Paleomicrobiology: Tracking the past microbial life from single species to entire microbial communities

Abstract

By deciphering information encoded in degraded ancient DNA extracted from up to million-years-old samples, molecular paleomicrobiology enables to objectively retrace the temporal evolution of microbial species and communities. Assembly of full-length genomes of ancient pathogen lineages allows not only to follow historical epidemics in space and time but also to identify the acquisition of genetic features that represent landmarks in the evolution of the host-microbe interaction. Analysis of microbial community DNA extracted from essentially human paleo-artefacts (paleofeces, dental calculi) evaluates the relative contribution of diet, lifestyle and geography on the taxonomic and functional diversity of these guilds in which have been identified species that may have gone extinct in today's human microbiome. As for non-host-associated environmental samples, such as stratified sediment cores, analysis of their DNA illustrates how and at which pace microbial communities are affected by local or widespread environmental disturbance. Description of pre-disturbance microbial diversity patterns can aid in evaluating the relevance and effectiveness of remediation policies. We finally discuss how recent achievements in paleomicrobiology could contribute to microbial biotechnology in the fields of medical microbiology and food science to trace the domestication of microorganisms used in food processing or to illustrate the historic evolution of food processing microbial consortia.

FIGURE 1

Main types of historical samples used as sources of ancient microbial DNA. These samples can be extremely ancient as Bronze Age teeth or dental calculi or much more recent such as often less than 100‐year‐old herbarium plants. These samples have been used to study either specific (often pathogenic) microbial species or entire communities.

FIGURE 2

Main characteristics of ancient DNA. While DNA extracted from living organisms is made of long molecules, often exceeding 1 kbp in length and perfectly representative of the original organism's genomic sequence, ancient DNA extracted from historical samples has experienced post‐mortem damages. They lead to DNA fragmentation (fragments often shorter than 100 bp) and base modifications altering the original sequence. Thus, cytosine deamination produces uracil, preferentially at the ends of the molecules. Photo credits: modern plant samples: ©Herbier LY, FR‐CERESE, UCBLyon1 Recolnat portal (https://explore.recolnat.org/) under accessions LY0662689.

FIGURE 3

Main achievements and research fields explored by molecular paleomicrobiology.