Paleomicrobiology of the human digestive tract: A review

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Highlights

  • Ancient microbiota can be studied through the analysis of ancient human remains.

  • Coprolites and mummified tissues are the primary sources for ancient gut microbiota.

  • Dental calculus is the primary source for ancient oral microbiota.

  • Ancient microbiota provide information on dietary habits of ancient populations.

  • Ancient microbiota reflect the evolution of human lifestyle throughout history.

Abstract

The microbiota is a hot topic of research in medical microbiology, boosted by culturomics and metagenomics, with unanticipated knowledge outputs in physiology and pathology. Knowledge of the microbiota in ancient populations may therefore be of prime interest in understanding factors shaping the coevolution of the microbiota and populations. Studies on ancient human microbiomes can help us understand how the community of microorganisms presents in the oral cavity and the gut was shaped during the evolution of our species and what environmental, social or cultural changes may have changed it. This review cumulates and summarizes the discoveries in the field of the ancient human microbiota, focusing on the remains used as samples and techniques used to handle and analyze them.

Introduction

In the last 20 years, there has been an exponential increase in interest in the microbiome and its effect on human health. We currently know that the microbiome plays a fundamental role in the host via the development, maintenance and priming of the immune system [[1], [2], [3]], defense against pathogens [4,5], metabolism, digestion and the production of vitamins [6]. Furthermore, slight modification of the bacterial equilibrium of the microbiome (dysbiosis) due to changes in diet, physical exercise or antibiotic treatments can lead to major consequences for the host [[7], [8], [9], [10], [11]]. Recent studies have focused their attention on the composition of the microbiome of our ancestors and its evolution throughout history. Particular attention was given to the periods of major revolutions in human lifestyles, such as the Neolithization process (debuted 12,000 years BCE [12]) and the industrialization period (1760–1840 CE). With the Neolithization process, we observed the transition from a nomadic hunter-gatherer diet characterized by the consumption of only wild and unprocessed food foraged and hunted from the environment [13] to a sedentary one based on agriculture and livestock. Then the industrialization period arose the advent of modern sanitation and Western diet, characterized by food that has been processed and modified and has a low quantity of vegetables and fibers [[14], [15], [16]].

In the literature, there is some confusion about the definition of the terms “microbiota” and “microbiome” and are often used interchangeably. The term “microbiota” refers to all the microbial taxa associated with the host [17], while “microbiome” can refer to “the ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space and have been all but ignored as determinants of health and disease” [18] or to “the collective genome of our indigenous microbes” [19].

Diets of past and present human populations are very variable and mostly depend on resource availability and ecological settings [20]. Comparative studies on the microbiota among human populations with different dietary habits have shown how differences in diet are reflected in differences in the microbiota composition [14,16]. For instance, De Filippo and colleagues [21] showed how children from urban Europe, with a modern Western diet, and children from rural Africa, with a diet very high in fibers, present differences in microbiota composition that can be attributed to an evolutionary adaptation to the diet composition, allowing each population to maximize the nutritional value of each diet. Other studies on mouse models have shown how changing diet correlated with changes in the microbial composition of the gut microbiota [22]. Moreover, Groussin et al. [23] demonstrated how microbiota composition reconstructed from ancient mammal remains could be used to reconstruct ancient diets of these animals and that information about dietary shift can be recorded by the gut microbiome. For these reasons, ancient microbiota studies are not restricted to the microbial diversity and composition of the ancient remains but also to the dietary information that is preserved inside these specimens. The first study to target the ancient DNA of multiple species of bacteria on human remains was conducted by Ubaldi et al. analyzing the gut microbiome from the colon of a mummy recovered in Cuzco, Peru, that dated back to the 10th-11th century CE [24]. After that, many other PCR-based studies on coprolites and mummified samples were published [[25], [26], [27]]. In 2008, Tito et al. performed the first study on an ancient microbiota using NGS techniques, and from that point, the number of ancient microbiome analyses multiplied [28].

Retrieving information on ancient human microbiomes is not easy and is strictly dependent on the availability of suitable samples for the analysis. Dental calculus and coprolite are the only two human remains that persist long enough to be used for these studies, with the exceptions of frozen and mummified tissues [29]. In this review, we will present the remains used as starting samples for ancient human microbiota studies and the methods used to retrieve this information.

Section snippets

Literature search strategy and terminology use

All the papers used for this review were obtained from PubMed and Google Scholar. The keywords used alone or in combination for the search were “paleomicrobiology”, “ancient”, “human”, “paleo”, “microbiota”, “microbiome”, “oral”, “dental calculus”, “gut”, “intestinal”, “feces”, “faeces”, “paleofeces”, “paleofaeces”, “coprolite”, “latrines”, “mummy”, “mummified”, “tissue”, “metagenomic”, “shotgun”, and “proteomics”.

Only studies written in English and on samples of human origin that targeted

Dental calculus

Dental calculus, or tartar, is a mineralized bacterial biofilm that forms on the teeth as a result of the action of bacteria and saliva in the oral cavity and is very common in adults without active dental hygiene [29]. Dental calculus presents some characteristics that make it the most reliable source for information about the oral microbiota. It is common and relatively abundant in archaeological sites; it has the capability to preserve ancient biomolecules, avoiding environmental

Coprolites and palaeofaeces

The primary sources for information about the ancient gut microbiota are coprolites, which are “any formed fecal mass remains, including mineralized, desiccated, or frozen feces and even the intestinal contents of mummies” [65]. These remains can be preserved for thousands or even millions of years [66], providing information about the gut microbiota components, the presence of pathogens and the diet of past human and animal populations [67]. In fact, traces of aliments consumed by the host,

Perspectives

We have just begun to understand the relationships between diet, health, pathological conditions, and the composition of our microbiota, but it is clear that the gut microbiota plays a role in the health and disease conditions of humans. This explains the strong interest in medical research for this subject. Combining modern techniques and protocols used in the field of paleomicrobiology for the analysis and the extraction of data from ancient human remains, we can study the past of humankind

Declaration of competing interest

The authors have no competing interests to declare.

Author statement

Riccardo Nodari: Investigation, Writing – original draft. Michel Drancourt: Writing – review & editing. Rémi Barbieri: Writing – original draft, Supervision, Writing – review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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