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Revival of Ice Age Nematode Reveals a New Species

A female P. kolymaensis.
P. kolymaensis, female. Scanning electron picture. Credit: Alexei V. Tchesunov and Anastasia Shatilovich / Institute of Physicochemical and Biological Problems in Soil Science RAS.
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Through genetic analyses, a collaborative research team has shown that a 46,000-year-old roundworm discovered in the Siberian Permafrost is a previously undescribed species. The research is published in PLoS Genetics.

Cryptobiosis – when organisms press pause on life

It may sound like science fiction, but some organisms are capable of pressing the “pause” button on life. When facing extreme adverse environmental conditions – such as oxygen deficiency or freezing cold temperatures – organisms including nematodes and tardigrades enter cryptobiosis, a condition where all metabolic processes come to a grinding halt. Reproductive, developmental and cellular repair mechanisms stop, yet the organism is able to survive for long periods of time until the environmental conditions are once again favorable.

Forms of cryptobiosis

There are different forms of cryptobiosis, including cryobiosis, which is initiated in response to decrease temperature, osmobiosis, a reaction to a rise in external osmotic pressure and anhydrobiosis, which occurs when there is excess water loss (desiccation).

In 2018, Anastasia Shatilovich and colleagues at the Institute of Physicochemical and Biological Problems in Soil Science RAS in Russia discovered two nematodes in a fossilized burrow in the Siberian Permafrost. The nematodes were thawed in the laboratory and plant material from the burrow was subjected to radiocarbon analysis, suggesting that the frozen deposits had not thawed since the late Pleistocene, between 45,839 and 47,769 years ago.

Over at the Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) in Dresden, Professor Teymuras Kurzchalia – who has since retired – was exploring how Caenorhabditis elegans, a commonly used laboratory mode, survives extreme conditions at its larval stage. After hearing about the Permafrost discovery, Kurzhalia’s team reached out to Shatilovich to collaborate. “What molecular and metabolic pathways these cryptobiotic organisms use and how long they would be able to suspend life are not fully understood,” says Dr. Vamshidhar Gade, who was a doctoral student in Kurzchalia’s team at the time. To uncover the organisms’ secrets for surviving thousands of years, the researchers teamed up with the Center for Systems Biology Dresden (CSBD) and the Institute of Zoology at the University of Cologne.

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A novel species – Panagrolaimus kolymaensis

Recent advancements in DNA extraction and next-generation sequencing are enabling scientists to piece together the genomes of ancient organisms. Eugene Myers, now professor of comparative genomics at the LOEWE-TBG and the Senckenberg Society for Nature Research, supported the efforts to conduct a high-quality genome assembly of one of the permafrost nematodes. This was not an easy feat, and Professor Philipp Schiffer, research group leader at the Institute of Zoology, came on board as support. Using phylogenomic analysis, his team identified the nematode belonged to a previously undescribed species. It was named Panagrolaimus kolymaensis in tribute to the Kolyma River where the organism was discovered, and bears a Latin name of “Kolymaensis”.

“Despite the challenges that a triploid genome poses for assembly, we obtained a highly contiguous contig assembly of the three pseudohaplotypes that comprise almost 266 Mb and thus have a similar genome size as other parthenogenetic Panagrolaimus species,” the researchers write.

The molecular mechanisms behind extreme long-term survival

As there are no existing genetic methods for studying P. kolymaensis, the researchers utilized C. elegans as a comparator system to further understand the molecular pathways involved in the new species’ long-term survival. Genes known to be implicated in cryptobiosis in C. elegans larva were also found in P. kolymaensis, including trehalose phosphate synthase gene (tps-2) and trehalose phosphatase gene (gob-1).

For C. elegans larva to survive extreme desiccation, it must first be preconditioned in conditions of high humidity. “During preconditioning, dauer larvae upregulate trehalose biosynthesis that ensures their survival to harsh desiccation,” the researchers describe. The group questioned whether P. kolymaensis would require similar conditions, discovering that mild dehydration exposure prior to freezing supported the nematodes’ preparation for cryptobiobsis. It also increased its survival at temperatures of 80 degrees °C.

“This study extends the longest reported cryptobiosis in nematodes by tens of thousands of years,” says Kurzchalia.

Both C. elegans and P. kolymaensis were found to produce trehalose – a type of sugar – when mildly dehydrated. The researchers suggest this molecule helps with their endurance through freezing and intense dehydration. “Our findings are essential for understanding evolutionary processes because generation times can range from days to millennia and because the long-term survival of a species' individuals can result in the re-emergence of lineages that would otherwise have gone extinct,” says Schiffer.

Myers adds: “P. kolymaensis's highly contiguous genome will make it possible to compare this feature to those of other Panagrolaimus species whose genomes are presently being sequenced by Schiffer’s team and colleagues.”

In Schiffer’s opinion, studying how species adapt to extreme environments will support conservation efforts as the threat of global warming intensifies.

Reference: Shatilovich A, Gade VR, Pippel M, et al. A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva. PLOS Genetics. 2023;19(7):e1010798. doi: 10.1371/journal.pgen.1010798

This article is a rework of a press release issued by the Max Planck Institute of Molecular Cell Biology and Genetics. Material has been edited for length and content.