The Charms of Cold

by Elio

Fig­ure 1. Scan­ning elec­tron mi­cro­scope im­age of Chry­seo­bacterium green­lan­den­sis found in a Green­land glac­ier. (Credit: Jen­nifer Love­land-Curtze, Penn State). Source. Front­page: Scan­ning elec­tron mi­cro­scope of Planococ­cus halo­cryophilus cells grown at −15°C in 18% NaCl and 7% glyc­erol, en­crusted in dense nodu­lar mate­rial. Source

The up­com­ing "pro­tein spot­light" #209 by Vivi­enne Bail­lie Ger­rit­sen on ice-bind­ing pro­teins brings up the near ma­gic things that hap­pen to mi­crobes in the cold. At a time when our worry is global warm­ing, it may be good to con­sider that some bac­te­ria do not shun cold habi­tat and thrive in such un­in­hab­it­able-sound­ing places as the per­ma­frost, po­lar ice, glac­i­ers, snow­fields, and cold deep ocean wa­ters. Of course, these places are be­ing se­verely af­fected by the change in cli­mate. But for now, even a par­tial list of what mi­crobes do in the cold is im­pres­sive.

• Fish, in­sects, plants, and above all mi­crobes can thrive in ex­tremely cold cli­mates and make use of a va­ri­ety of strate­gies to over­come such harsh condi­tions. Cer­tain fish re­sist sub-freez­ing tem­per­a­tures by mak­ing pro­teins that serve as an­tifreeze. This low­ers fishes' freez­ing point by about 1°C. Us­ing such an­tifreeze pro­teins, in­sects and plants can do even bet­ter than that, but it is mi­crobes that win the prize.
   
• Bac­te­ria and ar­chaea are said to sur­vive in ice for 50 mil­lion years, that is, are able to grow af­ter thaw­ing. Not un­ex­pect­edly, the data be­come more cred­i­ble the more re­cent the time of their frozen per­me­ance. A re­li­able da­tum is that they sur­vived frozen for 750,000 years in ice sam­ples from West­ern China. Mi­cro­bial ac­tiv­ity has been mea­sured in soils frozen be­low −39°C.
   
• Bac­te­ria in ice can re­pair their DNA. One would ex­pect that bac­te­ria liv­ing un­der such harsh con­di­tions should have ac­tive mech­a­nisms to re­pair dam­age to their DNA, and this has in fact been re­ported for vi­able bac­te­ria frozen in ice for 500,000 years. The au­thors pro­pose that the ac­tive me­tab­o­lism need to sus­tain such ac­tiv­ity is also present. For a dis­cus­sion of this is­sue in these pages, see here.
   
• Bac­te­ria sur­vive tem­per­a­tures near the ab­solute zero as long as ice crys­tal for­ma­tion is pre­vented, as when they are plunged into liq­uid ethane in prepa­ra­tion for elec­tron cryo­to­mo­graphy (Cry­oET). It is said that bac­te­ria frozen this way swim away hap­pily when thawed.
   

Fig­ure 2. Phase con­trast mi­cro­graph of Psychro­monas in­gra­hamii. Bar 1 µm. Source

• The word cham­pion bac­terium for growth at a low tem­per­a­ture ap­pears to be Psy­chromonas ingra­ha­mii, which can grow at −12°C with a gen­er­a­tion time in the lab of 240 h (Fig­ure 2). It is named af­ter my buddy from way back, John In­gra­ham, for his contri­butions to 'cold mi­cro­bi­ol­ogy'. These in­clude the first charac­te­ri­za­tion of cold-sen­si­tive mu­tants in es­sen­tial func­tions. ('buddy' refers, among other things to hav­ing jointly au­thored four books, to­gether with the late Fred Nei­d­hardt.) Chal­leng­ing the long-time cham­pion is now a Fir­mi­cutes bac­terium, Planococ­cus halocryophilus, which grows at −18°C and is still meta­bol­i­cally ac­tive at −25°C in its nat­ural habi­tat, Arc­tic per­mafrost (see front­page).
   
• Some bac­te­ria from Antarc­tic lakes cling to the un­der­side of the ice. They do this via a se­cre­ted long pro­tein thread rem­i­nis­cent of a pilus, but one that is much thin­ner than a reg­u­lar pilus. Yet, like many pili, it has an ad­he­sive end that does the ac­tual bind­ing. It is made by the Antarc­tic bac­terium, Mari­nomonas primoryen­sis. Now, you ask, why would bac­te­ria want to cling to ice? The rea­son prof­fered is that the un­der­neath of ice floes is a good a place for bac­teria to grow in seem­ingly in­hos­pitable places. Just un­der­neath the ice is a re­gion with higher con­cen­tra­tion of oxy­gen and nu­tri­ents, and more light. In the Antarc­tic lakes that are perma­nently cov­ered with ice (see a re­cent post), these re­gions are an ideal habi­tat for strictly aero­bic or­gan­ism such as M. pri­moryen­sis.

Re­lated: lis­ten to this episode of Meet the Mi­cro­bi­ol­o­gist (an ASM pod­cast) where Chris­tine Fore­man, Asso­ci­ate Pro­fes­sor, Mon­tana State Uni­ver­sity, ex­plains how mi­crobes can sur­vive and grow on glac­i­ers, and what we can learn from mi­crobes in glac­ier ice cores.