Robert Lauterborn (1869—1952) and His Paulinella Chromatophora

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Protist, Vol. 156, 253—262, August 2005 http://www.elsevier.de/protis Published online date 11 July 2005

FROM THE ARCHIVES

Robert Lauterborn (1869—1952) and his Paulinella chromatophora

Michael Melkoniana,1and Dieter Mollenhauerb aBotanisches Institut, Lehrstuhl I, Universita¨ tzuKo¨ ln, Gyrhofstr. 15, 50931 Ko¨ ln, Germany bForschungsinstitut Senckenberg, Frankfurt am Main, Forschungsstation fu¨ r Mittelgebirge, Lochmu¨ hle 2, 63599 Biebergemu¨ nd, Germany

In 1895, in his second, short contribution about among the most interesting representatives of its protozoa (Protozoenstudien II.), Robert Lauter- division in freshwater.’’ ? born, then at the Zoology Department of the In the second half of the 19th century the socio- University of Heidelberg, described a novel organ- economic situation in Germany (i.e. urbanization, ism (nov. gen. et nov. spec.) which he named industrialization and the rise of an urban proletar- Paulinella chromatophora. He must have been iat) led to pronounced and lasting environmental very exited about his discovery which he made on changes (e.g. degradation of soil and natural Christmas Eve 1894, since he clearly recognized waters, epidemic human diseases, plant diseases, the importance of his observations for symbiosis decline of forests). The Janus face of prosperity research and biology, in general. And although his were difficulties of supply, lack of hygiene in Paulinella featured only occasionally in scientific settlements, and various kinds of diseases. publications during the next 100 years, it now Gradually, questions were raised which today are appears to be taking center stage in discussions known as problems of waste disposal. Careful about the endosymbiotic origin of plastids (some observers such as Ferdinand Cohn (1828—1898) recent reviews in this field that mention Paulinella had early recognized the problems and with the include Bhattacharya et al. 2003; Delwiche 1999; methods then available initiated simple environ- Keeling 2004; McFadden 2001). Who was the mental monitoring systems (Cohn 1853; Kolkwitz discoverer, what characterized his time, socio- and Marsson 1908; Mez 1898). Jo¨ rg Lange, economically and scientifically, and finally what Gu¨ nther Leps (1934—2000; bibliography in Jahn did Lauterborn discover about Paulinella chroma- 2001), Thomas Potthast and Astrid E. Schwarz tophora that made him write (in the first sentence have described the circumstances of the ‘‘Wilhel- of his publication, p. 36; translated from German) minian’’ epoch and the early period of the ‘‘Among the many protozoa that populate the ‘‘republic of Weimar’’ and their influence on the extensive diatom mats of the Altrhein near development of science in Germany (Lange 1990, Neuhofen (about 6 km south of Ludwigshafen on 1994; Leps 1998; Potthast 2001; Schwarz 2001). Rhine, Germany) during the cold season, I found, The economic boom came after the German on December 24 last year, a new rhizopod, that in French war and finally led to overheating during more than one respect can demand to be ranked the Gru¨nderzeit (‘‘founder period’’; 1871—1873) and in consequence to many bankruptcies. During such phases of prosperity interest is initially focused on the requirements for economic 1Corresponding author; fax +49 221 470 5181 growth: production and delivery of food and e-mail [email protected] (M. Melkonian) raw materials. Concomitantly, the older ‘‘humus

254 M. Melkonian and D. Mollenhauer theory’’ of Albrecht Thaer (1752—1828; Fo¨ rderge- ever, Bu¨ tschli fell ill during the time when sellschaft Albrecht Daniel Thaer e.V. Mo¨ glin 2004) Thienemann was there and could not give was superseded by the modern concept of the lectures. This brought Thienemann closer to the mineral nutrition of plants by Justus von Liebig junior lecturer (Privatdozent) Robert Lauterborn (1803—1873). The victory of this concept and the (1869—1952). The meeting between the 21-year first successes of the production-oriented view old zoology student from Thuringia and the 34- diverted attention from the problem of waste year old lecturer from the Palatinate was fateful. disposal that usually seems to be of less im- August Thienemann in his research has always portance to the public. However, the above- dealt with both the fruitful suggestions as well as mentioned problems leading to increasing waste the pitfalls that ‘‘holism’’ held for biology. He landfills and the omnipresent wastewater, made it placed his life under the motto Schau auf zu den the more important to try to better understand the Sternen, hab acht auf die Gassen (‘‘look up to the decomposition process (today known as recy- stars, pay attention to the alleys’’). This phrase cling). Wastewater treatment using artificial wet- was introduced by the lower-saxon poet and lands and trickling filters was introduced during writer Wilhelm Raabe (1831—1910), whom Thie- this time (see Kolkwitz 1922). nemann valued highly (see Thienemann 1949). The scientific study of aquatic ecosystems had Raabe had dealt with environmental issues in his just been initiated. Franc-ois Alphonse Forel lesser known novel Pfisters Mu¨hle (Raabe 1970 (1841—1912) in Geneva had introduced the term [originally 1884]), not casually or in a general way limnology (the science of inland waters; Forel but specifically using records from a publicly 1882); many new ideas came from the aspiring discussed lawsuit that dealt with water pollution ecological research in the U.S.A. and with the about which the pharmaceutical chemist Heinrich book of Stephen Alfred Forbes (1844—1930) Beckurts (1855—1929) from Brunswick had in- entitled ‘‘The Lake as a Microcosm’’ (Forbes formed him (see also Beckurts 1882; Denkler 1887), the programmatic catchword of the further 1980; Popp 1959; Thienemann 1925a,b; Vaupel development was born (Schwarz 2001). 1985). The endurance of the constant tension After the First World War, August Thienemann between the duty to study the details and the (1882—1960) became the champion first of Ger- danger of losing context with the large picture, man and soon also of international limnology was what Thienemann saw realized in an exemp- (Thienemann 1956, 1959). He came from fisheries lary way in Lauterborn’s life and research. Lauter- science and had studied the chironomid midges (a born became Thienemann’s hero, whom he felt group of Diptera comprising about 10,000 spe- obliged during his whole life. But then who was cies), an important component of the aquatic food Robert Lauterborn? web. The chironomid larvae develop in the Robert Lauterborn’s rather unspectacular life profundal zone at the bottom of water bodies. has been described in several obituaries and There, they form characteristic communities de- biographies, most recently by Lange (2001; using pending on oxygen and nutrient levels. Based on preparatory work done by Ju¨ rgen Schwoerbel the presence or absence of certain benthic [1930—2002]). Born in Ludwigshafen (October 23, chironomid larvae, Thienemann introduced his 1869) as the son of a local publisher, Robert went first system of lake classification, which he soon to school in Ludwigshafen and Mannheim where extended in collaboration with his swedish colle- he received his school-leaving degree (Abitur) age Einar Naumann (1891—1934) by adding the from the Realgymnasium in 1889. He studied appropriate types of phytoplankton. This resulted zoology and botany in Heidelberg (1889—1898) in the typification of complex biotopes by their where he graduated as ‘‘Dr. phil. nat.’’ in 1897 and biocoenoses: the primary producers, the consu- received his Habilitation (entrance examination for mers, the secondary consumers and the decom- university lecturers) 2 years later. Originating from posers. The inland lakes became a test-case for a non-wealthy middle-class background, he was ecological thinking. The further elaboration of lake familiar with austere living conditions and had to classification through studies of nutrient cycles seek additional income during his years as a appeared predetermined. student and non-tenured lecturer (Privatdozent). August Thienemann originated from Thuringia Income was generated by consulting. The young and had studied in Greifswald, Innsbruck, and man changed need to virtue and obtained valu- also in Heidelberg. To Heidelberg he was drawn by able knowledge and know-how in the transitional the legendary reputation of the zoologist and field between theoretical and applied hydrobiol- protistologist Otto Bu¨ tschli (1848—1920). How- ogy/limnology. His knowledge about organismal ARTICLE IN PRESS

Paulinella chromatophora and Robert Lauterborn 255 biology (animals, plants and microorganisms) was phenomenal. One could envisage that he, who was a professor of forest zoology between 1918 and 1935, first in Karlsruhe, then in Freiburg (Fig. 1), could as well have succeeded as a professor of limnology or botany. This extremely unpretentious and modest man, unfortunately was not spared blows of destiny. His mother died when he was 2 years old, his aunt Pauline became his stepmother when his father married his mother’s sister. Robert remained single and lived together with his two sisters, Ella and Paula. Paula died in 1939, and Ella was killed during an air-raid on Freiburg in 1945 during which his house and library were also destroyed. A little earlier he lost Figure 2. Robert Lauterborn (together with H. his collection at the forestry institute through Utermo¨ hl, right) at the 10th International Limnologi- world-war II bombings; his father’s (later his cal Congress in Switzerland, 1948. brother’s) lithographic facility in Ludwigshafen which housed the back files of Robert Lauter- born’s publications was similarly lost in 1943. E.B. Wilson), they have been verified in every Nevertheless, Lauterborn did not resign and detail almost 100 years later by Jeremy Pickett- resumed his scientific work (Fig. 2) during the Heaps and collaborators (Pickett-Heaps 1983; seven remaining post-war years of his life (he died Pickett-Heaps et al. 1984). Robert Lauterborn’s on September 11, 1952 in Freiburg). contributions to phycology were honored by a Of the many research areas in which Lauterborn special exhibition during the 1st European Phyco- excelled, we will deal here mainly with protistology logical Congress held in Cologne in 1996. and its relation to limnology and the biology of Lauterborn set the standards of his time with his wastewater. Lauterborn’s Ph.D. thesis described studies about saprobial life and with his contribu- the peculiar mitotic features of dinoflagellates, tion to the development of the ‘‘saprobial system’’ using Ceratium hirundinella as an example. Of championed by Richard Kolkwitz (1873—1956) even greater significance is his work entitled und Maximilian Marsson (1845—1909). When Untersuchungen u¨ber den Bau, Kernteilung und preparing this article, we noticed an interesting Bewegung der Diatomeen (‘‘Studies on the mor- terminological detail: In the German language, a phology, nuclear division and motility of diatoms’’; differentiation is made between the different Lauterborn 1893, 1896). The observations were processes occurring during the decay of dead described and illustrated with extraordinary detail organisms, i.e. whether they take place in the and clarity, especially those relating to the mitotic presence or absence of oxygen and are caused by spindles and centrosomes. And although the bacteria or fungi, respectively (Fa¨ ulnis, Verrottung, latter observations were sometimes questioned Verwesung; similar expressions exist in the French (by eminent scientists such as F.E. Fritsch and language). In colloquial English, however, this distinction is not made (only the old terms rot or rottenness exist) and one has to rely on foreign words such as decomposition, putrefaction or saprobic. Perhaps, it is not by accident that the ‘‘saprobial system’’ originated in Germany and continental Europe. Sometimes, it appears, that in the prevailing unilingual scientific language the fine level of expression inherent in colloquial languages has been lost. Now familiar processes such as aerobiosis, anaerobiosis, respiration, and fermentation were hotly debated during Lauter- born’s student days or were just being solved. Biochemistry had just started as a scientific discipline and many phenomena needed atten- Figure 1. Robert Lauterborn in Freiburg (1928). tion. Only in 1866 had Heinrich Anton de Bary ARTICLE IN PRESS

256 M. Melkonian and D. Mollenhauer

(1831—1888) introduced the terms mycotrophic and saprotrophic, and Louis Pasteur (1822—1895) described fermentation as a conse´quence de la vie sans air (‘‘a consequence of life without oxygen’’). In connection with these debates, which also touched on human pathology, epidemiology, fisheries, water supply, urban hygiene, etc., Robert Lauterborn intensively studied saprobes, organism living immediately above or in rotten sludge (Faulschlamm; Lauterborn 1901). According to studies of Swedish limnologists and soil scientists who had intensively analyzed the formation of lake sediments, there exist different zones in the sediment, for which the Swedish language has Figure 3. ‘‘The public and the naturalist’’ (R. Lauter- its own terms (Gyttja, A¨ fja, etc.; summarized by born, 1934). Naumann 1931), which were in part incorporated into the earlier period of limnology. The chemical composition of these zones is as typical as is the Paulinella chromatophora, the generic name given biological phenomena taking place in the different by him to honor his stepmother (and aunt), zones as can be demonstrated today using although he made no mention of this in the microprobes. During Lauterborn’s times, however, published paper. The work about Paulinella (Lau- intuition and careful observation were necessary, terborn 1895) was published before Lauterborn to characterize such habitats. Lauterborn also received his doctorate. The nestor of British knew much about ethnobiology and profited from phycology, Felix Eugen Fritsch (1879—1954), the experience of inland fishermen and water who intimately knew the phycological literature authorities. His pioneering studies about the of continental Europe wrote about the discovery of saprobial organisms (Lauterborn 1901) made him Paulinella: ‘‘The classical instance of the occur- well-known, and he was officially asked to rence of a blue-green endophyte within a colorless participate in the large-scale analysis of pollution organism is furnished by the Rhizopod Paulinella.. of the river Rhine (Lauterborn 1905, 1907, .. which, since its first discovery, has been found in 1908a—c, 1909a,b, 1910, 1911). With this long- many parts of the world. The blue-green symbiont term monitoring program, the imperial public . . . here takes the form of two large sausage- health office in Berlin reacted to complaints about shaped structures (Synechococcus?), which re- the increasing pollution of the river Rhine. This main alive for some hours when squeezed out of pollution was not only caused by the ever the host. During the division of Paulinella, one of increasing discharge of industrial and domestic the two Cyanellae passes through the narrow effluents into the river, but in part was also related aperture of the test into the new daughter- to non-consideration of the risks and side-effects individual and, like that left in the parent, soon of the large-scale physical regulation of the river divides into two. Little success has hitherto performed by Johann Gottfried Tulla (1770— attended the efforts to cultivate these endophytes 1828), an engineer from Baden, which began in outside their host, which is probably due to their 1817 in the upper Rhine valley. During his studies profound adaptation to the environment so that on the Rhine, Lauterborn collaborated with his suitable conditions of existence are not readily colleagues Kolkwitz, Marsson and Schaudinn, reproduced. That the Cyanellae play an important who came over from Berlin. Over a dozen years part in the nutrition of the hosts is shown by the later, Lauterborn summarized his knowledge capacity of the latter to lead an autotrophic about the inhabitants of the saprobes again existence and by the absence of holozoic nutrition (Lauterborn 1915). in Paulinella’’ (Fritsch 1945, p. 876). John W.G. Trained in the study of protists and familiar with Lund, who studied under Fritsch, added: ‘‘The the practice of limnology and the study of waste- cyanelles differ from the symbiotic Cyanophytes . . water, Lauterborn made remarkable discoveries . in that they cannot be grown outside the host (Fig. 3). One of those was the description of the organism. They can be considered to be sym- only presently known amoeba with blue-green bionts which in the course of time have become intracellular symbionts, the filose, testate amoeba an integral part of the host cell, that is organelles ARTICLE IN PRESS

Paulinella chromatophora and Robert Lauterborn 257 just as chloroplasts are organelles. Paulinella can (1924), Kies (1974) arranged ‘‘blue-green endo- then be looked upon as a photosynthetic animal’’ symbionts’’ (i.e. cyanelles in Pascher’s sense; (Canter-Lund and Lund 1995, pp 252—253). But Pascher 1929a) in a series of decreasing morpho- what did Lauterborn himself find out? logical and functional complexity starting with the As already indicated, Lauterborn found the ‘‘cyanelles’’ of Geosiphon (which can be cultivated material on which his description was based in outside their host and represent the cyanobacter- 1894 in an old riverbed of the river Rhine near ium Nostoc punctiforme; Mollenhauer et al. 1996), Neuhofen in what was then the Bavarian Rhine- then the cyanelles of Paulinella chromatophora Palatinate. The town Neuhofen is located in the (Pascher had in one case observed division of an floodplain of the upper Rhine valley southeast of isolated cyanelle outside its ‘‘host’’ [he squeezed Ludwigshafen between Limburgerhof and Altrip out the cyanelles from the amoebae by pressure, a on the left bank of today’s river. Later Lauterborn procedure that frequently resulted in breakage of found Paulinella also in the Black Forest. His the cyanelle caused by the sharp edges of the observations were soon confirmed by Euge` ne silica scales]; Pascher 1929b, pp 192—193), and Penard (1855—1954) from Geneva, who observed finally the cyanelles of Cyanophora, Glaucocystis the morphology and arrangement of the silica and the like, organisms which Kies and Kremer scales of the test in apical view (Penard 1905). (1990) placed into the division Glaucocystophyta Surprisingly, Penard described and illustrated only and which are now known to be part of the a single endosymbiont per amoeba, and presum- kingdom Plantae (here termed subkingdom Glau- ably regarded the second one described by coplantae). And while the cyanelles of the Glau- Lauterborn as only a pre-division situation. Finally, coplantae are genuine plastids (albeit uniquely Hoogenraad who studied cell division and forma- retaining the peptidoglycan cell wall of their tion of the new test in Paulinella in detail cyanobacterial ancestors), which together with (Hoogenraad 1927) clarified this aspect and wrote the plastids (i.e. the rhodoplasts) of the Rhodo- (translated from Dutch) ‘‘Thus we can state with plantae (i.e. the red algae) and the plastids (i.e. the certainty that Paulinella reproduces by bipartition chloroplasts) of the Viridiplantae (i.e. the green as do Euglypha species and their relatives. During algae and embryophytes) are of monophyletic this process one of the daughter individuals origin within the cyanobacteria (Helmchen et al. receives a new test built up from reserve scales 1995; Martin et al. 1998; Turner et al. 1999), the secreted into the protoplasm by the mother status of the cyanelles of Paulinella chromato- individual before division. One of the chromatophora still remains to be determined using a phores moves into the daughter individual, while molecular approach. What is very likely, though, the other stays inside the test of the mother is that the cyanelles of P. chromatophora origi- individual. The normal situation of two chromato- nated by a separate endocytobiotic event than the phores per cell is brought about by transverse cyanelles of the Glaucoplantae, irrespective of division of each of the two chromatophores’’ whether they are genetically reduced (such as (Hoogenraad and De Groot 1927, p. 12). Cell plastids) or not (in which case they may represent division of Paulinella chromatophora is thus similar an intracellular cyanobacterial symbiont such as to that of Euglypha alveolata, as illustrated by Grell Nostoc punctiforme in Geosiphon). This conclu- (1956, p. 81; 1973, p. 124) based on observations sion is based on the fact that the host, the testate by Schewiakoff. amoeba, has been firmly placed within the Paulinella also attracted the interest of promi- Euglyphidae (Bhattacharya et al. 1995), which nent phycologists among them Lothar Geitler together with other filose amoebae, zooflagellates, (1927, 1959) and Adolf Pascher (1929a, b) who, foraminifera, polycystines and acantharia form a during these studies, introduced the terms cya- new superassemblage of eukaryotes, the Rhizaria nelle (Pascher 1929b) and syncyanosis (Pascher (Cavalier-Smith 2002), and thus that Paulinella is 1914; see Geitler 1959). Lackey (1936) and not monophyletic with the Glaucoplantae. The Lederberg (1952) discussed whether the endo- alternative hypothesis, although unlikely, namely symbionts of Paulinella should be regarded as that the cyanelles of the Glaucoplantae and those ‘‘cell organelles’’. Finally, morphological studies on of Paulinella are indeed monophyletic and that Paulinella chromatophora were concluded by Kies Paulinella received its cyanelles through a sec- (1974, 1992) who was the first to investigate the ondary endocytobiosis involving a glaucoplant organism by transmission electron microscopy. symbiont should not a priori be dismissed. He found the ‘‘cyanelles’’ ‘‘lying within vesicles in Geitler (1927), Pascher (1929b) and Kies (1974) the cytoplasma of the host’’. Following Geitler have all concluded that the cyanelles of ARTICLE IN PRESS

258 M. Melkonian and D. Mollenhauer

P. chromatophora are closely related to free-living and structure.’’ Lauterborn then goes on (p. 541) cyanobacteria and Pascher (1929b) even sug- with an interesting comparison ‘‘Perhaps the gested that the cyanelle of Paulinella may repre- difference between a symbiotic alga and a sent a species of the extant genus Synecho- chromatophore may not be so significant after all coccus (Lukavsky´ and Cepa´ k 1992 studied the because it may not be impossible that the nucleoids of P. chromatophora by DAPI fluores- chromatophores in general exist in a symbiotic cence and concluded that they most closely relationship with the cells containing them.’’ Here, resembled those of Synechococcus elongatus he seems to touch on the possible endosymbiotic f. thermalis). And what did Robert Lauterborn origin of the chromatophores (i.e. plastids) without conclude? explicitly advancing this hypothesis (as did Mer- In his description, Lauterborn (1895) cautiously eschkovsky 10 years later). Finally, Lauterborn referred to the blue-green endosymbionts of P. concludes ‘‘A decision about this question (the chromatophora as ‘‘chromatophore-like struc- nature of the chromatophores of Paulinella) must tures’’ (chromatophorenartige Gebilde). He ob- be left to the future, however, there can presently served an outer pigmented part and a central non- be no doubt that the blue-green inclusions in the pigmented part in the cyanelle, the latter contain- plasma of Paulinella function as real chromato- ing fine granules often arranged like a string of phores, i.e. the products of their assimilation pearls in the center of the cyanelle (Fig. 4). About nourish the rhizopod body. I reach this conclusion the possible nature of the cyanelles Lauterborn because in none of the 200 studied individuals of wrote ‘‘A priori the following possibilities can be the rhizopod, I observed any uptake of food taken into consideration about the nature of the particles, although I focused my attention speci- said inclusions. Either the blue-green structures fically on this aspect.’’ Lauterborn’s remarkably represent algae from the division Cyanophyceae insightful conclusions still hold today! which are taken up as food or they are indepen- It is noticeable that the older literature is largely dent organisms — in this case again Cyanophy- silent about the type of habitat in which Paulinella ceae — that live with the rhizopod in an intimate chromatophora thrives. Penard took over Lauter- symbiosis, or finally they are integral components, born’s description ‘‘in diatom mats’’ and provided real organs of the rhizopod cell body. The first no further information. Similarly, Kies (1974), assumption is untenable, because their universal Grospietsch (1958), Scho¨ nborn (1966), Thomas- presence in over 200 individuals studied, the son (1952), Skuja (1964), and Canter-Lund and absence of such structures in the natural environ- Lund (1995) all made only very general statements ment, and the ability of the structures to divide about the occurrence of Paulinella. However, our within the plasma rule out the possibility that said own experience suggests that the habitat of structures are only accidental components of the Paulinella chromatophora can be described more cell body of the rhizopod. More difficult, and precisely. Lauterborn’s location already gives perhaps currently impossible, is the decision some hints. The old riverbeds in the fertile plain between the last two possibilities. In favor of a of the Rhine often lead water with low oxygen symbiosis one may refer to many known examples content, which ascends from the soaked and in which algae from the group of the Cyanophy- oxygen-depleted subsoil. In addition, oxygen is ceae enter intimate associations with other organ- largely consumed by saprobial organisms, leading isms — for example one may think of the lichens to anoxic or microaerophilic conditions including which are nothing else than fungi (mostly asco- trace amounts of hydrogen sulfide near the mycetes) living intimately together with certain sediment surface. Paulinella chromatophora oc- blue-green (more rarely green) algae. Also the curs as part of a very characteristic community of above-mentioned fine structure of the ‘‘chroma- organisms that include (as already noticed by tophores’’ can be regarded as support for their Lauterborn) Gymnodinium aeruginosum, Glauco- independent status, the central non-pigmented cystis nostochinearum, Chroomonas nordtstedtii part representing the nucleus (or ‘‘central body’’) and several cyanobacteria (Lauterborn mentions of typical Cyanophyceae (e.g. Oscillatoria, Mer- ‘‘Merismopedia elegans’’, ‘‘Microcystis spp.’’, ismopedia, etc.). In support of the chromatophore ‘‘Spirulina spp.’’ and others). These organisms nature of the blue-green inclusions, one may refer are adjusted to this peculiar environment and may only to the fact that, as far as I am aware, no free- be adversely affected when transferred to oxygen- living Cyanophyceae exists or at least occurs in rich conditions. In addition, their habitat is rich in the natural environment of Paulinella that resem- organic compounds, the salinity is higher (up to bles the ‘‘chromatophores’’ of Paulinella in shape brackish conditions; see also Pankow 1982 who ARTICLE IN PRESS

Paulinella chromatophora and Robert Lauterborn 259

Figure 4. Plate 30 with 7 ﬁgures of various aspects of Paulinella chromatophora taken from Robert Lauterborn’s original description published in Zeitschrift fu¨r wissenschaftliche Zoologie (Vol. 59, 537—544, 1985). Figs. 1, 2 and 4 illustrate cells of Paulinella chromatophora in longitudinal (1,2) or cross section (4), a surface view of the test (3), ‘‘chromatophores’’ in side view (5) and optical cross section (6), and the apical, ﬁve-sided plate with the oval opening (‘‘mouth’’) (7). ARTICLE IN PRESS

260 M. Melkonian and D. Mollenhauer found P. chromatophora in the shallow bays of the Forbes S (1887) The lake as a microcosm. Bull Darss and Zingst in the Southern Baltic Sea; other Peoria Sci Ass 1887: 537—550 species of Paulinella, e.g. P. ovalis, have been Forel FA (1882) Programme d’e´ tudes limnologiques found in the marine environment feeding on pur les lacs subalpins. Arch Sci Phys Nat 3: cyanobacteria: Hannah et al. 1996; Johnson et 548—550 al. 1988; Vørs 1993) and often the pH is low. It is apparently difficult to reproduce these conditions Fritsch FE (1945) Structure and Reproduction of the in the laboratory and this may be one of the Algae, Vol. 1. Cambridge University Press, Cam- reasons for the failure to grow some of the bridge organisms of this community ex situ. Geitler L (1924) Der Zellbau von Glaucocystis nostochinearum und Gloeochaete wittrockiana und die Chromatophoren-Symbiosetheorie von Mer- Acknowledgement eschkowsky. Arch Protistenkd 47: 1—24 Geitler L (1927) Bemerkungen zu Paulinella chro- DM would like to thank B. Lechner (librarian, Max- matophora. Zool Anz 72: 333—334 Plank-Institute for Limnology, Plo¨ n, Germany) for providing photographs of Robert Lauterborn, Geitler L (1959) Syncyanosen. In Ruhland W (ed) which are here reprinted as Figures 1—3. Handbuch der Pflanzenphysiologie, Vol. 11, Hetero- trophie. Springer, Berlin, pp 530—545 Grell KG (1956) Protozoologie. J. Springer, Berlin, References Go¨ ttingen, Heidelberg Beckurts H (1882) Ueber die Verunreinigung der Grell KG (1973) Protozoology. Springer, Berlin, Flu¨ sse durch Effluvien von Zuckerfabriken. Monatsbl Heidelberg o¨ ffentl Gesundheitspfl 5: 161—173 Grospietsch T (1958) Wechseltierchen (Rhizopo- Bhattacharya D, Helmchen T, Melkonian M (1995) den). Kosmos (Franckh), Stuttgart Molecular evolutionary analyses of nuclear-encoded Hannah F, Rogerson A, Anderson OR (1996) A small subunit ribosomal RNA identify an indepen- description of Paulinella indentata n. sp. (Filosea: dent rhizopod lineage containing the Euglyphina and Euglyphina) from subtidal coastal benthic sediments. the Chlorarachniophyta. J Eukaryot Microbiol 42: J Eukaryot Microbiol 43: 1—4 65—69 Helmchen TA, Bhattacharya D, Melkonian M Bhattacharya D, Yoon HS, Hackett JD (2003) (1995) Analyses of ribosomal RNA sequences from Photosynthetic eukaryotes unit: endosymbiosis con- glaucocystophyte cyanelles provide new insights nects the dots. BioEssays 26: 50—60 into the evolutionary relationships of plastids. J Mol Canter-Lund HM, Lund JWG (1995) Freshwater Evol 41: 203—210 Algae: Their Microscopic World Explored. Biopress, Hoogenraad HR (1927) Zur Kenntnis der Fortpflan- Bristol zung von Paulinella chromatophora Lauterb. Zool Cavalier-Smith T (2002) The phagotrophic origin of Anz 72: 140—150 eukaryotes and phylogenetic classification of Proto- Hoogenraad HR, de Groot AA (1927) Rhizopoden zoa. Int J Syst Evol Microbiol 52: 297—354 en Heliozoe¨ uit het zoetwater van Nederland. Cohn F (1853) U¨ ber lebende Organismen im Tijdschr Nederl dierkund vereen (2) 20: 1—18 Trinkwasser. Gu¨ nzberg Z klin Med 4: 229—237 Jahn I (2001) Gu¨ nther Leps in memoriam. Verh Delwiche CF (1999) Tracing the thread of plastid Gesch Theor Biol 7: 9—12 diversity through the tapestry of life. Am Nat 154: Johnson PW, Hargraves PE, Sieburth JMcN (1988) S164—S177 Ultrastructure and acology of Calycomonas ovalis Denkler H (1980) [Appendix and epilogue to Wilhelm Wulff, 1919, (Chrysophyceae) and its redes- Raabe: Pfisters Mu¨ hle]. Reclams Universalbibliothek cription as a testate rhizopod, Paulinella ovalis 9988: 223—251 n. comb. (Filosea: Euglyphina). J Protozool 35: 618—626 Fo¨ rdergesellschaft Albrecht Daniel Thaer e.V. Mo¨ glin (2004) Albrecht Daniel Thaer in Brandenburg Keeling PJ (2004) Diversity and evolutionary his- und Berlin. Findling Buch und Zeitschriftenverlag, tory of plastids and their hosts. Am J Bot 91: Neuenhagen 1481—1493 ARTICLE IN PRESS

Paulinella chromatophora and Robert Lauterborn 261

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