Ancient microbes emerging from the permafrost
Next to the threat that is present in laboratories, a second risk is present in natural ecosystems, given that our planet is in a time of climate change.
These changes can be observed in the atmosphere (increasing temperatures), the ocean (ocean warming, increasing salinization, acidification, and rising sea levels), and the cryosphere (loss of ice mass and snow cover).
In general, climate change poses potential risks to people, society, economy, and ecosystems. The greatest increase in temperature has been observed in areas of mid‐ and high latitudes, as arctic temperatures are rising rapidly, being twice the global rate (Schuur & Abbott, 2011; Slenning, 2010).
Natural microbial populations in the permafrost are thus shaped by current and future environmental challenges and interactions. In particular, a historical factor that may induce future challenges is present via the resurrection of dormant propagules and viable vectors.
As the permafrost serves as a natural bank, it contains a variety of dormant propagules (seeds, eggs, cysts, or spores from plants and invertebrates) and other viable vectors (bacteria, viruses). This may increase the risk of infections (Revich & Podolnaya, 2011; Revich, Tokarevich, & Parkinson, 2012). Over the past few years, there has been increasing evidence that the permafrost is a gigantic reservoir of ancient microbes or viruses that may come back to life if environmental conditions change and set them free again.
The amount of microorganisms trapped in permafrost which remains viable can range up to 108 cells/g of dry soil (Vorobyova et al., 1997). The thawing of the permafrost increases the resurrection of different dormant vectors, such as bacteria which can remain viable for several million years (Vishnivetskaya, Kathariou, McGrath, Gilichinsky, & Tiedje, 2000).
For example in 2014, a viable specimen of a giant virus, named Pithovirus sibericum, was found in a 30,000‐year‐old ice core harvested from Siberian permafrost, and revived in the laboratory. Interestingly, this virus was found to be still infective to its natural amoeboid host (Legendre et al., 2014).
Similarly, Ng et al. (2014) recovered and characterized two viruses preserved in 700‐year‐old caribou feces frozen in a permanent ice patch. One of these viruses is a distant relative of the geminiviruses, a well‐known group of plant viruses, whereas the second one is related to a group of insect RNA viruses pathogenic to beneficial arthropods, such as honeybees, as well as to insect pests of medical and agricultural importance.
Remarkably, these viruses were still intact and remained infectious after being 700 years in ice. There is thus a risk, especially given that the Russian Arctic is particularly affected by climate change. Especially, the plant virus was shown to be infective to the modern plant Nicotiana benthamiana, a relative of tobacco that is native to northern Australia and is thus clearly not the natural host of this virus (Holmes, 2014; Ng et al., 2014).
Such results indicate that potentially infectious pathogens might be released from ancient permafrost layers exposed to thawing with potential consequences for human, animal, and plant populations. In addition, the rich mineral resources and oil reserves of the arctic regions are under increasing pressure for their industrial exploitation (i.e., mining and drilling; Revich et al., 2012; Legendre et al., 2014).
Such events will result in flooding and disruption of soil, which may release bacterial spores or viruses onto the surface soil and vegetation which would then be consumed by grazing animals, also increasing the risk of infection in humans who come into contact with infected animal products (under cooked meat, hides, bone; Revich et al., 2012).
Although the risk posed by potential pathogens trapped in ice is low compared to the normal horizontal spread of contemporary viruses among host populations, and the warmer temperature associated with ice melting may partly degrade viral nucleic acids (Holmes, 2014), these pathogens are not exempt from posing future threats to human and animal health (Legendre et al., 2014). In Russia, epizootic cycles of anthrax which caused the death of 1.5 million deer between 1897 and 1925 have resulted in more than 13,000 burial grounds containing the carcasses of infected animals. With ice thawing, these carcasses may reappear, resulting in frequent anthrax outbreaks among cattle and reindeer, also infecting humans who process infected animal products or ingest improperly cooked infected meat (Revich et al., 2012).
In 2016, the indigenous peoples in the Yamal‐Nenets Region (Russia) were victims of anthrax and needed to be hospitalized, while the herd of reindeer they use as food source had perished from either the infection or extermination by the Russian Defense Ministry. Thousands of people were forced to relocate, while others were quarantined. This outbreak is thought to stem from the thawing burial grounds of reindeer carcasses dead from an anthrax outbreak 75 years ago.
The community DNA immobilized in permafrost represents an important reservoir of genes that may potentially be acquired by extant microbes upon thawing through lateral gene transfer. Bidle et al. (2007) performed a metagenomic analysis of community DNA found in 100‐ka‐ to 8‐MA‐old ice samples and revealed many diverse orthologs to extant metabolic genes, and some microbes isolated from the same samples were even able to grow in the laboratory. Their analysis suggests that melting of polar ice in the geological past may have provided a conduit for large‐scale lateral gene transfer, potentially scrambling microbial phylogenies and accelerating the tempo of microbial evolution (Bidle et al., 2007).
Remarkably, genes encoding resistance against natural or modern semisynthetic antibiotics, as well as mobile elements participating in their horizontal transfer, were found in bacterial strains isolated from Siberian and Antarctic permafrost grounds, dating from 5,000 to 30,000 years ago (Perron et al., 2015; Petrova, Gorlenko, & Mindlin, 2009; Petrova, Kurakov, Shcherbatova, & Mindlin, 2014).
Many of these resistance genes were highly similar to resistance genes found in pathogenic bacteria today, confirming the hypothesis that the antibiotic resistance genes of clinical bacteria originated from environmental bacteria. Taken together, these results support the hypothesis that a reservoir of resistance genes existed in a range of bacteria species prior to the anthropogenic use of antibiotics and contribute to a growing body of evidence demonstrating that antibiotic resistance evolved alongside antibiotic production in the natural environment (Perron et al., 2015; Petrova et al., 2014).
These results also support the growing body of evidence that nonpathogenic environmental organisms, including those present in the permafrost, are a reservoir of resistance genes that have the potential to be transferred into pathogens, and thus greatly affect the evolution of multidrug‐resistant bacteria in clinical settings (Bhullar et al., 2012).
To make it more complex, there are also microbes that protect their hosts from pathogenic infections. The interaction between these “defensive” microbes and pathogens coevolves within host populations.
Ford, Wiliams, Paterson, and King (2017) experimentally coevolved a microbe with host‐protective properties (Enterococcus faecalis) and a pathogen (Staphylococcus aureus) within nonevolving Caenorhabditis elegans host populations.
They found that after 10 passages, all replicate pathogen populations were locally adapted in time to the defensive microbe, while the defensive microbe was locally maladapted.
This pattern is parallel with host–pathogen coevolution studies which have found that pathogen local adaptation is more commonly identified than host local adaptation because pathogens have faster evolutionary responses to reciprocal adaptation than hosts (due to shorter generation time, larger populations sizes, and higher rates of migration; Ford et al., 2017; Kawecki & Ebert, 2004).
By performing time‐shift experiments, Ford et al. (2017) showed that both the defensive microbe and the pathogen peaked in fitness against antagonist populations recently experienced in evolutionary history.
Defensive microbes from the future were significantly better at suppressing pathogens than defensive microbes from the past, while future pathogens were significantly better at suppressing defensive microbes than pathogens from the past. The fitness of a focal species against their recent enemy is expected to be higher than against their current enemy as the current enemy has begun to respond to the adaptive changes of the focal species.
This shows that interactions between non‐native pathogens (emerging from a different location or from a different time) and native hosts can be very complex. Besides pathogens, defensive microbes can also enter the community and alter the interactions between pathogen and host.
This can be in a positive way by reducing the virulence of the pathogen, but it can also be in a negative way by increasing the virulence of the pathogen, depending on the time lag between the pathogen and the host (Dybdahl & Lively, 1998; Ford et al., 2017; and see further details in the temporal adaptation section below).