Oldest reconstructed bacterial genomes link farming, herding with emergence of new disease

February 24, 2020

The Neolithic revolution, and the corresponding transition to agricultural and pastoralist lifestyles, represents one of the greatest cultural shifts in human history, and it has long been hypothesized that this might have also provided the opportunity for the emergence of human-adapted diseases. A new study published in Nature Ecology & Evolution led by Felix M. Key, Alexander Herbig, and Johannes Krause of the Max Planck Institute for the Science of Human History studied human remains excavated across Western Eurasia and reconstructed eight ancient Salmonella enterica genomes - all part of a related group within the much larger diversity of modern S. enterica. These results illuminate what was likely a serious health concern in the past and reveal how this bacterial pathogen evolved over a period of 6,500 years.

Searching for ancient pathogens

Most pathogens do not cause any lasting impact on the skeleton, which can make identifying affected archeological remains difficult for scientists. In order to identify past diseases and reconstruct their histories, researchers have turned to genetic techniques. Using a newly developed bacterial screening pipeline called HOPS, Key and colleagues were able to overcome many of the challenges of finding ancient pathogens in metagenomics data.

"With our newly developed methodologies we were able to screen thousands of archaeological samples for traces of Salmonella DNA," says Herbig. The researchers screened 2,739 ancient human remains in total, eventually reconstructing eight Salmonella genomes up to 6,500 years old - the oldest reconstructed bacterial genomes to date. This highlights an inherent difficulty in the field of ancient pathogen research, as hundreds of human samples are often required to recover just a single microbial genome. The genomes in the current study were recovered by taking samples from the teeth of the deceased. The presence of S. enterica in the teeth of these ancient individuals suggests they were suffering from systemic disease at their time of death.

The individuals whose remains were studied came from sites located from Russia to Switzerland, representing different cultural groups, from late hunter-gatherers to nomadic herders to early farmers. "This broad spectrum in time, geography and culture allowed us, for the first time, to apply molecular genetics to link the evolution of a pathogen to the development of a new human lifestyle," explained Herbig.

"Neolithization process" provided opportunities for pathogen evolution

With the introduction of domesticated animals, increased contact with both human and animal excrement, and a dramatic change in mobility, it has long been hypothesized that "Neolithization" - the transition to a sedentary, agricultural lifestyle - enabled more constant and recurrent exposure to pathogens and thus the emergence of new diseases. However, prior to the current study, there was no direct molecular evidence.

"Ancient metagenomics provides an unprecedented window into the past of human diseases," says lead author Felix M. Key, formerly of the Max Planck Institute for the Science of Human History and now at the Massachusetts Institute of Technology. "We now have molecular data to understand the emergence and spread of pathogens thousands of years ago, and it is exciting how we can utilize high-throughput technology to address long standing questions about microbial evolution."

Humans, Pigs, and the Origin of Paratyphi C

The researchers were able to determine that all six Salmonella genomes recovered from herders and farmers are progenitors to a strain that specifically infects humans but is rare today, Paratyphi C. Those ancient Salmonella, however, were probably not yet adapted to humans, and instead infected humans and animals alike, which suggests the cultural practices uniquely associated with the Neolithization process facilitated the emergence of those progenitors and subsequently human-specific disease. It was previously suggested that this strain of Salmonella spread from domesticated pigs to humans around 4000 years ago, but the discovery of progenitor strains in humans more than 5000 years ago suggests they might have spread from humans to pigs. However, the authors argue for a more moderate hypothesis, where both human and pig specific Salmonella evolved independently from unspecific progenitors within the permissive environment of close human-animal contact.

"The fascinating possibilities of ancient DNA allow us to examine infectious microbes in the past, which sometimes puts the spotlight on diseases that today most people don't consider to be a major health concern," says Johannes Krause, director at the Max Planck Institute for the Science of Human History.

The current study allows the scientists to gain a perspective on the changes in the disease over time and in different human cultural contexts. "We're beginning to understand the genetics of host adaptation in Salmonella," says Key, "and we can translate that knowledge into mechanistic understanding about the emergence of human and animal adapted diseases."

The scientists hope that the current study will illuminate the possibilities of these methods and that future research will further examine the ways that human cultural evolution has impacted and driven the evolution of human-adapted diseases.
-end-
Publication information:

Title: Emergence of human-adapted Salmonella enterica is linked to the Neolithization process

Authors: Felix M. Key, Cosimo Posth, Luis R. Esquivel-Gomez, Ron Hübler, Maria A. Spyrou, Gunnar U. Neumann, Anja Furtwängler, Susanna Sabin, Marta Burri, Antje Wissgott, Aditya Kumar Lankapalli, Åshild J. Vågene, Matthias Meyer, Sarah Nagel, Rezeda Tukhbatova, Aleksandr Khokhlov, Andrey Chizhevsky, Svend Hansen, Andrey B. Belinsky, Alexey Kalmykov, Anatoly R. Kantorovich, Vladimir E. Maslov, Philipp W. Stockhammer, Stefania Vai, Monica Zavattaro, Alessandro Riga, David Caramelli, Robin Skeates, Jessica Beckett, Maria Giuseppina Gradoli, Noah Steuri, Albert Hafner, Marianne Ramstein, Inga Siebke, Sandra Lösch, Yilmaz Selim Erdal, Nabil-Fareed Alikhan, Zhemin Zhou, Mark Achtman, Kirsten Bos, Sabine Reinhold, Wolfgang Haak, Denise Kühnert, Alexander Herbig, Johannes Krause

Publication: Nature Ecology and Evolution

DOI: 10.1038/s41559-020-1106-9

Media Contacts:

Felix M. Key
fkey@mit.edu
Massachusetts Institute of Technology

Alexander Herbig
Max Planck Institute for the Science of Human History
herbig@shh.mpg.de

Johannes Krause
Max Planck Institute for the Science of Human History
Krause@shh.mpg.de

AJ Zeilstra / Petra Mader
Max Planck Institute for the Science of Human History
Public Relations & Press Office
Kahlaische Str. 10
07745 Jena
GERMANY
Phone: +49 (0) 3641 686-950 / 960
Email: presse@shh.mpg.de

Max Planck Institute for the Science of Human History

Related Science Articles from Brightsurf:

75 science societies urge the education department to base Title IX sexual harassment regulations on evidence and science
The American Educational Research Association (AERA) and the American Association for the Advancement of Science (AAAS) today led 75 scientific societies in submitting comments on the US Department of Education's proposed changes to Title IX regulations.

Science/Science Careers' survey ranks top biotech, biopharma, and pharma employers
The Science and Science Careers' 2018 annual Top Employers Survey polled employees in the biotechnology, biopharmaceutical, pharmaceutical, and related industries to determine the 20 best employers in these industries as well as their driving characteristics.

Science in the palm of your hand: How citizen science transforms passive learners
Citizen science projects can engage even children who previously were not interested in science.

Applied science may yield more translational research publications than basic science
While translational research can happen at any stage of the research process, a recent investigation of behavioral and social science research awards granted by the NIH between 2008 and 2014 revealed that applied science yielded a higher volume of translational research publications than basic science, according to a study published May 9, 2018 in the open-access journal PLOS ONE by Xueying Han from the Science and Technology Policy Institute, USA, and colleagues.

Prominent academics, including Salk's Thomas Albright, call for more science in forensic science
Six scientists who recently served on the National Commission on Forensic Science are calling on the scientific community at large to advocate for increased research and financial support of forensic science as well as the introduction of empirical testing requirements to ensure the validity of outcomes.

World Science Forum 2017 Jordan issues Science for Peace Declaration
On behalf of the coordinating organizations responsible for delivering the World Science Forum Jordan, the concluding Science for Peace Declaration issued at the Dead Sea represents a global call for action to science and society to build a future that promises greater equality, security and opportunity for all, and in which science plays an increasingly prominent role as an enabler of fair and sustainable development.

PETA science group promotes animal-free science at society of toxicology conference
The PETA International Science Consortium Ltd. is presenting two posters on animal-free methods for testing inhalation toxicity at the 56th annual Society of Toxicology (SOT) meeting March 12 to 16, 2017, in Baltimore, Maryland.

Citizen Science in the Digital Age: Rhetoric, Science and Public Engagement
James Wynn's timely investigation highlights scientific studies grounded in publicly gathered data and probes the rhetoric these studies employ.

Science/Science Careers' survey ranks top biotech, pharma, and biopharma employers
The Science and Science Careers' 2016 annual Top Employers Survey polled employees in the biotechnology, biopharmaceutical, pharmaceutical, and related industries to determine the 20 best employers in these industries as well as their driving characteristics.

Three natural science professors win TJ Park Science Fellowship
Professor Jung-Min Kee (Department of Chemistry, UNIST), Professor Kyudong Choi (Department of Mathematical Sciences, UNIST), and Professor Kwanpyo Kim (Department of Physics, UNIST) are the recipients of the Cheong-Am (TJ Park) Science Fellowship of the year 2016.

Read More: Science News and Science Current Events
Brightsurf.com is a participant in the Amazon Services LLC Associates Program, an affiliate advertising program designed to provide a means for sites to earn advertising fees by advertising and linking to Amazon.com.