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Category: General Interest; Microbial Genetics and Molecular Biology
Paleomicrobiology of Humans is now available on Wiley.comMembers, use the code ASM20 at check out to receive your 20% discount.
A comprehensive examination of the technical and anthropological issues in this new multidisciplinary field
Only recently was it determined that two of the world’s most devastating plagues, the plague of Justinian and the medieval Black Death, were caused by distinct strains of the same pathogen. Use of paleomicrobiological techniques led to this discovery. This work is just one example of the historical mysteries that this emerging field has helped to clarify. Others, such as when tuberculosis began to afflict humans, the role of lice in plague pandemics, and the history of smallpox, are explored and further illuminated in Paleomicrobiology of Humans.
Led by editors Michel Drancourt and Didier Raoult, the book’s expert contributors address larger issues using paleomicrobiology. These include the recognition of human remains associated with epidemic outbreaks, identification of the graves associated with disasters, and the discovery of demographic structures that reveal the presence of an epidemic moment. In addition, this book reviews the technical approaches and controversies associated with recovering and sequencing very old DNA and surveys modern human diseases that have ancient roots.
Essentially, paleomicrobiologists aim to identify past epidemics at the crossroads of different specialties, including anthropology, medicine, molecular biology, and microbiology. Thus, this book is of great interest not only to microbiologists but to medical historians and anthropologists as well.
Paleomicrobiology of Humans is the first comprehensive book to examine so many aspects of this new, multidisciplinary, scientific field.
Paperback, 212 pages, full-color illustrations.
Some ancient burial grounds are valuable testimonies of past epidemics. For both funerary archaeologists and paleobiologists, such archaeological sites offer a remarkable research framework to reveal unfamiliar aspects of these historical events, especially those that occurred during periods for which very few or no written sources exist. The multiplicity of congresses, articles, and syntheses on this topic in recent years illustrates the interdisciplinary research that has progressively emerged over the past two decades.
There are several scenarios regarding how burial sites in archaeological contexts are discovered. We will focus on two scenarios according to the degree of historical knowledge regarding the studied sector. The excavation may be performed in a known funeral place or a highly suspected place (e.g., the interior or immediate exterior space in a religious monument or a parish cemetery). Also, the excavation of unexpected graves or graves discovered by chance may occur in places that had unknown or forgotten funeral purposes.
With the advent of next-generation sequencing, the field of paleogenetics has considerably expanded over the past few years, making investigations that were once considered impossible a reality. A milestone in paleogenetics was reached in the year 2010, which saw for the first time the reconstruction of the nuclear genome of ancient humans who lived thousands of years ago. The genomes characterized that year covered both modern humans, with the approximately 4,000-year-old Saqqaq man ( 1 ), and archaic humans, with the approximately 38,000-year-old Neanderthals from Croatia ( 2 ) and a more than 30,000-year-old Denisovan individual discovered in Siberia ( 3 ). These studies notably uncovered a migration of modern humans from Siberia into the New World some 5,500 years ago ( 1 ) and a new group of archaic humans who lived in Siberia, the Denisovans ( 3 , 4 ). With these molecular data, it was also possible to refine the separation between modern and archaic humans to between 272,000 and 435,000 years ago, with a genetic divergence time of 734,000 to 1,087,000 years ago ( 2 ). Consistent with such an ancient genetic divergence between modern and archaic humans, for the human endogenous retrovirus (HERV) that is thought to have promoted the development of the placenta in mammals ( 5 ), archaic individuals have six HERV-K proviruses (three common to Denisovans and Neanderthals, two specific to Neanderthals, and one specific to the Denisovan individual) that are absent in a 402-genome set of modern-day individuals ( 6 ). Following these early characterizations of draft genomes of archaic humans, efforts focused on reconstructing high-quality genome sequences, and this was achieved for the original Denisovan genome ( 7 ) and for the genome of a Neanderthal individual who lived in Altai ( Fig. 1 ) ( 8 ).
As early researchers in paleomicrobiology, we have used its techniques to study the plague, generating controversy after the publication of our initial results ( 1 ). The controversy has allowed us to respond and propose new approaches to understanding plague pandemics. Our conclusion is that the plague was related to outbreaks of lice, not to rat fleas, because fleas cannot explain epidemics of this magnitude ( 1 ).
Paleomicrobiology aims to establish the diagnosis of ancient infectious diseases from human or environmental ancient samples, including animal specimens dating back thousands of years but with conservation differences depending on the nature of the molecules (DNA or proteins) or conservation environmental conditions ( 1 ). This science, born of the multiple disciplines of medical microbiology, anthropology, history, and related sciences such as archaeozoology, initially aimed to highlight ancient pathogens and more recently ancient microbiota, including functional data such as antibiotic resistance ( 2 ). The works of Ruffer are among the oldest works ( 3 – 5 ), especially on the discovery of a solution for rehydrating the mummified tissue.
Paleomicrobiology is a part of general microbiology that aims to describe microbial flora (including bacteria, archaea, viruses, parasites, and microscopic fungi) in older specimens; it includes the retrospective diagnosis of infectious and tropical diseases ( 1 , 2 ). There is no precise numerical definition of an old specimen; we consider as paleomicrobiological specimens any specimen older than 100 years, while the study of more recent samples may be called meso-microbiology. Also, we will consider in this chapter only animal and human specimens, excluding inanimate environmental specimens. The initial works of paleopathology, which used molecular biology techniques based on PCR, highlighted the possibility of the contamination of old samples by contemporary human DNA, casting doubt on the validity of PCR-based work for the detection of human and microbial ancient DNA (aDNA). These doubts, arising in the field of human aDNA, were then relayed to the field of paleomicrobiology by colleagues not practicing microbiology and without microbiological knowledge, who simply derived doubts from their observations of old human DNA. In fact, microbial contamination of an ancient specimen can take place in situ from the surrounding flora, which can be either ancient flora contemporary with the sample or flora from operators at the time of excavation and storage of the old material or during laboratory manipulations, which is modern contamination. Contamination can occur with whole organisms or biomolecules of interest, such as nucleic acids or proteins or mycolic acids ( Fig. 1 ). Indeed, several methods are now used for discovering microbes in ancient specimens beyond the now-conventional aDNA analyses ( 2 ).
Paleomicrobiology—the search for ancient microbes—is based on the analysis of human bones, teeth, and mummified soft tissues ( 1 – 3 ). In addition, ancient fecal remains preserved by mineralization or desiccation in the form of organic or permineralized coprolites, as well as intestinal contents and latrines, have yielded data on the environmental and gut microbiota of humans and animals that lived centuries to millennia ago ( 4 – 10 ). Also, coprolites appear to be a valuable source to study the diet of past populations ( 11 ). Combined, microbial and diet data support hypotheses regarding the role of environmental and cultural factors in the evolution of the human gut microbiota.
It is generally now known that the emergence of antibiotic resistance in bacteria is an ancient biological event, meaning that the existence of resistance genes predates our present-day use of antibiotics. In other words, antibiotic resistance is not a modern phenomenon. These findings have been made possible by emerging fields, such as paleomicrobiology, and paleo-environmental studies of ancient biological samples, deep subsurface environments, and isolated pristine environments that are free of contemporary sources (contemporary antibiotic compounds or genes) ( 1 ). Paleomicrobiology has been employed to gain insight into ancient infections, such as the Black Death and Justinian’s plague, and has shown evidence of the involvement of bacteria in these pandemics ( 2 , 3 ).
Bacteria of the order Rickettsiales were first described as short Gram-negative bacillary microorganisms that retained basic fuchsin when stained by the method of Gimenez and grew in association with eukaryotic cells ( 1 ). In 1993, the order Rickettsiales was divided into three families—namely, Rickettsiaceae, Bartonellaceae, and Anaplasmataceae. Two distinct groups are found within the Rickettsia genus, including the spotted fever group and the typhus group. In the typhus group, the two species Rickettsia typhi and Rickettsia prowazekii are pathogenic in humans ( Table 1 ). R. typhi causes murine typhus, which is a flea-transmitted disease that occurs in warm climates ( 2 ). R. prowazekii is responsible for epidemic typhus, a disease of the cold months, during which heavy clothing and poor sanitary conditions are conducive to lice proliferation ( 3 ).
Paleopathology is the most recent discipline among the sciences of the past; it studies traces of diseases that can be recognized in animal and human remains from ancient times. This research field is located at the interface of medicine, anthropology, and archaeology. Since its beginning in the late 19th century, paleopathology has developed a specific interest in the origin and evolution of infectious diseases affecting human populations. Since the mid 1990s, thanks to the introduction of PCR into the field, the studies of past human infections have undergone a significant revival, evolving from the analysis of ancient writings and bones to that of ancient molecules, allowing evidence-based diagnosis. The goal of this chapter is to provide some examples of an integrative approach that combines these three sources of data for reconstructing the history of human infections.
To date, several bacteria have been detected in ancient specimens as causative agents of various diseases, in both humans and animals ( 1 ). These include Bartonella henselae ( 2 ), Bartonella quintana ( 3 ), Borrelia burgdorferi ( 4 ), Enterobacteriaceae ( 5 ), Mycobacterium leprae ( 6 ), Mycobacterium tuberculosis ( 7 ), Rickettsia prowazekii ( 8 ), Treponema pallidum, and Yersinia pestis ( 9 ). Most of these microorganisms have been detected with molecular methods ( 1 ), although culture, immunohistochemistry ( 10 ), and the detection of specific antibodies ( 11 ) have occasionally been successful.
Tuberculosis remains one of the world’s deadliest communicable diseases. In 2014, tuberculosis developed in an estimated 9.6 million people, and 1.5 million died of the disease ( 1 ). The principal causative organism is Mycobacterium tuberculosis, an obligate pathogen that is a member of the M. tuberculosis complex (MTBC), a group of closely related organisms that primarily infect different animal hosts. Tuberculosis may involve every organ in the body, but the most common clinical presentation is pulmonary disease, in which transmission is via infectious aerosols released from the lungs of an infected person. In the alveolus of the lung, inhaled tubercle bacilli are ingested by macrophages and are normally contained by the host immune response. This leads to granuloma formation and eventually to calcified lesions. Swallowing infected sputum can cause intestinal tuberculosis. Transmission can occur via direct contact in cases of scrofula (skin tuberculosis). In addition, ingestion of milk or food from an infected animal can cause human infection with Mycobacterium bovis or other members of the MTBC. However, subsequent transmission of these animal MTBC lineages from person to person is rare. M. tuberculosis can survive and grow within macrophages, so that it is able to evade the host immune system. An active cell-mediated immune response is required to contain and kill the tubercle bacilli, so any underlying conditions that reduce its efficiency increase susceptibility to tuberculosis. One-third of the global population is estimated to have latent tuberculosis infection. These individuals do not have active disease but may develop it in the near or remote future, a process called tuberculosis reactivation. The lifetime risk for reactivation is estimated to be 5% to 10%, with tuberculosis developing in the majority of cases within the first 5 years after initial infection. However, the risk is considerably higher in the presence of predisposing factors ( 2 ).
Leprosy (or Hansen’s disease) is a chronic infectious disease caused by a slowly multiplying obligate pathogen, Mycobacterium leprae, an acid-fast, rod-shaped bacillus belonging to a single species with limited genetic variability ( 1 ). M. leprae has four types and 16 subtypes based on single-nucleotide polymorphisms (SNPs) and variations (InDels) in insertions and deletions ( 2 ). Although not highly infectious, it is transmitted via droplets from the nose and mouth during close and frequent contacts with untreated cases. The incubation period can be very long (in some cases up to 20 years) before clinical signs and symptoms become apparent ( 3 , 4 ). Leprosy can affect all age groups and both sexes. To this day, we cannot grow the bacillus in the laboratory. The bacillus is almost specific to humans but does affect some armadillos (Dasypus novemcinctus) from the southeastern United States (Texas and Louisiana) ( 5 ) and a specific type of monkey. In the laboratory, rats, mice, and hamsters can be infected. The diagnosis of the disease in archaeological specimens can be problematic because the characteristic bony changes can occur in a number of other diseases. Thus, paleomicrobiology can help to confirm a clinical incidence and, along with genotyping, can trace the spread of the disease and even human migration patterns responsible for its spread ( 6 ).
The study of ancient parasites, paleoparasitology, is an area of parasitology that evolved as a research field combining archaeology, anthropology, biology, and health sciences ( 1 ). It aims to detect parasite traces in ancient samples and to study parasitism evolution over time and space ( 2 ). This research field covers the study of parasites in humans and other animal remains recovered from archaeological and paleontological sites.
Malaria, one of the deadliest diseases of humankind, remains a major global health problem in the 21st century ( 1 , 2 ). In 2014, 198 million persons were infected, with more than 0.5 million deaths from malaria globally. Malaria is recognized as the second leading cause of death from infectious diseases in Africa, after HIV/AIDS, and is the fifth most frequent cause of death from infectious diseases worldwide, after respiratory infections, HIV/AIDS, diarrheal diseases, and tuberculosis ( 2 ).
Smallpox, the infectious disease caused by species of the variola virus (VARV), is probably one of the most terrible diseases to have affected human populations over the past hundreds of years. Its dissemination was significantly related to global population growth and the movement of people across regions and continents. The geographical origin of the disease remains a matter of debate; hypotheses suggest the Indus Valley or Egypt and the Near East, regions that had high population densities 3,000 to 4,000 years ago ( 1 , 2 ). The latter hypothesis was recently refined by Babkin and Babkina ( 3 ), who suggested that the initial spread of the virus in humans could have occurred in the Horn of Africa (Kingdom of the Queen of Sheba). In this region, active trade expeditions overlapped with the distribution areas of several animal poxvirus hosts (including the naked-soled gerbil) and the introduction of the domesticated camel as a new potential host. The disease spread from these regions to the west and east, with historical reports suggesting epidemics in China and Europe as early as the 1st or 2nd century CE, with a subsequent progressive emergence of the virus in western Africa ( 4 ). During the 16th century, smallpox was a significant cause of death in Europe. The smallpox agent was also exported to South America during this time and passed over both American continents ( 5 , 6 ). As noted by Fenner et al., smallpox was a major global endemic disease by the mid-18th century, with the exception of Australia ( 4 ). Only the variolation and vaccination campaigns initiated more than two centuries ago reduced dramatically the spread and impact of the disease in contemporary populations.
Cholera is an acute and often fatal disease of the gastrointestinal tract. In its typical epidemic form, it presents with profuse watery diarrhea and often leads to dehydration and eventually the death of an untreated patient within a few hours ( 1 ). The causative agent of cholera is a bacterium known as Vibrio cholerae, two serogroups of which (O1, to which the El Tor biotype belongs, and O139) have epidemic potential and are also responsible for endemic cholera. V. cholerae has two known reservoirs: humans (who can also be asymptomatic carriers) and the aquatic environment (both freshwater, such as that of the Ganges River delta in India, and the sea). Humans mostly are infected through contaminated water used for drinking or preparing foods, and (when symptomatic) they keep shedding bacteria with feces during 1 to 2 weeks ( 1 ). In the aquatic reservoir, V. cholerae can persist indefinitely and undergo genetic modification, which makes the eradication of cholera unlikely to be achieved, if not impossible ( 1 ).
Lice (Insecta, Phthiraptera) are permanent obligate parasites of birds and mammals. Approximately 4,900 species of lice are recorded and distributed into four suborders: chewing or biting lice, including Rhynchophthirina, Ischnocera, and Amblycera, and sucking lice, Anoplura ( 1 ).
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This volume edited by Drancourt and Raoult, two of the biggest names in paleomicrobiology, is both educational and informative for researchers in the field. This compendium of articles spans subjects from the demography of epidemics to the more pointed analyses of specific pathogens (e.g., tuberculosis, malaria). In a book format (which always take a long time from conception to printing), most of the articles are already somewhat behind the curve of technological advances. But this does not detract from the usefulness of the information presented. Certainly, we find the biggest names in paleoarcheology and paleomicrobiology, such as the editors themselves, as well as Nerlich, Donoghue, and Aboudharam, among others. It is clear that the intention for this volume was to be an update of what has been done in paleomicrobiology. And, in that mission, it certainly succeeds. From the research articles, we clearly have get a good panorama of how far research on specific pathogens or “-omics” techniques for use on archeological samples has come. For example, the article on ancient resistome (Olaitain and Rolain) is an exciting new look at the potential of uncovering the evolutionary history of antibiotic resistance from historical samples. From the wider subject articles, we have an impressive array of methodologies and new guidelines to handle historical samples (and their data) in the field and in the laboratory. The chapter by Aboudharam is a thoughtful and detailed review of the types of samples with potential use for paleomicrobiology research, and also offers a small but important section on the ethical and legal framework in sample collection. Drancourt’s article should figure prominently in all paleomicrobiology (and indeed field archeology) textbooks, as it offers an excellent and useful synthesis on data authentication and interpretation, which often plagues (pun intended) historical samples.
We also have insightful essays, such as Abi-Rached and Raoult’s Paleogenetics and Past Infections, presenting a roadmap of possibilities for connecting data that is often kept in their own respective field. It also offers a map of our current knowledge of the impact of archaic humans on the genomes of modern populations, showing us one glaring crucial area for which no data is available, and yet is fundamental for our understanding of human evolution: Africa. Although the authors do not go as far as invalidating results from local archeogenome comparisons with their respective modern denizens, they do mention that such gaps in data certainly produce biased results, especially when considering Neanderthal ancestry and hybridism with “modern” humans.
So much in paleomicrobiology has changed so fast since the early work of Svante Pääbo in the 1990s. It is often hard to catch up on the “state-of-the-field” literature, particularly now that publication outlets are numerous and publishing happens at a frantic pace. Although this volume suffers perhaps from a lack of structure (articles jump from specific agents of infection to data handling and back), it certainly achieves its goal of collecting, summarizing, and synthesizing decades of research into a succinct, well-edited, and user-friendly format.
Angélique Corthals, Science, John Jay College of Criminal Justice, City University of New York, New York, New York