The Isolation, Characterization, and Identification of the Crystalline Inclusions of the Large Free-Living Amebae*

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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central The Isolation, Characterization, and Identification of the Crystalline Inclusions of the Large Free-Living Amebae* By JOE L. GRIFFIN,:~ Ph.D. (From the Department of Biology, Princeton University) PLATES 115 TO 117 (Received for publication, June 25, 1959) ABSTRACT Amoeba proteus, Amoeba dubia, and Chaos chaos all contain similar plate-like and bipyramidal cytoplasmic crystals. Isolated crystals, purified by recrystalliza- tion from water, yield plate-like crystals which have been shown to be identical with synthesized carbonyl diurea (triuret) with regard to physicochemical proper- ties, elemental analysis, x-ray diffraction patterns, infrared spectra, and optical properties. The birefringent plates found in the cytoplasm are carbonyl diurea. While the exact composition of the isotropic plates and of the bipyramids is not clear at present, the major constituent of these crystal types is also carbonyl diurea. It is suggested that carbonyl diurea is a nitrogen excretion product, not previously found in living organisms, and probably represents an end product of purine metabolism in amebic. INTRODUCTION proteus), Trichamoeba villosa, and Cochlipodium bilimbosum were similar, but differed as a group Crystalline inclusions are found in the cytoplasm from those of Mayorella sp. and other protozoa of most of the large free-living amebae. These which he studied. A recent study by Grunbaum, crystals are particularly apparent in the carnivo- Max M¢ller, and Thomas (9) will be discussed rous amebae, Amoeba proteus, Amoeba dubia, and more fully below. Chaos chaos, while the lack of crystals is one of Until recently (14, 15) the culture methods for several characteristics that distinguish the herbiv- amebic were not sufficiently productive to allow orous ameba, Pelomyxa palustris, from the species isolation and purification of the crystalline ma- above (10). Many speculations have been made as terial. The need for relatively large quantities of to the chemical nature of the crystals and as to material led the author, before undertaking the their function in the cytoplasm. Most authors present work, to develop controlled mass culture have considered them to be either food reserves or methods that would be suitable for the sustained excretory products (of. 2, 3, 5, ll, 12, 16, 18). production of very large populations of amebae Mast and Doyle (12) suggested, on insufficient (7, 8). evidence, that the plate-like and bipyramidal crystals found in Amoeba proteus were leucine and Materials and Methods a magnesium salt of glycine respectively. Bern- In the present investigation, crystals from the three heimer (4) studied the refractive index, melting species, Amoeba proteus, Amoeba dubia, and Chaos point, and solubility properties of bipyramidal chaos (Chaos carolinensis, Pdomyxa carolinensis) have crystals from various ameba species. He demon- been compared. The amebae were grown on Tetrahy- strated that the crystals of Chaos di.l~tuem (A. mena by improved mass culture methods, described in (7) and (8). The strains used, PROT 1, PROT 4, DUB * This study was aided in part by a Research Grant 1, and CH 1, are described more fully there. Isolation (C-3022-C1 and 2) from the National Cancer Institute of the crystalline inclusions was carried out in the National Institutes of Health, administered by Dr. following manner. The anaebae were concentrated by R. D. Allen. centrifugation and small pellets were frozen with dry :~ Present address: Department of Biology, Brown ice and acetone and lyophilized in a high vacuum University, Providence, Rhode Island. system at room temperature. The dried material was 227 J. BtopiiYsic. AND BIOCIIEM. CYTOL., 1960, VOI. 7, No. 2 228 IDENTIFICATION OF AMEBA CRYSTALS dispersed by grinding in dim-butyl phthalate with an ratios of crystal types in the cytoplasm are listed agate mortar and pestle. When microscopic examina- below for the three species. (See also Figs. 1 to 3). tion showed that most of the crystals were free from attached cytoplasm, the dispersed material was centri- Approximate fuged in carbon tetrachloride. This solvent is inter- Bipyra- Plates ratio Bipyra- mids mediate in density between the heavier crystals and mids/Plates the lighter cytoplasm. The supernatant was then poured off and the heavy material washed 3 times #t with carbon tetrachloride. The cytoplasmic material 1. A. dubia .......... 10 3O 2/l floating in the supernatant was again dispersed and 2. A. proteus ......... 5 3 5/1 centrifuged to obtain remaining crystals. Crystals 3. C. chaos .......... 3 2 5/1 prepared by the above technique are contaminated with small amounts of cytoplasmic material (protein, While some of the crystals are contained in vacu- nucleic acid, etc.). However, such amorphous material oles, careful observations on uncompressed cells does not interfere with petrographic or x-ray diffraction with bright field, phase contrast, and television analysis (see Figs. 5 and 8), and comparative studies of the crystals from the three species were made using microscopes indicated that many crystals have no such preparations. visible surrounding membrane. Care must be taken The crystalline material was further purified for in such observation since compression can cause chemical studies. Since, as will be shown later, the vacuoles to appear around crystals (cf. 1). material is the same in the three species, crystals from A. proteus were used for this purpose. This species Optical Crystallography: grows rapidly and contains more crystals than A. dubia The bipyramidal crystals from all three species or C. chaos. The crude preparation described above was are isotropic, have similar shapes, and show re- placed in a dialysis sack with a small amount of water fractive indices of 1.638 to 1.642. By contrast, most and dialysed for a few hours at 60 to 70° C. against a relatively large volume of distilled water. The dissolved of the plates in A. dubia are highly birefringent. crystalline material passed through the dialysis mem- The refractive indices were >1.72 and <1.52. brane and was recovered when the external volume of When the plates were tilted, the spread of re- water was concentrated by boiling under reduced fractive indices was even higher so that precise pressure. After macromolecules had been removed from values could not be obtained. Many of these plates the preparation in this way, the material was further showed a characteristic twinning pattern, which purified by recrystallizing 3 times from minimal volumes proved to be a useful diagnostic feature. Some of boiling water. "Millipore filters" (HA) were used plates, however, were not twinned, and others were throughout. The yield of recrystallized material (8 to apparently isotropic (See Fig. 5). The plates found 12 rag./350 mg. dry amebae) was vacuum-dried and in A. proteus and C. chaos were small and ap- used as an analytical sample. parently very thin. An extensive search, however, Since the crystals are small, immersion refractometry with a phase contrast microscope was used for deter- revealed some plates that were birefringent. mining refractive index rather than the Beck~ line When A. proteus crystals (mostly isotropic bi- technique. When a rotatable polaroid was introduced pyramids) were put in solution, they recrystallized above the phase condensor, the refractive index could as birefringent plates identical in optical proper- be determined for a single crystallographic direction in ties with the plates found in A. dubia. The two the birefringent crystals. compared closely in the spread of refractive in- dices, external morphology (when carefully re- RESULTS crystallized), and characteristic twinning pattern (See Figs. 5 and 6). Large crystals (0.2 to 1.0 mm.) Observations on Living Cells: of this material could be formed by slow cooling The number of crystals per cell generally ap- (Fig. 4). When examined petrographically, they peared to increase when amebae were transferred proved to be uniaxial, negative, and probably of from "stock" infusion cultures to cultures fed on hexagonal symmetry. The most prominent Tetrahymena. Two morphologically distinct types deavage plane forms an angle of 45 ° with the c of crystals are found in the three species: bipy- axis. The flat surfaces of the birefringent plates ramidal crystals, often truncated, and thin square are oriented parallel to this cleavage plane, which or rectangular plates. The long dimension of the explains the higher spread of refractive indices of largest crystals usually found and the approximate such plates when they are tilted. JOE L. GRIFFIN 229 X-ray Crystallography: fringence and retardation) and would be expected The x-ray diffraction patterns of concentrated to give comparatively weak bands. With the ex- crystal preparations were found to be the same for ception of a few weak lines in the A. dubia pattern, all three species (See Figs, 9 and 10 for patterns the diffraction patterns of the naturally occurring from A. dubia and A. proteus and Table I for d- crystals seem to be due to the bipyramidal crys- spacings). The recrystallized material exhibited a tals. It can be seen from the number of bands pres- pattern different from that of the naturally oc- ent and their spacing that the crystal symmetry is curring crystals (compare Figs. 10 and 11). In not cubic and is probably of a higher order of the isolated crystal preparations washed in carbon symmetry, even though the bipyramidal crystals tetrachloride, bipyramidal crystals were close to appear to be isotropic. the ideal size and thickness for x-ray powder photo- Physicochemical Properties: graphs (3 to 5 #). The plates, however, were less than 0.4 # thick even in A. dubia (computed from Several properties of the recrystallized material independent direct measurements of both bire- obtained from A. proteus were investigated. Visible and Ultraviolet Absorption Spectra.--By TABLE I heating aqueous solutions it was possible to analyze d-Spacings Calculated from X-ray Diffraction concentrations of approximately 10 rag./100 ml.
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