and support the cause! I guess donating your body wouldn’t hurt either.

References:

  1. Benbow, M.E., Lewis, A.J., Tomberlin, J.K. and Pechal, J.L. (2013) Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. Journal of Medical Entomology. 50(2), 440–50.
  2. Carter, D.O., Yellowlees, D. and Tibbett, M. (2007) Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften. 94(1), 12–24.
  3. Metcalf, J.L., Xu, Z.Z., Weiss, S., Lax, S., Van Treuren, W., Hyde, E.R., Song, S.J., Amir, A., Larsen, P., Sangwan, N., Haarmann, D., Humphrey, G.C., Ackermann, G., Thompson, L.R., Lauber, C., Bibat, A., Nicholas, C., Gebert, M.J., Petrosino, J.F., Reed, S.C., Gilbert, J.A., Lynne, A.M., Bucheli, S.R., Carter, D.O. and Knight, R. (2016) Microbial community assembly and metabolic function during mammalian corpse decomposition. Science. 351(6269), 158–62.
  4. Cobaugh, K.L., Schaeffer, S.M. and DeBruyn J.M. (2015) Functional and structural succession of soil microbial communities below decomposing human cadavers. PLoS One. 10(6), e0130201.
  5. Hauther, K.A., Cobaugh, K.L., Jantz, L.M., Sparer, T.E., DeBruyn, J.M. (2015) Estimating time since death from postmortem human gut microbial communities. Journal of Forensic Sciences. 60(5), 1234–40.
  6. Revich, B.A. and Podolnaya, M.A. (2011) Thawing of permafrost may disturb historic cattle burial grounds in East Siberia. Global Health Action, 4.
  7. Kutz, S., Bollinger, T., Branigan, M., Checkley, S., Davison, T., Dumond, M., Elkin, B., Forde, T., Hutchins, W., Niptanatiak, A. and Orsel, K. (2015) Erysipelothrix rhusiopathiae associated with recent widespread muskox mortalities in the Canadian Arctic. The Canadian Veterinary Journal. 56(6), 560–563.
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