Microbial community assembly and metabolic function during mammalian corpse decomposition

Abstract

Vertebrate corpse decomposition provides an important stage in nutrient cycling in most terrestrial habitats, yet microbially mediated processes are poorly understood. Here we combine deep microbial community characterization, community-level metabolic reconstruction, and soil biogeochemical assessment to understand the principles governing microbial community assembly during decomposition of mouse and human corpses on different soil substrates. We find a suite of bacterial and fungal groups that contribute to nitrogen cycling and a reproducible network of decomposers that emerge on predictable time scales. Our results show that this decomposer community is derived primarily from bulk soil, but key decomposers are ubiquitous in low abundance. Soil type was not a dominant factor driving community development, and the process of decomposition is sufficiently reproducible to offer new opportunities for forensic investigations.T he process of decay and decomposition in mammalian and other vertebrate taxa is a key step in biological nutrient cycling. Without the action of vertebrate and invertebrate scavengers, bacteria, archaea, fungi, and protists, chemical decomposition of animal waste would proceed extremely slowly and lead to reservoirs of biochemical waste (1). The coevolution of microbial decomposers with the availability of vertebrate corpses over the past 400 million years is expected to result in conservation of key biochemical metabolic pathways and cross-kingdom ecological interactions for efficient recycling of nutrient reserves. Although mammalian corpses likely represent a relatively small component of the detritus pool (2, 3) in most ecosystems, their role in nutrient cycling and community dynamics may be disproportionately large relative to input size, owing to the high nutrient content of corpses (3, 4) and their rapid rates of decomposition [e.g., up to three orders of magnitude faster than plant litter (2)]. These qualities make corpses a distinct and potentially critical driver of terrestrial function (5, 6).When a mammalian body is decomposing, microbial and biochemical activity results in a series of decomposition stages (5) that are associated with a reproducible microbial succession across mice (7), swine (8), and human corpses (9). Yet the microbial metabolism and successional ecology underpinning decomposition are still poorly understood. At present, we do not fully comprehend (i) whether microbial taxa that drive decomposition are ubiquitous across environment, season, and host phylogeny; (ii) whether microbes that drive decomposition derive primarily from the host or from the environment; and (iii) whether the metabolic succession of microbial decomposition is conserved across the physicochemical context of decay and host phylogeny.Several questions arise: Are microbial decomposer communities ubiquitous? What is the origin of the microbial decomposer community? How does mammalian decomposition affect the metabolic capacity of microbial communities? To answer these questions, we used mouse...

Can microbes keep time for forensic investigators?

“…At least some of these microbes are opportunistic members of the livinghuman microbiome (5). "Most likely there are some microbes that are just waiting for us to keel over," Metcalf says.…”

“…In a previous collaboration with Bucheli, Metcalf found that at least a small percentage of the postmortem microbiome may also be deposited by flies colonizing a body (5). In one study Bucheli designed, she and her team found that the community of microbes on flies visiting recently placed bodies varied in diversity and abundance across different seasons and even across the same seasons in different years.…”

Microbial effects on the development of forensically important blow fly species

“…To date there is limited research documenting microbial succession on a corpse. However, recent research indicates that microbial communities change significantly, following a predictable timescale during decomposition [15]. The initial bacterial community varies with the age [16] and health [17] of the victim, the location on the body [18], environmental temperature and humidity [19], and the season [20][21].…”

“…As decomposition continues, the microbial community changes as bacteria move from sites internal to the body to locations on the surface, and are transferred from the soil, scavengers and insects [15,17,23]. Different species of bacteria are known to be associated with different stages of the decomposition process.…”

“…During the bloat stage, Ignatzschineria and Wohlfahrtimonas bacteria are commonly found on the skin of the corpse, and anaerobic bacteria including Lactobacillus and Bacteriodes increase in the abdominal 3 cavity [18]. Microbial communities on a corpse generally become less diverse [23,25] and more similar to each other across body sites [15] with time.…”