Pathogenic microorganisms in frozen environments

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Ancient bacteria found in the permafrost possess a remarkable range of antibiotic resistance genes (red). However, their capacity to resist is also generally lower than of modern bacteria from the same area (black). Perron 2015 permafrost antibiotic resistances.png
Ancient bacteria found in the permafrost possess a remarkable range of antibiotic resistance genes (red). However, their capacity to resist is also generally lower than of modern bacteria from the same area (black).

On Earth, frozen environments such as permafrost and glaciers are known for their ability to preserve items, as they are too cold for ordinary decomposition to take place. This makes them a valuable source of archeological artefacts and prehistoric fossils, yet it also means that there are certain risks once ancient organic matter is finally subject to thaw. The best-studied risk is that of decomposition of such organic matter releasing a substantial quantity of carbon dioxide and methane, and thus acting as a notable climate change feedback. Yet, some scientists have also raised concerns about the possibility that some metabolically dormant bacteria and protists, as well as always metabolically inactive viruses, may both survive the thaw and either threaten humans directly, or affect some of the animal or plant species important for human wellbeing.

Contents

As of 2023, there has been at least one recorded reemergence of anthrax, a pathogen long-known for its ability to hibernate in soils. There have also been several cases when truly novel microorganisms discovered in the frozen environments were successfully revived by researchers, or were found live in a recently thawed environment. So far, most only affect amoebas, and none have been known to pose a risk to humans or to crops. Of the already-studied pathogens, at least one anthrax outbreak has been connected to decades-old infected carrion thaw; yet, samples of influenza and smallpox pathogens have failed to survive the thaw even in laboratory conditions. Some researchers have also raised alarm about the potential of horizontal gene transfer between ancient and modern bacteria, and the risk it could exacerbate the challenge of antibiotic resistance. At the same time, other scientists consider these concerns overblown, and argue that ancient microorganisms are unlikely to make a difference today.

Timeline of research into the subject

20th century

Johan Hultin made multiple attempts during the 20th century to culture 1918 influenza virus he found in the frozen corpses of pandemic victims at Brevig Mission in Alaska. Every attempt failed, which suggested that the influenza virus is incapable of surviving the thaw after being frozen. In the 1990s, other scientists have tried to revive pneumonia-causing bacteria and the smallpox virus, yet all of those attempts were unsuccessful as well. [2]

1999

A group of researchers was able to extract potentially viable microscopic fungi, as well as the RNA of tomato mosaic virus, from Greenland ice cores up to 140,000 years old. [3] [4]

2004

It was estimated that between 1017 and 1021 microorganisms, ranging from fungi and bacteria in addition to viruses, were already released every year due to ice melt, often directly into the ocean. According to researchers behind this estimate, only viruses with high abundance, ability to be transported through ice, and ability to resume disease cycles after the thaw would be of any concern.

In particular, caliciviruses of Vesivirus genus were hypothesized as the most likely to spread from ancient ice, due to their high abundance and using ocean animals as hosts, where the migratory nature of many species of fish and birds could potentially enable a high transmission rate. Caliciviruses are poorly adapted to humans, and the only known infections were of marine biologists who worked closely with infected seals. However, Enteroviruses (a group which includes polioviruses, echoviruses and Coxsackie viruses) and even influenza A were also considered less likely but still plausible candidates. [5]

2005

In the 1960s, the United States Army Corps of Engineers had dug out Fox tunnel in Alaska, to provide a good test ground to better understand permafrost before the construction of the Trans-Alaska Pipeline System. By 2005, scientists revisiting that tunnel have discovered frozen cells of carnobacterium pleistocenium, with an estimated age of 32,000 years. Melting the ice had revived them, resulting in the first documented case of an organism "coming back to life" from ancient ice. [6] None of the bacteria in carnobacterium genus are known to be pathogenic in humans, although some are known for spoiling chilled food products, and one species may cause disease in fish. [7]

2011

A paper by two Russian scientists in Global Health Action, a journal published by Umeå University in Sweden, had warned of the risk that the old burial grounds of cattle which had died to anthrax in the early last century may thaw and lead to the re-emergence of the viable pathogen. The authors noted that at the time, there were about 13,885 cattle burial grounds in Northern Russia, a substantial fraction of which did not meet sanitary standards, and some had their maps or other records missing. [8]

2014

A completely unknown plant virus was revived from a frozen caribou feces deposit which was only 700 years old. It was named "ancient caribou feces associated virus" (aCFV) by its discoverers. The scientists have also introduced this virus into the tissues of Nicotiana benthamiana, a common model species for plant pathogens. aCFV had successfully replicated, yet was unable to cause more than an asymptomatic infection. According to the researchers, this either suggests a large genetic distance between the original host species of aCFV and more modern plants, or that N. benthamiana was simply a suboptimal host for this species. [9]

Also in 2014, two ~30,000 years old giant virus species, Pithovirus sibericum [10] and Mollivirus sibericum, [11] were discovered in the Siberian permafrost and they retained their infectivity. Like the other giant viruses with large genomes, they are larger in size than most bacteria and pose no risk to humans, as they infect other microorganisms like Acanthamoeba, a genus of amoebas. [11]

2016

An anthrax outbreak had occurred in the Yamal Peninsula region in Northern Russia. It was thought to be linked to an infected reindeer corpse, which died 75 years earlier, yet had thawed after a heatwave. Over 2,000 reindeer had been infected and the disease had spread to humans, hospitalizing dozens and killing a child before the outbreak was contained. [12]

2023

Some of the ancient amoeba-eating viruses revived by the research team of Jean-Michel Claverie. Clockwise from the top: Pandoravirus yedoma; Pandoravirus mammoth and Megavirus mammoth; Cedratvirus lena; Pithovirus mammoth; Megavirus mammoth; Pacmanvirus lupus. Alempic 2023 permafrost viruses.jpg
Some of the ancient amoeba-eating viruses revived by the research team of Jean-Michel Claverie. Clockwise from the top: Pandoravirus yedoma; Pandoravirus mammoth and Megavirus mammoth; Cedratvirus lena; Pithovirus mammoth; Megavirus mammoth; Pacmanvirus lupus.

The same team of French researchers behind the 2014 revival of two giant viruses had also managed to revive 8 more ancient amoeba-infecting viral species. Four of these species were from the pandoravirus, cedratvirus (sometimes classified as a subgroup of pithovirus), megavirus and pacmanvirus (part of Asfarviridae) families, which weren't previously revived from the permafrost. In addition, five more species from these families were found in already thawed permafrost, with no way to tell their age. The oldest revived virus was a 48,500-year-old Pandoravirus yedoma . [13] [14]

Current scientific understanding

Scientists are split on whether revived microorganisms from the permafrost can pose a significant threat to humans. Jean-Michel Claverie, who led the most successful attempts to revive such "zombie viruses", believes that the public health threat from them is underestimated, and that while his research focused on amoeba-infecting viruses, this decision was in part motivated by the desire to avoid viral spillover as well as convenience, and "one can reasonably infer" other viral species would also remain infectious. [13] [14] Another professor, Birgitta Evengård, argued that permafrost thaw would eventually uncover microorganisms older than the human species, and to which there would be no preexisting immunity. In the same interview, Claverie had even suggested that ancient microorganisms might have had caused or contributed to the extinction of Neanderthals or mammoths, and that those may still be preserved in the permafrost. [15] On the other hand, University of British Columbia virologist Curtis Suttle argued that "people already inhale thousands of viruses every day, and swallow billions whenever they swim in the sea". In his view, the odds of a frozen virus replicating and then circulating to a sufficient extent to threaten humans "stretches scientific rationality to the breaking point". [16]

While some point to the 2016 Yamal Peninsula outbreak as an example of dangers associated with the thaw, [12] others argue that anthrax is not a pathogen which can spread contagiously between humans, and that it has been known for its ability to remain dormant in the soil since the Middle Ages, without requiring the cold to do so. [2] Some scientists have argued that Hultin's inability to revive thawed influenza virus, as well as other researchers' failure to revive pneumonia-causing bacteria or smallpox viruses show that pathogens adapted to warm-blooded hosts cannot survive being frozen for a prolonged period of time. [2] [17] However, many of the amoeba-infecting viruses revived in Claverie's 2023 research were taken from a ~27,000-year-old site with "a large amount of mammoth wool", and one species, Pacmanvirus lupus, was found in the intestine of an equally old Siberian wolf carcass. [13]

There is some agreement that revived bacteria would be less dangerous than the revived viruses, since they would still be affected by broad-spectrum antibiotics and would not require wholly new treatments. [13] However, they would not be completely vulnerable either, due to the discovery of ancient antibiotic resistance genes in permafrost samples. Antibiotics to which permafrost bacteria have displayed at least some resistance include chloramphenicol, streptomycin, kanamycin, gentamicin, tetracycline, spectinomycin and neomycin. [18] Some scientists consider horizontal gene transfer of novel antibiotic resistance sequences from otherwise harmless ancient bacteria into modern pathogens to be a far more realistic threat than a revival of an ancient pathogen. [19] At the same time, other studies show that resistance levels in ancient bacteria to modern antibiotics remain lower than in the contemporary bacteria from the active (thawed) layer above them, [1] suggesting that this risk is "no greater" than in any other soil. [17]

According to an 2023 interview with Marion Koopmans, the head of the Netherlands' Versatile Emerging infectious disease Observatory (VEO), precautions taken by the researchers studying potentially risky sites in Greenland include not starting new digs and only analyizing the locations which were already going to be studied by archeologists, wearing protective gear while in the field, and operating under high BSL standards in the lab. If a place was found to harbour a potentially dangerous microorganism, they have the authority to advise the Naalakkersuisut to shut down access to the area. [20]

See also

Related Research Articles

<span class="mw-page-title-main">Antimicrobial resistance</span> Resistance of microbes to drugs directed against them

Antimicrobial resistance (AMR) occurs when microbes evolve mechanisms that protect them from the effects of antimicrobials. All classes of microbes can evolve resistance where the drugs are no longer effective. Fungi evolve antifungal resistance, viruses evolve antiviral resistance, protozoa evolve antiprotozoal resistance, and bacteria evolve antibiotic resistance. Together all of these come under the umbrella of antimicrobial resistance. Microbes resistant to multiple antimicrobials are called multidrug resistant (MDR) and are sometimes referred to as superbugs. Although antimicrobial resistance is a naturally occurring process, it is often the result of improper usage of the drugs and management of the infections.

<span class="mw-page-title-main">Microorganism</span> Microscopic living organism

A microorganism, or microbe, is an organism of microscopic size, which may exist in its single-celled form or as a colony of cells.

<span class="mw-page-title-main">Pandemic</span> Widespread, often global, epidemic of severe infectious disease

A pandemic is an epidemic of an infectious disease that has spread across a large region, for instance multiple continents or worldwide, affecting a substantial number of individuals. Widespread endemic diseases with a stable number of infected individuals such as recurrences of seasonal influenza are generally excluded as they occur simultaneously in large regions of the globe rather than being spread worldwide.

A human pathogen is a pathogen that causes disease in humans.

<span class="mw-page-title-main">Zoonosis</span> Disease that can be transmitted from other species to humans

A zoonosis or zoonotic disease is an infectious disease of humans caused by a pathogen that can jump from a non-human to a human and vice versa.

<span class="mw-page-title-main">Infection</span> Invasion of an organisms body by pathogenic agents

An infection is the invasion of tissues by pathogens, their multiplication, and the reaction of host tissues to the infectious agent and the toxins they produce. An infectious disease, also known as a transmissible disease or communicable disease, is an illness resulting from an infection.

<span class="mw-page-title-main">Anthrax</span> Infection caused by Bacillus anthracis bacteria

Anthrax is an infection caused by the bacterium Bacillus anthracis. Infection typically occurs by contact with the skin, inhalation, or intestinal absorption. Symptom onset occurs between one day and more than two months after the infection is contracted. The skin form presents with a small blister with surrounding swelling that often turns into a painless ulcer with a black center. The inhalation form presents with fever, chest pain and shortness of breath. The intestinal form presents with diarrhea, abdominal pains, nausea and vomiting.

<span class="mw-page-title-main">Koch's postulates</span> Four criteria showing a causal relationship between a causative microbe and a disease

Koch's postulates are four criteria designed to establish a causal relationship between a microbe and a disease. The postulates were formulated by Robert Koch and Friedrich Loeffler in 1884, based on earlier concepts described by Jakob Henle, and the statements were refined and published by Koch in 1890. Koch applied the postulates to describe the etiology of cholera and tuberculosis, both of which are now ascribed to bacteria. The postulates have been controversially generalized to other diseases. More modern concepts in microbial pathogenesis cannot be examined using Koch's postulates, including viruses and asymptomatic carriers. They have largely been supplanted by other criteria such as the Bradford Hill criteria for infectious disease causality in modern public health and the Molecular Koch's postulates for microbial pathogenesis.

<span class="mw-page-title-main">Permafrost</span> Soil frozen for a duration of at least two years

Permafrost is soil or underwater sediment which continuously remains below 0 °C (32 °F) for two years or more: the oldest permafrost had been continuously frozen for around 700,000 years. While the shallowest permafrost has a vertical extent of below a meter (3 ft), the deepest is greater than 1,500 m (4,900 ft). Similarly, the area of individual permafrost zones may be limited to narrow mountain summits or extend across vast Arctic regions. The ground beneath glaciers and ice sheets is not usually defined as permafrost, so on land, permafrost is generally located beneath a so-called active layer of soil which freezes and thaws depending on the season.

Serial passage is the process of growing bacteria or a virus in iterations. For instance, a virus may be grown in one environment, and then a portion of that virus population can be removed and put into a new environment. This process is repeated with as many stages as desired, and then the final product is studied, often in comparison with the original virus.

<i>Mimivirus</i> Genus of viruses

Mimivirus is a genus of giant viruses, in the family Mimiviridae. Amoeba serve as their natural hosts. This genus contains a single identified species named Acanthamoeba polyphaga mimivirus (APMV). It also refers to a group of phylogenetically related large viruses.

<span class="mw-page-title-main">Medical microbiology</span> Branch of medical science

Medical microbiology, the large subset of microbiology that is applied to medicine, is a branch of medical science concerned with the prevention, diagnosis and treatment of infectious diseases. In addition, this field of science studies various clinical applications of microbes for the improvement of health. There are four kinds of microorganisms that cause infectious disease: bacteria, fungi, parasites and viruses, and one type of infectious protein called prion.

<span class="mw-page-title-main">Introduction to viruses</span> Non-technical introduction to viruses

A virus is a tiny infectious agent that reproduces inside the cells of living hosts. When infected, the host cell is forced to rapidly produce thousands of identical copies of the original virus. Unlike most living things, viruses do not have cells that divide; new viruses assemble in the infected host cell. But unlike simpler infectious agents like prions, they contain genes, which allow them to mutate and evolve. Over 4,800 species of viruses have been described in detail out of the millions in the environment. Their origin is unclear: some may have evolved from plasmids—pieces of DNA that can move between cells—while others may have evolved from bacteria.

<i>Silene stenophylla</i> Species of flowering plant

Silene stenophylla is a species of flowering plant in the family Caryophyllaceae. Commonly called narrow-leafed campion, it is a species in the genus Silene. It grows in the Arctic tundra of far eastern Siberia and the mountains of northern Japan. Frozen samples, estimated via radiocarbon dating to be around 32,000 years old, were discovered in the same area as current living specimens, and in 2012, a team of scientists successfully regenerated a plant from the samples.

In biology, a pathogen, in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ.

The host–pathogen interaction is defined as how microbes or viruses sustain themselves within host organisms on a molecular, cellular, organismal or population level. This term is most commonly used to refer to disease-causing microorganisms although they may not cause illness in all hosts. Because of this, the definition has been expanded to how known pathogens survive within their host, whether they cause disease or not.

<i>Pandoravirus</i> Genus of giant virus possessing a large double-stranded DNA genome

Pandoravirus is a genus of giant virus, first discovered in 2013. It is the second largest in physical size of any known viral genus, behind only Pithovirus. Pandoraviruses have double stranded DNA genomes, with the largest genome size of any known viral genus.

<i>Pithovirus</i> Genus of viruses

Pithovirus, first described in a 2014 paper, is a genus of giant virus known from two species, Pithovirus sibericum, which infects amoebas and Pithovirus massiliensis. It is a DNA based virus and is a member of the nucleocytoplasmic large DNA viruses clade. The 2014 discovery was made when a viable specimen was found in a 30,000-year-old ice core harvested from permafrost in Siberia, Russia.

Mollivirus sibericum is a giant virus discovered in 2015 by French researchers Chantal Abergel and Jean-Michel Claverie in a 30,000-year-old sample of Siberian permafrost, where the team had previously found the unrelated giant virus Pithovirus sibericum. Mollivirus sibericum is a spherical DNA virus with a diameter of 500–600 nanometers (0.5–0.6 μm).

References

  1. 1 2 Perron, Gabriel G.; Whyte, Lyle; Turnbaugh, Peter J.; Goordial, Jacqueline; Hanage, William P.; Dantas, Gautam; Desai, Michael M. Desai (25 March 2015). "Functional Characterization of Bacteria Isolated from Ancient Arctic Soil Exposes Diverse Resistance Mechanisms to Modern Antibiotics". PLOS ONE. 10 (3): e0069533. Bibcode:2015PLoSO..1069533P. doi: 10.1371/journal.pone.0069533 . PMC   4373940 . PMID   25807523.
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  3. ↑ Ma, Lijun; Catranis, Catharine M.; Starmer, William T.; Rogers, Scott O. (1999). "Revival and characterization of fungi from ancient polar ice". Mycologist. 13 (2): 70–73. doi:10.1016/S0269-915X(99)80012-3.
  4. ↑ Castello, John D.; Rogers, Scott O.; Starmer, William T.; Catranis, Catharine M.; Ma, Lijun; Bachand, George D.; Zhao, Yinghao; Smith, James E. (1999). "Detection of tomato mosaic tobamovirus RNA in ancient glacial ice". Polar Biology. 22 (3): 207–212. Bibcode:1999PoBio..22..207C. doi:10.1007/s003000050411. S2CID   19202446.
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  6. ↑ Pikuta, E. V. (1 January 2005). "Carnobacterium pleistocenium sp. nov., a novel psychrotolerant, facultative anaerobe isolated from permafrost of the Fox Tunnel in Alaska". International Journal of Systematic and Evolutionary Microbiology. 55 (1): 473–478. doi: 10.1099/ijs.0.63384-0 . PMID   15653921.
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  11. 1 2 Legendre, Matthieu; Lartigue, Audrey; Bertaux, Lionel; Jeudy, Sandra; Bartoli, Julia; Lescot, Magali; Alempic, Jean-Marie; Ramus, Claire; Bruley, Christophe; Labadie, Karine; Shmakova, Lyubov (2015). "In-depth study of Mollivirus sibericum, a new 30,000-y-old giant virus infecting Acanthamoeba". Proceedings of the National Academy of Sciences of the United States of America. 112 (38): E5327–E5335. Bibcode:2015PNAS..112E5327L. doi: 10.1073/pnas.1510795112 . JSTOR   26465169. PMC   4586845 . PMID   26351664.
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  13. 1 2 3 4 5 Alempic, Jean-Marie; Lartigue, Audrey; Goncharov, Artemiy; Grosse, Guido; Strauss, Jens; Tikhonov, Alexey N.; Fedorov, Alexander N.; Poirot, Olivier; Legendre, Matthieu; Santini, Sébastien; Abergel, Chantal; Claverie, Jean-Michel (18 February 2023). "An Update on Eukaryotic Viruses Revived from Ancient Permafrost". Viruses. 15 (2): 564. doi: 10.3390/v15020564 . PMC   9958942 . PMID   36851778.
  14. 1 2 Alund, Natalie Neysa (9 March 2023). "Scientists revive 'zombie virus' that was frozen for nearly 50,000 years". USA Today . Archived from the original on 2023-04-24. Retrieved 2023-04-23.
  15. ↑ Dewan, Pandora (12 November 2023). "Scientists Fear Cataclysmic 'Factor X' Will Emerge From Earth's Permafrost". Newsweek. Archived from the original on 21 November 2023. Retrieved 14 December 2023.
  16. ↑ Yong, Ed (3 March 2014). "Giant virus resurrected from 30,000-year-old ice". Nature . Archived from the original on 2023-04-24. Retrieved 2023-04-24.
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  19. ↑ Sajjad, Wasim; Rafiq, Muhammad; Din, Ghufranud; Hasan, Fariha; Iqbal, Awais; Zada, Sahib; Ali, Barkat; Hayat, Muhammad; Irfan, Muhammad; Kang, Shichang (15 September 2020). "Resurrection of inactive microbes and resistome present in the natural frozen world: Reality or myth?". Science of the Total Environment. 735: 139275. Bibcode:2020ScTEn.735m9275S. doi:10.1016/j.scitotenv.2020.139275. PMID   32480145. S2CID   219169932.
  20. ↑ Cohen, Jon (2023). "Lurking in the deep freeze?". Science . 381 (6665): 1406–1407. Bibcode:2023Sci...381.1406C. doi:10.1126/science.adl0420. PMID   37769079. S2CID   263135356. Archived from the original on 2 October 2023. Retrieved 26 October 2023.
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