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Feb 28, 2014

Medieval Feces Preserves the Microbiome's Tale of Antibiotic Resistance

  • Archeologists have been known to sift through the contents of long-abandoned privy pits in their search for historical pay dirt. Now it appears the archeologists will have the company of scientists wielding the tools of genomic science. Microbiologists, for example, have demonstrated that fossilized fecal samples preserve the remains of ancient intestinal and environmental microbiota. By subjecting the microbiota to genomic analysis, the microbiologists can reconstruct long-passed microbial communities and the genetic transactions that animated them—practically carrying out, in miniature, the work of archaeologists, sifting through left-behind materials, bringing to light the activities of bygone societies.

    In one recent investigation, microbiologists studied the viral community of a 14th-century coprolite, or fossilized fecal specimen. The coprolite, which had been taken from a closed barrel in a Middle Age site in Belgium, yielded viruses known to infect eukaryotes, bacteria, and archaea. In some cases, the presence of viruses was confirmed by ad hoc suicide PCR. Most important, through the application of metagenomic analysis, the microbiologists were able to discover that the viral community contained genes for antibiotic resistance.

    The scientists, based at Aix Marseille Université, look forward to publishing their findings in the May issue of Applied and Environmental Microbiology. An early version of their article, entitled “Viruses in a 14th-century coprolite,” appeared online February 7. In the online article, the authors wrote: “The coprolite DNA viral metagenome was dominated by sequences showing homologies to phages commonly found in modern stools and soil [and, hence, the human gastrointestinal tract]. Although their phylogenetic compositions differed, the metabolic functions of the viral communities have remained conserved across centuries.”

    One of the conserved metabolic functions was antibiotic resistance, as the investigators confirmed by detecting genes for resistance to toxins and antibiotics in the viral metagenome. It would appear, suggested lead researcher Christelle Desnues, that viruses were capable of passing these genes to gut bacteria and thereby protecting them from toxins and antibiotics. These viruses were active long before antibiotics were used in medicine, but both toxins and antibiotics are common in nature. Indeed, phylogenetic studies have demonstrated that the evolution and dissemination of resistance genes started well before the use of antibiotics.

    “Our evidence demonstrates that bacteriophages represent an ancient reservoir of resistance genes, and that this dates at least as far back as the Middle Ages,” said Desnues. And, as Desnues and her colleagues noted in their article, the “persistence of metabolic functionalities across centuries may reinforce the crucial role of the viral community in the human gastrointestinal tract.” Despite reflecting inter-individual taxonomic variability, the medieval viral genome’s metabolic profile was significantly conserved—a characteristic also seen with other viromes from the same ecological niche. In this case, however, the virome that was analyzed lost its viability long ago.

    “We were interested in viruses because these are 100 times more abundant than human cells in our bodies, but their diversity is still largely unexplored,” said Desnues. “In the present study, we thus focused on the viral fraction of the coprolite by using, for the first time, a combination of electron microscopy, high-throughput sequencing, and suicide PCR approaches.”

    Characterizing the medieval coprolite virome’s diversity, the researchers indicated that it “displayed higher species richness (315.279) and seemed to be more functionally diverse (average Shannon-Wiener index of 4.8693) than modern stool viromes (average species richness of 77.824 and average Shannon-Wiener index of 4.1264).” Other differences, the researchers added, “included an overrepresentation of lipid transport and metabolism, fatty acid biosynthesis, and amino acid transport and metabolism.”

    Desnues and her collaborators are currently conducting further studies on the fungi and parasites in the coprolites, which she says will be of interest not only to microbiologists, but to historians, anthropologists, and evolutionists.



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