How Do Tardi­grades With­stand Dry­ing?

by Elio

Re­cently, tardi­grades or wa­ter bears made the news be­cause they had been loaded on a space cap­sule headed for the moon. Alas, the space­craft crashed on its way down and the fate of the ti­ny pas­sen­gers is un­known. This gives us a rea­son for re­vis­it­ing these fas­ci­nat­ing crea­tures and to bring the topic up to date. They have been in­tro­duced here in a fine ar­ti­cle by Christoph. For a re­view, see here (Open Ac­cess).

These small an­i­mals (they are about ¼ to ½ mil­lime­ters in length) are re­mark­able for their abil­ity to with­stand dry­ing, ex­treme heat and cold, and even some ion­iz­ing ra­di­a­tion. Their abil­ity to sur­vive in a dry state makes them es­pe­cially suit­able for space travel. They can go with­out wa­ter for years on end and hap­pily swim away once wa­ter is pro­vided. What mech­a­nisms are in­volved has been sub­ject of spec­u­la­tion and in­ves­ti­ga­tion for over 250 years. In some species, a dis­ac­cha­ride called tre­halose, known to be es­sen­tial for with­stand­ing dry­ing in some other or­gan­isms has been im­pli­cated here too. How­ever, some species of tardi­grades lack this com­pound, so the search for other com­pounds has been on. In a de­tailed study, Boothby and col­lab­o­ra­tors re­ported that a class of pro­teins known as 'Tardi­grade In­trin­si­cally Dis­or­dered pro­teins' (TDPs) be­come en­riched in the des­ic­ca­tion process and are re­quired for sur­vival.

A Pub­lished data on the sur­vival ver­sus rel­a­tive humi­dity for Hypsi­bius du­jar­dini (red), Parama­cro­biotus richtersi (green), and Mil­ne­sium tardi­gradum (black). Ani­mals des­ic­cated at lower re­la­tive humi­dity experi­ence in­creased rates of dry­ing com­pared with those des­ic­cated at hig­her rel­a­tive hu­mid­ity. B Sur­vival of H. du­jar­dini af­ter slow dry­ing (95% rel­a­tive hu­mid­ity), quick dry­ing (70% RH), and slow fol­lowed by quick dry­ing. C MA plot show­ing en­richment (log2-fold change) ver­sus ab­undance (log2 CPM) of ex­pressed H. du­jar­dini genes un­der hy­drated and dry con­di­tions. Col­ored cir­cles in­di­cate CAHS (red), SAHS (blue), and MAHS (green) ge­nes en­cod­ing tardi­grade-spe­cific IDPs. Source. Fron­tispiece: Acti­nar­c­tus do­rypho­rus (ma­r­ine tardi­gra­de) aut­o­flu­o­res­cence of cu­ti­cle. Magn. 40×. Im­age by A. Schmidt-Rhaesa C. Schulze, R. Neves. Source

TDPs are ex­pressed con­sti­tu­tively at high lev­els in many species of tardi­grades. These pro­teins vit­rify (be­come glass-like) upon dry­ing, which may ex­plain their protec­tive abil­ity, as vit­ri­fi­ca­tion keeps harm­ful ice nee­dles from form­ing. What are in­trin­si­cally dis­or­dered pro­teins? Un­like the typ­i­cal glob­u­lar pro­teins, these have no per­sis­tent ter­tiary struc­ture but es­sen­tially flop around in the en­vi­ronment.

Sev­eral facts speak in fa­vor of the role of these pro­teins in sur­viv­ing dry­ing. Thus, tardi­grades up­reg­u­late the ex­pression of TDP genes in re­sponse to dry­ing. Sure enough, tran­scrip­tion and trans­la­tion are re­quired for sur­vival. Tol­er­ance to dry­ing di­min­ishes when TDP genes are dis­rupted (us­ing RNAi) In ad­di­tion, het­erol­o­gous ex­pression of TDP genes in sev­eral prokary­otic and eukar­yotic cells (E. coli, yeast, and hu­man cells in cul­ture) in­creases their tol­er­ance to dry­ing. Con­vinc­ing, no?

One of the most telling find­ings has been that tardigra­des that are dried rapidly die faster than when dried slowly, sug­gest­ing that a pro­tec­tive sub­stance needs to be made in or­der to al­low pro­tec­tion. Boothby and col­laborators an­a­lyzed the gene ex­pres­sion in the transcrip­tomes of slowly dried spec­i­mens and con­trols, find­ing that 11 of 17 cy­toso­lic abun­dant heat sol­u­ble (CAHS) pro­tein tran­scripts were en­riched 4- to 22-fold dur­ing des­ic­ca­tion. Three gene fam­i­lies, CAHS, SAHS, and MAHS, had been pre­vi­ously iden­ti­fied in a pro­teomic analy­sis of tardi­grades by Ya­m­aguchi et al. in 2012 and Tanaka et al. in 2015. That IDPs lack per­sis­tent sec­ondary struc­ture was con­firmed us­ing nu­clear mag­netic res­o­nance spec­troscopy (NMR) heat sol­u­bil­ity ex­per­i­ments, cir­cu­lar di­chroism spec­tropo­larime­try, and a tech­nique called back­bone pro­ton-deu­terium ex­change. So, there is now good ev­i­dence for role of this spe­cial class of pro­teins in pro­tec­tion from des­ic­ca­tion.

The au­thors say: 'We an­tic­i­pate that these find­ings will build a foun­da­tion for pur­su­ing long-term goals of the des­ic­ca­tion tol­er­ance field, in­clud­ing the en­gi­neer­ing of des­ic­ca­tion-tol­er­ant crops and the de­vel­op­ment of techno­logies for the dry preser­va­tion of phar­ma­ceu­ti­cals, cells, and tis­sues.' It may seems a bit star­tling that the study of such lowly lit­tle an­i­mals has con­tributed to our un­der­stand­ing of such ba­sic bi­o­log­i­cal at­trib­utes as pro­tein struc­ture. But mi­cro­bi­ol­o­gists are used to that.

To re­turn for a mo­ment to the lu­nar tardi­grades, it is of course un­known if they sur­vived, as their site won't be re­vis­ited for quite some time. If shielded from ra­di­a­tion by space craft de­bris, they might with­stand the con­di­tions of dry­ing and ex­tremes of tem­per­a­ture. For those of us con­cerned with is­sues of cos­mic pol­lu­tion, the NASA Of­fice of Plan­e­tary Pro­tec­tion lim­its its con­cerns to the con­tamination of sites that may con­ceiv­ably har­bor life, the moon not be­ing one of them (sure enough, on its sur­face there are bags con­tain­ing pounds of hu­man fe­ces). Yet we must be thank­ful to the tardi­grades for re­mind­ing us of the grav­ity of such is­sues in space ex­plo­ration.

 

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