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Hyperprolinemic Larvae of the Drosophilid Fly, Chymomyza Costata, Survive Cryopreservation in Liquid Nitrogen

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Hyperprolinemic Larvae of the Drosophilid Fly, Chymomyza Costata, Survive Cryopreservation in Liquid Nitrogen Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen Vladimír Koštála,b,1, Helena Zahradníčkováa, and Petr Šimeka aInstitute of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic; and bFaculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved June 30, 2011 (received for review May 3, 2011) The larva of the drosophilid fly, Chymomyza costata, is probably phospholipids that pair palmitic and linoleic fatty acids in cell the most complex metazoan organism that can survive submer- membranes (10), which may contribute to the preservation of gence in liquid nitrogen (−196 °C) in a fully hydrated state. We protein and membrane structures at low temperatures (11, 12). examined the associations between the physiological and bio- In this paper, we examined the associations between physiolo- chemical parameters of differently acclimated larvae and their gical and biochemical parameters of differently acclimated larvae freeze tolerance. Entering diapause is an essential and sufficient of C. costata and their freeze tolerance; i.e., the ability to survive prerequisite for attaining high levels of survival in liquid nitrogen when frozen at −32 °C and subsequent submersion in liquid N2. (23% survival to adult stage), although cold acclimation further We showed that larvae acquire high freeze tolerance without cold improves this capacity (62% survival). Profiling of 61 different acclimation during their transition to diapause at a relatively high metabolites identified proline as a prominent compound whose temperature of 18 °C, although their freeze tolerance is further concentration increased from 20 to 147 mM during diapause tran- improved by cold acclimation. Metabolomic profiling of 61 dif- sition and subsequent cold acclimation. This study provides direct ferent compounds identified proline as a prominent metabolite, evidence for the essential role of proline in high freeze tolerance. as the increase in the molar concentration of proline explains SCIENCES We increased the levels of proline in the larval tissues by feeding most of the change in the overall osmolality of body fluids during larvae proline-augmented diets and found that this simple treat- APPLIED BIOLOGICAL ment dramatically improved their freeze tolerance. Cell and tissue diapause transition and cold acclimation. Next, we artificially survival following exposure to liquid nitrogen was evident in pro- elevated proline concentrations in larval tissues by feeding the line-fed nondiapause larvae, and survival to adult stage increased larvae diets augmented with proline, which resulted in a signifi- from 0% to 36% in proline-fed diapause-destined larvae. A signif- cant improvement of larval freeze tolerance. On the basis of icant statistical correlation was found between the whole-body the results of differential scanning calorimetry (DSC), we suggest concentration of proline, either natural or artificial, and survival that high proline levels, and relatively low content of osmotically to the adult stage in liquid nitrogen for diapause larvae. Differen- active water resulting from the freeze dehydration process during tial scanning calorimetry analysis suggested that high proline slow cooling to −32 °C, increased the propensity of unfrozen levels, in combination with a relatively low content of osmotically water to undergo glass-like transition (vitrification), which prob- active water and freeze dehydration, increased the propensity of ably contributed to high larval survival in liquid N2. the remaining unfrozen water to undergo a glass-like transition (vitrification) and thus facilitated the prevention of cryoinjury. Results and Discussion Larvae Acquire a High Freeze Tolerance with Entrance to Diapause, insect freeze tolerance ∣ cold hardiness ∣ glass transition ∣ metabolomics which is Further Improved by Cold Acclimation. In our experiments, nondiapause larvae of C. costata (variant 1) showed no ability to emperate and polar insects overwinter at subzero body survive in a frozen state at −32 °C or in liquid N2. No signs of Ttemperatures (1–3), which makes them suitable models for cellular or tissue survival were recorded 12 h after melting. Dia- studying the principles of survival in animal cells, tissues, and pause-destined larvae (variant 2) showed relatively high survival complex organisms at cryothermic conditions. The drosophilid at the cellular and larval levels but were not able to pupariate and fly, Chymomyza costata (Zetterstedt) (Diptera: Drosophilidae), metamorphose to adult flies. High survival into the adult stage appears to be a highly promising model. It is distributed over was observed in the diapause, warm-acclimated larvae (variant 3), a cool-temperate, Holarctic area (4) and fully grown third instar and this was further improved by cold acclimation (variant 4) larvae enter facultative winter diapause in response to long night (Fig. 1 A and B). These results verify previous reports (7–9) and length and/or low temperature (5). Diapause larvae supercool extend their findings by showing that cold acclimation does not to between −15 °C and −25 °C (6) but can survive freezing to appear to be an essential prerequisite for attaining high freeze −100 °C provided they undergo cold acclimation (1 mo at 4 °C), tolerance. We found that reaching the appropriate stage of dia- are inoculated by external ice at −2 °C, and are cooled at a slow rate of 0.1 °C∕ min (7, 8). Diapause, cold-acclimated larvae of pause development [i.e., transition from initiation to mainte- C. costata were successfully cryopreserved at the temperature nance phase (5, 13)], at a constant high temperature of 18 °C is of liquid nitrogen (N2)(−196 °C) for 1 h (9). To our knowledge, sufficient for the development of high freeze tolerance. larva of C. costata represents the most complex metazoan organ- ism that has reportedly survived after submergence in liquid N2 Author contributions: V.K. designed research; V.K. and H.Z. performed research; P.S. in a fully hydrated state. Physiological mechanisms underlying contributed new reagents/analytic tools; V.K. and P.S. analyzed data; and V.K. wrote this unique capacity remain poorly understood. Inoculative freez- the paper. ing and a slow cooling rate allow time for osmotic equilibration The authors declare no conflict of interest. during extracellular freezing and prevent formation of intracellu- This article is a PNAS Direct Submission. lar ice crystals (9). The process of cold acclimation involves 1To whom correspondence should be addressed. E-mail: [email protected]. remarkable biochemical changes such as the accumulation of pro- This article contains supporting information online at www.pnas.org/lookup/suppl/ line and trehalose (8) and the increase in relative proportions of doi:10.1073/pnas.1107060108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1107060108 PNAS Early Edition ∣ 1of6 Downloaded by guest on September 30, 2021 Fig. 1. Survival of differently acclimated larvae of Chymomyza costata (A)at−32 °C or (B) in liquid N2. The total heights of columns depict survival at the cellular level. Proportions of larval, pupal, and adult survivors (of the total) are depicted using different column-filling styles, as specified. The acclimation treatments were: 1, nondiapause, warm-acclimated larvae; 2, diapause-destined, warm-acclimated larvae; 3, diapause, warm-acclimated larvae; and 4, dia- pause, cold-acclimated larvae. Total numbers of larvae (n) in each experiment are given in parentheses. (C) Fat body tissue photographed under a Zeiss Axioplan 2 fluorescence microscope. Upper row: control larvae, not exposed to freezing temperatures: (Left) no staining, (Center) DAPI, (Right) Nile red. Lower row: larvae exposed to liquid N2 were stained with (Left) DAPI, (Center) Nile red, and (Right) trypan blue during recovery. The scale bar is 100 μm in all photographs. Control larvae (not exposed to freezing temperatures) were C. costata is no exception to this scenario (7–9), in which decreas- negative for trypan blue staining and exhibited numerous small ing the amount of unfrozen (OA) water diminishes the amount of lipid droplets in fat body cells (Fig. 1C, upper row). In contrast, ice formed at any given temperature and, consequently, reduces all recovering larvae after freezing treatments, irrespective of the freeze concentration of intracellular fluids below potentially temperature and acclimation variant, displayed massive coales- damaging levels (26–28). cence of lipid droplets in fat body cells. Small lipid droplets The survival capacity of C. costata larvae, however, goes merged and formed a few large droplets or a single lipid droplet beyond the ecological limits of freeze tolerance. After being (Fig. 1C, lower row). Trypan blue staining was observed in ap- slowly frozen to −32 °C, these larvae can survive plunging in proximately 10–30% of fat body cells 12 h after melting irrespec- liquid N2. Fig. 2B is a cryo-SEM micrograph of one such larva tive of temperature and acclimation variant. The large lipid (note that the larva shows no signs of body water loss). Fig. S1 droplets and islands of damaged fat body tissue persisted shows cryofractured larvae with dehydrated tissues surrounded throughout the rest of larval life and were also observed during by a mass of frozen extracellular
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