In Memoriam: Krystyna Golińska (1933-2013)

IN MEMORIAM

In Memoriam: Krystyna Goli�nska (1933–2013)Maria Jerka-Dziadosza & Joseph Frankelb

a Department of Cell Biology, M. Nencki Institute of Experimental Biology, 3 Pasteur Str 02-093, Warsaw, Poland

b Department of Biology, University of Iowa, 129 East Jefferson Street, Iowa City, Iowa 52242, USA

KRYSTYNA GOLI�NSKA (Fig. 1) was born on November

30, 1933 in Warsaw (Poland), and she died there on

November 6, 2013. Her whole scientific life was con-

nected to the Nencki Institute of Experimental Biology

(Polish Academy of Science, Warsaw, Poland) where she

started to work in 1954 in the Department of General Biol-

ogy, in a building raised anew in postwar Warsaw under

the directorship of Professor Jan Dembowski. She was

first a technical assistant in the Department, at the same

time carrying out extramural studies in biology at the Uni-

versity of Łod�z. Her master’s degree thesis, completed in

1962 under the supervision of Jan Dembowski, dealt with

behavioral studies on Paramecium rebounding from a

mechanical obstacle (Goli�nska 1963). She then started a

long-lasting cooperation with Dr. Marek Doroszewski

(Head of the Laboratory of Regeneration and Morphogene-

sis of Protozoa: 1961–1974) focused on the excitability,

morphology, morphogenesis, and regeneration of the litos-

tome ciliate Dileptus. She worked on four species: Dilep-

tus cygnus (now Pseudomonilicaryon anser, see Vd’a�cn�yand Foissner 2012), Dileptus anser (Dileptus margaritifer

since 1985, see Wirnsberger et al. 1984), Dileptus vissc-

heri (now Apodileptus visscheri, see Vd’a�cn�y et al. 2011)

and a new species, Dileptus anatinus, that she described

(Goli�nska 1971). She was an expert in using the Pierre de

Fonbrune micromanipulator and in making her own tools

(micro-scalpels and micro-needles) for microsurgery on

single cells.

In 1967 Krystyna earned a Ph.D. degree in biological

sciences under the supervision of Dr. Marek Doroszew-

ski. Her thesis contains studies on the regenerative

potential of cell fragments of “Dileptus cygnus”. Parts of

these data were published in three papers (Goli�nska1965, 1966; Goli�nska and Doroszewski 1964). Her post-

doctoral training in the Laboratory of Prof. Pierre de Puyt-

orac and Dr. Jean Grain at the University of Clermont-

Ferrand (France) resulted in two publications on the ultra-

structure of the same species (Golinska and Grain 1969;

Grain and Golinska 1969) and had a major impact on her

future interests. She became an enthusiastic user of

electron microscopy and passed her knowledge and

experience on to young researchers working on amoebas

and ciliates in her home Department of Cell Biology at

the Nencki Institute. In 1972, she spent her second post-

doc in the Laboratory of Professor Earl D. Hanson at

Wesleyan University in Middletown, Connecticut, USA,

where she investigated the ultrastructure of Paramecium

morphogenesis.

After returning to the Laboratory of Regeneration and

Morphogenesis of Protozoa, Krystyna began her own inde-

pendent studies on the ultrastructure of cytoskeletal com-

ponents of the cell cortex during cell division and

regeneration in Dileptus. The results of her insightful

analyses of the regulation of cortical pattern of ciliary

structures in dileptids were published between 1976 and

1995 in well-recognized international journals such as the

Journal of Cell Science, the Journal of Embryology and

Experimental Morphology (now Development), the Journal

Correspondence

J. Frankel, Department of Biology, University of Iowa, 129 East Jefferson

Street, Iowa City, Iowa 52242, USA

Telephone number: +1 319-335-1110; FAX number: +1 319-335-1069;

e-mail: [email protected]

Figure 1 Krystyna Goli�nska at Pisa: September, 1979.

© 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists

Journal of Eukaryotic Microbiology 2014, 61, 328–332328

Journal of Eukaryotic Microbiology ISSN 1066-5234

Published bythe International Society of ProtistologistsEukaryotic Microbiology

The Journal of

of Protozoology (now the Journal of Eukaryotic Microbiol-

ogy), Protoplasma, and the Wilhelm Roux Archives of

Developmental Biology, in addition to several publications

in Acta Protozoologica (an international journal founded by

the Nencki Institute in 1963). Remarkably, she was the

sole author (11 papers) or the leading author (3 papers) in

studies performed in this period. This whole series of

studies was devoted to one group of ciliate species: the

dileptids—the remarkable carnivorous beasts that when

observed in a depression slide are beautiful and exciting,

waving their mighty probosces armored with toxicysts

while hunting for prey.

Krystyna’s work was recognized in the Nencki Insti-

tute. She earned her “habilitation” in 1981 and become

an associate professor in 1985. She also was a recipient

of two group Scientific Awards granted by the Polish

Academy of Sciences for her contribution to studies on

“Regulation of the pattern of cortical structures in unicel-

lular organisms” (1978) and “Studies on cytoskeleton

plasticity in modified morphogenesis” (1990). Although

she was very reluctant in accepting administrative duties,

she was the Head of the Laboratory of Electron Micros-

copy of the Nencki Institute in 1978/1979, and willingly

took over the duties of the Head of the Laboratory of

Regeneration and Morphogenesis of Protozoa when tem-

porarily replacing the formal Head (1974–2009), Maria

Jerka-Dziadosz, while she was away on sabbatical

leaves. Krystyna was a very loyal, helpful, and caring col-

league and friend to her co-workers and a highly protec-

tive chief for her subordinates. She was a talented artist

in drawings and had a tremendous sense of humor.

(See Fig. 2, showing the two principal organisms studied

from the 1960s into the 1990s in the Laboratory of

Regeneration and Morphogenesis of Protozoa, respec-

tively dileptids by Krystyna and urostylids by Maria

Jerka-Dziadosz.)

Krystyna formally retired in 1995 at the age of 62

because of declining health, and she stopped working

with dileptids after over 40 yr, however regretfully, with-

out summarizing her exciting results in a review paper.

Later on, she did sometimes help out with electron

microscopy of the Tetrahymena cortex, one of the inter-

ests in the laboratory of Janina and Andrzej Kaczanowski

at the University of Warsaw.

In addition to her two post-doctoral periods in France

and the U.S., Krystyna rarely participated in international

meetings and congresses. She was a member of the

Groupement Protistologues de la Langue Franc�aise, and,

being fluent in French, she attended some of their annual

meetings. She also took part in two International Con-

gresses of Protozoology (Warsaw 1981, Nairobi 1985),

one European Congress of Cell Biology (Budapest 1986),

and the European Ciliatology Conferences in Camerino

(1979) and in Aarhus (1987).

Krystyna’s three most important discoveries on dileptids

concerned their capacity for in situ remodeling of oral

structures, their long-term readjustment of body propor-

tions, and their position-dependent transdifferentiation of

specialized ciliary structures.

A basic understanding of each of these major discover-

ies requires a brief introduction to the unique dileptid body

plan. Each cell consists of a thicker trunk surmounted by a

thinner long flexible proboscis. The body surface (in

D. margaritifer) is covered by between 35 and 70 longitu-

dinal somatic ciliary rows (kineties) (Drzewi�nska and

Goli�nska 1987), made up of ciliated single basal bodies

(somatic monokinetids). The cell’s mouth (cytostome) is

located at the base of the proboscis. The oral ciliature

forms a continuous perimeter that includes three distin-

guishable regions: the right and a left paracytostomal kin-

eties that line the two sides of the ventral surface of the

proboscis, and a circumcytostomal kinety that encloses a

cytopharyngeal basket surrounding the cytostome (Golin-

ska 1991; Kink 1976). The circumcytostomal kinety,

although physically connected to the two paracytostomal

kineties, is structurally different: while the paracytostomal

kineties are made up of oral dikinetids each consisting of

one ciliated and one nonciliated basal body, the circumcy-

tostomal kinety consists exclusively of nonciliated single

Figure 2 Dileptus (Krystyna) and Urostyla (Maria). Drawn by Krystyna

Goli�nska in 1972 while carrying out a joint project with Maria

Jerka-Dziadosz on fragment size and capacity for division in Dileptus

“anser”/margaritifer and (Pseudo)urostyla cristata (Goli�nska and

Jerka-Dziadosz 1973).


Journal of Eukaryotic Microbiology 2014, 61, 328–332 329

Jerka-Dziadosz & Frankel Krystyna Goli�nska: In Memoriam

basal bodies (oral monokinetids). This tripartite structure is

normally formed anew in each posterior daughter cell, in

close association with the cell division furrow, through the

formation, rotation, and fusion of fragments derived from

the somatic kineties (Goli�nska 1972, 1995; Vd’a�cn�y and

Foissner 2009).

The first of Krystyna’s major discoveries, accomplished

together with her de facto student Jolanta Kink, was of

the growth and repair of the oral structures of dileptids by

in situ proliferation of basal bodies within the circumcyto-

stomal kinety followed by migration of the new basal

bodies into the two paracytostomal kineties (where they

develop into dikinetids). This was first observed in cells of

(Apo)Dileptus visscheri growing after excystment (Kink

1976) and in cells of “Dileptus cygnus” (now P. anser)

regenerating part or all of the proboscis after its amputa-

tion distal to the circumcytostomal kinety (Goli�nska and

Kink 1976). In subsequent experiments carried out on pro-

boscis fragments of Dileptus “anser”/margaritifer, in

which only the right and left paracytostomal kineties

remained, the ciliated basal bodies of some of the dikinet-

ids near the line of transection were resorbed, thereby

converting these dikinetids into nonciliated monokinetids.

These then served as platforms for the formation of new,

likewise unciliated, basal bodies that then went on to

reconstitute the missing circumcytostomal kinety

(Goli�nska 1978).

Both the capacity for in situ replacement of ciliature of

differentiated ciliary structures and the limitations imposed

on this process are of great comparative interest. All other

ciliates that have been subjected to extensive morphoge-

netic scrutiny can regenerate their complex ciliary struc-

tures (such as oral apparatuses and cirri) only by replacing

them during development and differentiation within new

ciliary primordia, in processes comparable to the morpho-

genesis that takes place during cell division (reviewed in

Frankel 1989). Only the dileptids are known to be able to

carry out in situ repair of fully differentiated structures.

However, even they are subject to the restriction that only

the “simple ciliature”, i.e. monokinetids, have this capacity

for seeding new ciliary units within the oral structures

(Jerka-Dziadosz and Goli�nska 1977).

Recent cladistic analysis has revealed that the presence

of monokinetids in the circumcytostomal kinety is a

“unique, highly derived” state in dileptids (Vd’a�cn�y et al.

2011); their other litostome relatives have oral ciliature

composed exclusively of dikinetids. This raises the possi-

bility that the remarkable morphogenetic flexibility of the

dileptids is itself a derived state, possibly an adaptation for

their dangerous predatory existence.

The second area in which Krystyna has made a major

contribution is in her analysis of the adjustment of body

proportions. Dileptids have two well-delineated major body

regions, trunk and proboscis, which can readily be tran-

sected to produce trunk or proboscis fragments. Further-

more, species of Dileptus sensu stricto, such as Dileptus

“anser”/margaritifer, have more than 200 independent

macronuclei scattered throughout the trunk and base of

the proboscis (Goli�nska 1971; Hayes 1938). This makes it

possible, with some manipulation, to generate fragments

made up of proboscis only that are nucleated and there-

fore are able to reconstruct the entire body (Golinska

1979; Goli�nska 1978).

A detailed analysis of the regulation of proportions of

trunk and proboscis in regenerating Dileptus “anser”/mar-

garitifer was carried out in two studies (Golinska 1979;

Goli�nska and Kink 1977); in the more recent study the

dileptus was forced to regenerate its entire body from all

or part of a proboscis fragment. Two things then hap-

pened very rapidly (i) the entire oral ciliature regenerated

and (ii) new trunk and proboscis regions were rapidly

delineated. However, the initial proportions of proboscis

and trunk varied enormously, with fragments derived from

a whole amputated proboscis giving rise to remodeled

regenerates in which the proboscis was far too long in

relation to the trunk (Golinska 1979). Readjustments sub-

sequently occurred, so that by 24 h after amputation the

relative proportions of trunk and proboscis were similar to

those of the cell prior to sectioning, although their com-

bined lengths often were different (Golinska 1979;

Goli�nska and Kink 1977). Thus, a dual mechanism

appeared to have been at work, a fast one that allowed

the dileptus to hunt again very soon after being deprived

of the majority of its body, and a mysterious slower pro-

cess that eventually restored the normal proportions of

the reconstituted body parts.

The third and perhaps most dramatic discovery was of

the transdetermination of the specialized dorsal ciliature of

Dileptus “anser”/margaritifer following the severing of the

proboscis from the trunk. A portion of the dorsal surface

of the proboscis, called the brosse (“brush”) by French

investigators, is ornamented with 3–5 rows of paired

short, nonmotile cilia. These cilia have swollen shafts that

contain singlet outer microtubules plus central doublets,

but no dynein arms or radial spokes, and distinctive basal

body rootlets (Golinska 1982, 1987). Although a sensory

function is not proven for these cilia, it is extremely likely,

given their lack of motility and unique internal structure,

as well as their partial resemblance to specialized sensory

cilia in metazoans (see references in Golinska 1982 and in

Fisch and Dupuis-Williams 2011).

When the proboscis of Dileptus “anser”/margaritifer

was isolated, some of the sensory cilia of the dorsal pro-

boscis were transformed into locomotor cilia. The sensory

cilia were not resorbed, but instead became converted to

locomotor cilia by an in situ conversion of outer A-micro-

tubule singlets to doublets (by side-assembly of the

B-tubule), formation of dynein arms, compaction and

growth of the axoneme, and restructuring or possible

replacement of the basal body rootlets. Krystyna’s state-

ment that “To my knowledge this represents the first

description of differentiated organelles undergoing trans-

determination” (p. 111 in Golinska 1982) is, to our current

knowledge, still true, at least as it applies to cilia and

flagella. Both this process in itself and its spatial control

should be of strong general interest to cell biologists

working on ciliary organization and development (see the

review of Farnum and Wilsman 2011).



Krystyna Goli�nska: In Memoriam Jerka-Dziadosz & Frankel

When the complementary operation was carried out,

removing the proboscis and leaving behind most of the

trunk, the organism quickly regenerated its oral ciliature

and reconstituted its normal form (Golinska 1991). The

anterior portion of the transected trunk formed a new pro-

boscis, and a region of locomotor cilia was replaced by

sensory cilia. In this case, the locomotor cilia were

resorbed, the remaining naked basal bodies each nucle-

ated the formation of one new basal body (as the sensory

cilia are grouped in pairs), and new sensory cilia shafts

grew out of these basal bodies while the basal body root-

lets were (probably) transformed from the locomotor to

the sensory type (Golinska 1983). In this case, the “trans-

determination” was less dramatic, involving mainly the

basal body, but nonetheless was distinguished from other

known cases of regression and regrowth of cilia by the

fact that “the cilium that regresses is of a different type

from the one that grows out again” (p. 472 in Golinska

1983).

All three of these remarkable and up to now under-

appreciated discoveries reveal an organism that has

evolved an amazing level of developmental flexibility,

exceeding that of any other ciliate known to us. Krystyna’s

persistent reliance on the combination of microsurgery

and transmission electron microscopy as her principal

mode of investigation has facilitated, indeed has been

essential for, the discovery of this multifaceted develop-

mental flexibility of her experimental organisms, the dilept-

ids, while undoubtedly reducing her “productivity” as

measured in number of publications (a complete list of her

publications can be found in Additional References S1).

She also worked within an older tradition that made it

impossible for young investigators, who did not yet have a

“habilitation”, to formally mentor graduate students.

Owing partially to this situation and partially to her working

methods, Krystyna did not develop a “school” that could

carry forward the investigation of dileptids as new “cell

regeneration models.” However, the Dileptida have

aroused recent interest among ciliate systematists, and

we hope that Dileptus will also be taken up anew by cell

biologists who might follow up on Krystyna’s discoveries

with further ultrastructural, molecular, and genetic investi-

gations of this fascinating, voracious ciliate.

ACKNOWLEDGMENTS

The authors thank Drs Anne W.K. Frankel, Jacek Gaertig,

Denis H. Lynn, and Dorota Włoga for their helpful com-

ments on the manuscript.

LITERATURE CITED

Drzewi�nska, J. & Goli�nska, K. 1987. Relationship between the

size of cell and the number of its ciliary rows in the ciliate

Dileptus. Acta Protozool., 26(1):19–30.Farnum, C. E. & Wilsman, N. J. 2011. Axonemal positioning orien-

tation in three-dimensional space for primary cilia: what is

known, what is assumed, and what needs clarification. Dev.

Dynamics, 240(11):2405–2431.

Fisch, C. & Dupuis-Williams, O. 2011. Ultrastructure of cilia and

flagella – back to the future! Biol. Cell, 103(6):249–270.Frankel, J. 1989. Pattern Formation: Ciliate Studies and Models.

Oxford University Press, New York, NY. 314 p.

Goli�nska, K. 1963. Experimental study on rebounding from

mechanical obstacle in Paramecium caudatum. Acta Protozool.,

1(13):113–120.Goli�nska, K. 1965. Macronucleus in Dileptus cygnus and its

changes in division. Acta Protozool., 3(13):143–151.Goli�nska, K. 1966. Regeneration of anuclear fragments in Dileptus

cygnus Clap. et Lachm. Acta Protozool., 4(5):41–49.Goli�nska, K. 1971. Comparative studies on the morphology of

Dileptus anatinus sp. n. (Holotricha, Gymnostomata). Acta

Protozool., 8(29):367–377.Goli�nska, K. 1972. Studies on stomatogenesis in Dileptus (Ciliata,

Holotricha) in the course of division processes. Acta Protozool.,

9(18):285–297.Goli�nska, K. 1978. The course of in situ remodeling of injured

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the

online version of this article:

Additional References S1. A complete listing of Krystyna

Goli�nska’s publications. All issues of Acta Protozoologica

are available online at http://www.rcin.org.pl/dlibra/publica-

tion/2622.



Krystyna Goli�nska: In Memoriam Jerka-Dziadosz & Frankel

In Memoriam: Krystyna Golińska (1933-2013)

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