1. Introduction

2 ) due to human activities since the industrial revolution is causing significant climate change through global warming. It is now widely acknowledged that an average temperature increase of 1.5 °C relative to 1850–1900 would be exceeded during the 21st century, under all realistic circumstances [ Ongoing international modeling and monitoring studies keep confirming that the continuous release of greenhouse gas (mostly CO) due to human activities since the industrial revolution is causing significant climate change through global warming. It is now widely acknowledged that an average temperature increase of 1.5 °C relative to 1850–1900 would be exceeded during the 21st century, under all realistic circumstances [ 1 ] even though the adequacy of present climate models to predict regional changes remains in debate [ 2 ]. For instance, climate warming is particularly noticeable in the Arctic where average temperatures appear to increase more than twice as fast as in temperate regions [ 3 ]. One of the most visible consequences is the global thawing of permafrost at increasing depths [ 4 5 ], the rapid erosion of permafrost bluffs [ 6 7 ], as well as erosion of deep and old permafrost by thaw slumping in hillslopes [ 8 9 ]. This rapid permafrost thaw causes mobilization of ancient organic matter previously preserved for millennia in permafrost deep layers, a phenomenon most visible in Siberia, where deep continuous permafrost underlays most of the North Eastern territories.

11,12,13, 2 and methane further contributing greenhouse gas to the atmosphere [15, Bacillus anthracis spores from old animals burial grounds or carcasses to resurface [20, The thawing of permafrost has significant microbiological consequences. First, above freezing temperatures, the return of liquid water triggers the metabolic reactivation of numerous soil microorganisms (bacteria, archaea, protists, fungi) [ 10 14 ], exposing the organic material previously trapped in permafrost to decomposition, releasing additional COand methane further contributing greenhouse gas to the atmosphere [ 5 16 ]. Yet, a more immediate public health concern is the physical release and reactivation of bacteria (or archaea) that have remained in cryptobiosis trapped in deep permafrost, isolated from the Earth’s surface for up to two million years [ 10 17 ] (although a more consensual limit would be half a million years [ 18 ]). On a shorter time scale, the periodical return of anthrax epidemics devastating reindeer populations has been linked to the deeper thawing of the permafrost active layer at the soil surface during exceptionally hot summers, allowing century-oldspores from old animals burial grounds or carcasses to resurface [ 19 21 ].

11,12,17,24,25,26,27,29, Acinetobacter , Bacillus anthracis , Brucella , Campylobacter , Clostridia , Mycoplasma , various Enterobacteria , Mycobacteria , Streptococci , Staphylococci , Rickettsia ) [12,24,29,31, One could imagine that very deep permafrost layers (i.e., million-year-old), such as those extracted by open-pit mining, could release totally unknown pathogens [ 22 ]. Finally, the abrupt thawing vertically operating along the whole wall of permafrost bluffs (consisting of specific ice-rich deposits called “yedoma”) such as seen in the Kolyma lowland or around the Yukon River, Alaska, causes the simultaneous release of ancient microorganisms from frozen soils dating from the whole Holocene to the late Pleistocene (i.e., up to 120,000 years ago) [ 23 ]. Many culture-based and culture-independent studies (i.e., barcoding and/or metagenomics) have documented the presence of a large diversity of bacteria in ancient permafrost [ 10 28 ], a significant proportion of which are thought to be alive, although estimates vary greatly with the depth (age) and soil properties [ 17 30 ]. These bacterial populations include relatives of common contemporary pathogens (, various) [ 11 31 ]. Fortunately, we can reasonably hope that an epidemic caused by a revived prehistoric pathogenic bacterium could be quickly controlled by the modern antibiotics at our disposal, as they target cellular structures (e.g., ribosomes) and metabolic pathways (transcription, translation or cell wall synthesis) conserved during the evolution of all bacterial phyla [ 32 ], even though bacteria carrying antibiotic-resistance genes appear to be surprisingly prevalent in permafrost [ 26 33 ].

The situation would be much more disastrous in the case of plant, animal, or human diseases caused by the revival of an ancient unknown virus. As unfortunately well documented by recent (and ongoing) pandemics [ 34 35 ], each new virus, even related to known families, almost always requires the development of highly specific medical responses, such as new antivirals or vaccines. There is no equivalent to “broad spectrum antibiotics” against viruses, because of the lack of universally conserved druggable processes across the different viral families [ 36 37 ]. It is therefore legitimate to ponder the risk of ancient viral particles remaining infectious and getting back into circulation by the thawing of ancient permafrost layers. Focusing on eukaryote-infecting viruses should also be a priority, as bacteriophages are no direct threat to plants, animals, or humans, even though they might shape the microbial ecology of thawing permafrost [ 38 ].