How to put life on hold… or die temporarily

The heart stops, there is no brain activ­i­ty, the body cools down and, final­ly, the mol­e­c­u­lar activ­i­ty with­in each cell dis­ap­pears. Although not simul­ta­ne­ous, human death is marked by sev­er­al char­ac­ter­is­tic ele­ments. How­ev­er, deter­min­ing whether an organ­ism is dead or alive is not always straight­for­ward. There are com­plex clin­i­cal sit­u­a­tions: ani­mals, for exam­ple, prac­tice thanato­sis, or death sim­u­la­tion, to deter preda­tors. Many organ­isms can go through states that chal­lenge our bina­ry per­cep­tion of life and death. 

In your kitchen cup­boards you may find rice, lentils, nuts, pota­toes, onions, apples… All these struc­tures are of plant ori­gin. In oth­er words, they were once alive. But which ones are still alive? In some cas­es, the answer is obvi­ous: a stalk pro­trud­ing from a pota­to fil­let or a sprout pierc­ing the skin of an onion are not so sub­tle clues. There is life in your cup­boards. But it’s not always so clear-cut: how can you tell the dif­fer­ence between a dead and a liv­ing lentil?

Seeds are repro­duc­tive struc­tures, con­tain­ing an embryo and nutri­ent reserves shel­tered by a pro­tec­tive integu­ment. They are capa­ble of remain­ing in a state of appar­ent inac­tiv­i­ty until exter­nal con­di­tions (tem­per­a­ture, light, humid­i­ty, etc.) trig­ger ger­mi­na­tion. In the mean­time, they show no signs of life, but this does not mean they are dead. In fact, they are in an extreme­ly slowed-down state of life known as dor­man­cy. And this state is reversible: if you place lentils on wet cot­ton wool, they will prob­a­bly end up ger­mi­nat­ing. But there’s no point in try­ing the same thing with white rice. Those seeds have been hulled and only the nutri­ent tis­sue they con­tained has reached your kitchen.

Dor­man­cy is a wide­spread phe­nom­e­non in the nat­ur­al world. In some organ­isms, it is sys­tem­at­ic and genet­i­cal­ly pro­grammed, while in oth­ers it is trig­gered only when liv­ing con­di­tions become too unfavourable. The term dia­pause or qui­es­cence is also used to describe cer­tain forms of life slow­ing down. Like seed plants, var­i­ous mam­mals can, for exam­ple, put their repro­duc­tion on hold, with females sav­ing embryos with­out imme­di­ate­ly implant­i­ng them in their uterus. This process, known as embry­on­ic dia­pause¹, makes it pos­si­ble to adapt life cycles to the resources avail­able – which vary accord­ing to the sea­son – and to ensure the best pos­si­ble con­di­tions for the offspring.

In some organ­isms, the metab­o­lism doesn’t just slow down: it stops. These organ­isms are said to be in cryp­to­bio­sis, lit­er­al­ly “hid­den life.” They are not dead, since this state is reversible, but they are no longer obvi­ous­ly alive. Cryp­to­bio­sis can there­fore be con­sid­ered as life in a latent state, a form of tem­po­rary death, or as a third state, dif­fer­ent from both life and death². In fact, the phys­i­ol­o­gy of organ­isms in cryp­to­bio­sis is pro­found­ly altered.

There are sev­er­al forms of cryp­to­bio­sis, linked to dif­fer­ent extreme con­di­tions. The most exten­sive­ly stud­ied is anhy­dro­bio­sis. Anhy­dro­bio­sis is char­ac­terised by the loss of almost all the water in an organ­ism, which is essen­tial for main­tain­ing its integri­ty at cel­lu­lar and bod­i­ly lev­el³. Local replace­ment of water, tran­si­tion to a vit­ri­fied state or spe­cif­ic pro­tec­tion of cer­tain com­pounds, var­i­ous mol­e­c­u­lar adap­ta­tions make it pos­si­ble to tol­er­ate this dras­tic change⁴. As a result, when they are rehy­drat­ed, anhy­dro­bi­ot­ic organ­isms can come back to life, or reviv­i­fy. Under­stand­ing the mech­a­nisms involved in this phe­nom­e­non could be a source of inno­va­tion for all process­es for pre­serv­ing bio­log­i­cal struc­tures by dry­ing or freez­ing, both in med­i­cine and the food industry.

Cryp­to­bio­sis exists on every branch of the liv­ing tree. Ani­mals are capa­ble of it, notably rotifers, nema­todes and the famous tardi­grades⁵. But plants are also affect­ed, such as moss­es and cer­tain ferns. The list extends to lichens, fun­gi and many uni­cel­lu­lar, eukary­ot­ic and prokary­ot­ic organ­isms. Many micro-organ­isms can also form resis­tance struc­tures, more or less dehy­drat­ed, whose meta­bol­ic activ­i­ty is slowed or even stopped.

Some fun­gi and myx­omycetes, such as the blob Physarum poly­cephalum, sur­vive dif­fi­cult peri­ods in the form of des­ic­cat­ed scle­ro­tia. Bac­te­ria can divide asym­met­ri­cal­ly to pro­duce endospores that are extreme­ly resis­tant, includ­ing to heat and antibi­otics. Many pro­tists, unclas­si­fi­able uni­cel­lu­lar eukary­otes that are nei­ther ani­mals, plants nor fun­gi, form cysts. Resis­tant to cold and des­ic­ca­tion, these struc­tures enable many par­a­sitic species to spread. Sim­i­lar­ly, viral par­ti­cles are inert in the exter­nal envi­ron­ment until they encounter a cell to be infected.

Whether this is dor­man­cy or true cryp­to­bio­sis with ces­sa­tion of metab­o­lism (which is not eas­i­ly deter­mined in prac­tice⁶), these aston­ish­ing states can become ver­i­ta­ble time cap­sules, par­tic­u­lar­ly when placed in favourable con­ser­va­tion con­di­tions. Cysts have been brought back to life after spend­ing a hun­dred years in the sed­i­ments of a Swedish fjord⁷ or at the bot­tom of the Baltic Sea⁸. Moss­es have been revived after a thou­sand years in the Antarc­tic per­mafrost⁹. In the Arc­tic, nema­todes that emerged from 30,000 to 40,000-year-old per­mafrost have been revived in the lab­o­ra­to­ry¹⁰, as have partheno­genet­ic rotifers that have been buried for around 24,000 years¹¹. The old­est virus­es that are still infec­tious, tak­en from frozen Siber­ian soil, are giant virus­es that infect amoe­bas and are close to 50,000 years old…

The exis­tence of dif­fer­ent forms of slowed or arrest­ed life has giv­en rise to debate among spe­cial­ists: where does dor­man­cy end and cryp­to­bio­sis begin? Is the lat­ter just an extreme form of the for­mer? Which struc­tures fall into which cat­e­gories? The world around us is in fact a con­tin­u­um, in which it may seem futile to try to dis­tin­guish clear-cut cat­e­gories. And this also applies to the notions of life and death. Whether we favour a def­i­n­i­tion based on func­tions, struc­tures, phys­i­cal chem­istry or phi­los­o­phy, extreme cas­es are valu­able food for thought.

Can we say that micro­scop­ic ani­mals that have sur­vived for tens of thou­sands of years in frozen ground have “lived” there? Did they live for an extreme­ly long time, were they tem­porar­i­ly dead, or did they expe­ri­ence a state that is nei­ther life nor death? These ques­tions seem to be tak­en from works of sci­ence fic­tion, involv­ing long inter­stel­lar jour­neys, but they are being asked by organ­isms that live on our plan­et today. And for the moment, there is no con­sen­sus on how to answer them.