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Protist, Vol. 156, 253—262, August 2005

1Correspondinfax +49 221 47e-mail michae

& 2005 Elsevdoi:10.1016/j

elsevier.de/protis

http://www.Published online date 11 July 2005

FROM THE ARCHIVES

Robert Lauterborn (1869—1952) and his Paulinellachromatophora

Michael Melkoniana,1and Dieter Mollenhauerb

aBotanisches Institut, Lehrstuhl I, Universita t zu Koln, Gyrhofstr. 15, 50931 Koln, GermanybForschungsinstitut Senckenberg, Frankfurt am Main, Forschungsstation fur Mittelgebirge, Lochmuhle 2,63599 Biebergemund, Germany

In 1895, in his second, short contribution aboutprotozoa (Protozoenstudien II.), Robert Lauter-born, then at the Zoology Department of theUniversity of Heidelberg, described a novel organ-ism (nov. gen. et nov. spec.) which he namedPaulinella chromatophora. He must have beenvery exited about his discovery which he made onChristmas Eve 1894, since he clearly recognizedthe importance of his observations for symbiosisresearch and biology, in general. And although hisPaulinella featured only occasionally in scientificpublications during the next 100 years, it nowappears to be taking center stage in discussionsabout the endosymbiotic origin of plastids (somerecent reviews in this field that mention Paulinellainclude Bhattacharya et al. 2003; Delwiche 1999;Keeling 2004; McFadden 2001). Who was thediscoverer, what characterized his time, socio-economically and scientifically, and finally whatdid Lauterborn discover about Paulinella chroma-tophora that made him write (in the first sentenceof his publication, p. 36; translated from German)‘‘Among the many protozoa that populate theextensive diatom mats of the Altrhein nearNeuhofen (about 6 km south of Ludwigshafen onRhine, Germany) during the cold season, I found,on December 24 last year, a new rhizopod, that inmore than one respect can demand to be ranked

g author;0 5181l.melkonian@uni-koeln.de (M. Melkonian)

ier GmbH. All rights reserved..protis.2005.06.001

among the most interesting representatives of itsdivision in freshwater.’’ ?

In the second half of the 19th century the socio-economic situation in Germany (i.e. urbanization,industrialization and the rise of an urban proletar-iat) led to pronounced and lasting environmentalchanges (e.g. degradation of soil and naturalwaters, epidemic human diseases, plant diseases,decline of forests). The Janus face of prosperitywere difficulties of supply, lack of hygiene insettlements, and various kinds of diseases.Gradually, questions were raised which today areknown as problems of waste disposal. Carefulobservers such as Ferdinand Cohn (1828—1898)had early recognized the problems and with themethods then available initiated simple environ-mental monitoring systems (Cohn 1853; Kolkwitzand Marsson 1908; Mez 1898). Jorg Lange,Gunther Leps (1934—2000; bibliography in Jahn2001), Thomas Potthast and Astrid E. Schwarzhave described the circumstances of the ‘‘Wilhel-minian’’ epoch and the early period of the‘‘republic of Weimar’’ and their influence on thedevelopment of science in Germany (Lange 1990,1994; Leps 1998; Potthast 2001; Schwarz 2001).

The economic boom came after the GermanFrench war and finally led to overheating duringthe Grunderzeit (‘‘founder period’’; 1871—1873)and in consequence to many bankruptcies. Duringsuch phases of prosperity interest is initiallyfocused on the requirements for economicgrowth: production and delivery of food andraw materials. Concomitantly, the older ‘‘humus

ARTICLE IN PRESS254 M. Melkonian and D. Mollenhauer

theory’’ of Albrecht Thaer (1752—1828; Forderge-sellschaft Albrecht Daniel Thaer e.V. Moglin 2004)was superseded by the modern concept of themineral nutrition of plants by Justus von Liebig(1803—1873). The victory of this concept and thefirst successes of the production-oriented viewdiverted attention from the problem of wastedisposal that usually seems to be of less im-portance to the public. However, the above-mentioned problems leading to increasing wastelandfills and the omnipresent wastewater, made itthe more important to try to better understand thedecomposition process (today known as recy-cling). Wastewater treatment using artificial wet-lands and trickling filters was introduced duringthis time (see Kolkwitz 1922).

The scientific study of aquatic ecosystems hadjust been initiated. Franc-ois Alphonse Forel(1841—1912) in Geneva had introduced the termlimnology (the science of inland waters; Forel1882); many new ideas came from the aspiringecological research in the U.S.A. and with thebook of Stephen Alfred Forbes (1844—1930)entitled ‘‘The Lake as a Microcosm’’ (Forbes1887), the programmatic catchword of the furtherdevelopment was born (Schwarz 2001).

After the First World War, August Thienemann(1882—1960) became the champion first of Ger-man and soon also of international limnology(Thienemann 1956, 1959). He came from fisheriesscience and had studied the chironomid midges (agroup of Diptera comprising about 10,000 spe-cies), an important component of the aquatic foodweb. The chironomid larvae develop in theprofundal zone at the bottom of water bodies.There, they form characteristic communities de-pending on oxygen and nutrient levels. Based onthe presence or absence of certain benthicchironomid larvae, Thienemann introduced hisfirst system of lake classification, which he soonextended in collaboration with his swedish colle-age Einar Naumann (1891—1934) by adding theappropriate types of phytoplankton. This resultedin the typification of complex biotopes by theirbiocoenoses: the primary producers, the consu-mers, the secondary consumers and the decom-posers. The inland lakes became a test-case forecological thinking. The further elaboration of lakeclassification through studies of nutrient cyclesappeared predetermined.

August Thienemann originated from Thuringiaand had studied in Greifswald, Innsbruck, andalso in Heidelberg. To Heidelberg he was drawn bythe legendary reputation of the zoologist andprotistologist Otto Butschli (1848—1920). How-

ever, Butschli fell ill during the time whenThienemann was there and could not givelectures. This brought Thienemann closer to thejunior lecturer (Privatdozent) Robert Lauterborn(1869—1952). The meeting between the 21-yearold zoology student from Thuringia and the 34-year old lecturer from the Palatinate was fateful.August Thienemann in his research has alwaysdealt with both the fruitful suggestions as well asthe pitfalls that ‘‘holism’’ held for biology. Heplaced his life under the motto Schau auf zu denSternen, hab acht auf die Gassen (‘‘look up to thestars, pay attention to the alleys’’). This phrasewas introduced by the lower-saxon poet andwriter Wilhelm Raabe (1831—1910), whom Thie-nemann valued highly (see Thienemann 1949).Raabe had dealt with environmental issues in hislesser known novel Pfisters Muhle (Raabe 1970[originally 1884]), not casually or in a general waybut specifically using records from a publiclydiscussed lawsuit that dealt with water pollutionabout which the pharmaceutical chemist HeinrichBeckurts (1855—1929) from Brunswick had in-formed him (see also Beckurts 1882; Denkler1980; Popp 1959; Thienemann 1925a,b; Vaupel1985). The endurance of the constant tensionbetween the duty to study the details and thedanger of losing context with the large picture,was what Thienemann saw realized in an exemp-lary way in Lauterborn’s life and research. Lauter-born became Thienemann’s hero, whom he feltobliged during his whole life. But then who wasRobert Lauterborn?

Robert Lauterborn’s rather unspectacular lifehas been described in several obituaries andbiographies, most recently by Lange (2001; usingpreparatory work done by Jurgen Schwoerbel[1930—2002]). Born in Ludwigshafen (October 23,1869) as the son of a local publisher, Robert wentto school in Ludwigshafen and Mannheim wherehe received his school-leaving degree (Abitur)from the Realgymnasium in 1889. He studiedzoology and botany in Heidelberg (1889—1898)where he graduated as ‘‘Dr. phil. nat.’’ in 1897 andreceived his Habilitation (entrance examination foruniversity lecturers) 2 years later. Originating froma non-wealthy middle-class background, he wasfamiliar with austere living conditions and had toseek additional income during his years as astudent and non-tenured lecturer (Privatdozent).Income was generated by consulting. The youngman changed need to virtue and obtained valu-able knowledge and know-how in the transitionalfield between theoretical and applied hydrobiol-ogy/limnology. His knowledge about organismal

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Figure 2. Robert Lauterborn (together with H.Utermohl, right) at the 10th International Limnologi-cal Congress in Switzerland, 1948.

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 between1918 and 1935, first in Karlsruhe, then in Freiburg(Fig. 1), could as well have succeeded as aprofessor of limnology or botany. This extremelyunpretentious and modest man, unfortunately wasnot spared blows of destiny. His mother died whenhe was 2 years old, his aunt Pauline became hisstepmother when his father married his mother’ssister. Robert remained single and lived togetherwith his two sisters, Ella and Paula. Paula died in1939, and Ella was killed during an air-raid onFreiburg in 1945 during which his house andlibrary were also destroyed. A little earlier he losthis collection at the forestry institute throughworld-war II bombings; his father’s (later hisbrother’s) lithographic facility in Ludwigshafenwhich housed the back files of Robert Lauter-born’s publications was similarly lost in 1943.Nevertheless, Lauterborn did not resign andresumed his scientific work (Fig. 2) during theseven remaining post-war years of his life (he diedon September 11, 1952 in Freiburg).

Of the many research areas in which Lauterbornexcelled, we will deal here mainly with protistologyand its relation to limnology and the biology ofwastewater. Lauterborn’s Ph.D. thesis describedthe peculiar mitotic features of dinoflagellates,using Ceratium hirundinella as an example. Ofeven greater significance is his work entitledUntersuchungen uber den Bau, Kernteilung undBewegung der Diatomeen (‘‘Studies on the mor-phology, nuclear division and motility of diatoms’’;Lauterborn 1893, 1896). The observations weredescribed and illustrated with extraordinary detailand clarity, especially those relating to the mitoticspindles and centrosomes. And although thelatter observations were sometimes questioned(by eminent scientists such as F.E. Fritsch and

Figure 1. Robert Lauterborn in Freiburg (1928).

E.B. Wilson), they have been verified in everydetail almost 100 years later by Jeremy Pickett-Heaps and collaborators (Pickett-Heaps 1983;Pickett-Heaps et al. 1984). Robert Lauterborn’scontributions to phycology were honored by aspecial exhibition during the 1st European Phyco-logical Congress held in Cologne in 1996.

Lauterborn set the standards of his time with hisstudies about saprobial life and with his contribu-tion to the development of the ‘‘saprobial system’’championed by Richard Kolkwitz (1873—1956)und Maximilian Marsson (1845—1909). Whenpreparing this article, we noticed an interestingterminological detail: In the German language, adifferentiation is made between the differentprocesses occurring during the decay of deadorganisms, i.e. whether they take place in thepresence or absence of oxygen and are caused bybacteria or fungi, respectively (Faulnis, Verrottung,Verwesung; similar expressions exist in the Frenchlanguage). In colloquial English, however, thisdistinction is not made (only the old terms rot orrottenness exist) and one has to rely on foreignwords such as decomposition, putrefaction orsaprobic. Perhaps, it is not by accident that the‘‘saprobial system’’ originated in Germany andcontinental Europe. Sometimes, it appears, that inthe prevailing unilingual scientific language thefine level of expression inherent in colloquiallanguages has been lost. Now familiar processessuch as aerobiosis, anaerobiosis, respiration, andfermentation were hotly debated during Lauter-born’s student days or were just being solved.Biochemistry had just started as a scientificdiscipline and many phenomena needed atten-tion. Only in 1866 had Heinrich Anton de Bary

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Figure 3. ‘‘The public and the naturalist’’ (R. Lauter-born, 1934).

256 M. Melkonian and D. Mollenhauer

(1831—1888) introduced the terms mycotrophicand saprotrophic, and Louis Pasteur (1822—1895)described fermentation as a consequence de lavie sans air (‘‘a consequence of life withoutoxygen’’).

In connection with these debates, which alsotouched on human pathology, epidemiology, fish-eries, water supply, urban hygiene, etc., RobertLauterborn intensively studied saprobes, organ-ism living immediately above or in rotten sludge(Faulschlamm; Lauterborn 1901). According tostudies of Swedish limnologists and soil scientistswho had intensively analyzed the formation of lakesediments, there exist different zones in thesediment, for which the Swedish language hasits own terms (Gyttja, Afja, etc.; summarized byNaumann 1931), which were in part incorporatedinto the earlier period of limnology. The chemicalcomposition of these zones is as typical as is thebiological phenomena taking place in the differentzones as can be demonstrated today usingmicroprobes. During Lauterborn’s times, however,intuition and careful observation were necessary,to characterize such habitats. Lauterborn alsoknew much about ethnobiology and profited fromthe experience of inland fishermen and waterauthorities. His pioneering studies about thesaprobial organisms (Lauterborn 1901) made himwell-known, and he was officially asked toparticipate in the large-scale analysis of pollutionof the river Rhine (Lauterborn 1905, 1907,1908a—c, 1909a,b, 1910, 1911). With this long-term monitoring program, the imperial publichealth office in Berlin reacted to complaints aboutthe increasing pollution of the river Rhine. Thispollution was not only caused by the everincreasing discharge of industrial and domesticeffluents into the river, but in part was also relatedto non-consideration of the risks and side-effectsof the large-scale physical regulation of the riverperformed by Johann Gottfried Tulla (1770—1828), an engineer from Baden, which began in1817 in the upper Rhine valley. During his studieson the Rhine, Lauterborn collaborated with hiscolleagues Kolkwitz, Marsson and Schaudinn,who came over from Berlin. Over a dozen yearslater, Lauterborn summarized his knowledgeabout the inhabitants of the saprobes again(Lauterborn 1915).

Trained in the study of protists and familiar withthe practice of limnology and the study of waste-water, Lauterborn made remarkable discoveries(Fig. 3). One of those was the description of theonly presently known amoeba with blue-greenintracellular symbionts, the filose, testate amoeba

Paulinella chromatophora, the generic name givenby him to honor his stepmother (and aunt),although he made no mention of this in thepublished paper. The work about Paulinella (Lau-terborn 1895) was published before Lauterbornreceived his doctorate. The nestor of Britishphycology, Felix Eugen Fritsch (1879—1954),who intimately knew the phycological literatureof continental Europe wrote about the discovery ofPaulinella: ‘‘The classical instance of the occur-rence of a blue-green endophyte within a colorlessorganism is furnished by the Rhizopod Paulinella. ... which, since its first discovery, has been found inmany parts of the world. The blue-green symbiont. . . here takes the form of two large sausage-shaped structures (Synechococcus?), which re-main alive for some hours when squeezed out ofthe host. During the division of Paulinella, one ofthe two Cyanellae passes through the narrowaperture of the test into the new daughter-individual and, like that left in the parent, soondivides into two. Little success has hithertoattended the efforts to cultivate these endophytesoutside their host, which is probably due to theirprofound adaptation to the environment so thatsuitable conditions of existence are not readilyreproduced. That the Cyanellae play an importantpart in the nutrition of the hosts is shown by thecapacity of the latter to lead an autotrophicexistence and by the absence of holozoic nutritionin Paulinella’’ (Fritsch 1945, p. 876). John W.G.Lund, who studied under Fritsch, added: ‘‘Thecyanelles differ from the symbiotic Cyanophytes . .. in that they cannot be grown outside the hostorganism. They can be considered to be sym-bionts which in the course of time have becomean integral part of the host cell, that is organelles

ARTICLE IN PRESSPaulinella chromatophora and Robert Lauterborn 257

just as chloroplasts are organelles. Paulinella canthen be looked upon as a photosynthetic animal’’(Canter-Lund and Lund 1995, pp 252—253). Butwhat did Lauterborn himself find out?

As already indicated, Lauterborn found thematerial on which his description was based in1894 in an old riverbed of the river Rhine nearNeuhofen in what was then the Bavarian Rhine-Palatinate. The town Neuhofen is located in thefloodplain of the upper Rhine valley southeast ofLudwigshafen between Limburgerhof and Altripon the left bank of today’s river. Later Lauterbornfound Paulinella also in the Black Forest. Hisobservations were soon confirmed by EugenePenard (1855—1954) from Geneva, who observedthe morphology and arrangement of the silicascales of the test in apical view (Penard 1905).Surprisingly, Penard described and illustrated onlya single endosymbiont per amoeba, and presum-ably regarded the second one described byLauterborn as only a pre-division situation. Finally,Hoogenraad who studied cell division and forma-tion of the new test in Paulinella in detail(Hoogenraad 1927) clarified this aspect and wrote(translated from Dutch) ‘‘Thus we can state withcertainty that Paulinella reproduces by bipartitionas do Euglypha species and their relatives. Duringthis process one of the daughter individualsreceives a new test built up from reserve scalessecreted into the protoplasm by the motherindividual before division. One of the chromato-phores moves into the daughter individual, whilethe other stays inside the test of the motherindividual. The normal situation of two chromato-phores per cell is brought about by transversedivision of each of the two chromatophores’’(Hoogenraad and De Groot 1927, p. 12). Celldivision of Paulinella chromatophora is thus similarto that of Euglypha alveolata, as illustrated by Grell(1956, p. 81; 1973, p. 124) based on observationsby Schewiakoff.

Paulinella also attracted the interest of promi-nent phycologists among them Lothar Geitler(1927, 1959) and Adolf Pascher (1929a, b) who,during these studies, introduced the terms cya-nelle (Pascher 1929b) and syncyanosis (Pascher1914; see Geitler 1959). Lackey (1936) andLederberg (1952) discussed whether the endo-symbionts of Paulinella should be regarded as‘‘cell organelles’’. Finally, morphological studies onPaulinella chromatophora were concluded by Kies(1974, 1992) who was the first to investigate theorganism by transmission electron microscopy.He found the ‘‘cyanelles’’ ‘‘lying within vesicles inthe cytoplasma of the host’’. Following Geitler

(1924), Kies (1974) arranged ‘‘blue-green endo-symbionts’’ (i.e. cyanelles in Pascher’s sense;Pascher 1929a) in a series of decreasing morpho-logical and functional complexity starting with the‘‘cyanelles’’ of Geosiphon (which can be cultivatedoutside their host and represent the cyanobacter-ium Nostoc punctiforme; Mollenhauer et al. 1996),then the cyanelles of Paulinella chromatophora(Pascher had in one case observed division of anisolated cyanelle outside its ‘‘host’’ [he squeezedout the cyanelles from the amoebae by pressure, aprocedure that frequently resulted in breakage ofthe cyanelle caused by the sharp edges of thesilica scales]; Pascher 1929b, pp 192—193), andfinally the cyanelles of Cyanophora, Glaucocystisand the like, organisms which Kies and Kremer(1990) placed into the division Glaucocystophytaand which are now known to be part of thekingdom Plantae (here termed subkingdom Glau-coplantae). And while the cyanelles of the Glau-coplantae are genuine plastids (albeit uniquelyretaining the peptidoglycan cell wall of theircyanobacterial ancestors), which together withthe plastids (i.e. the rhodoplasts) of the Rhodo-plantae (i.e. the red algae) and the plastids (i.e. thechloroplasts) of the Viridiplantae (i.e. the greenalgae and embryophytes) are of monophyleticorigin within the cyanobacteria (Helmchen et al.1995; Martin et al. 1998; Turner et al. 1999), thestatus of the cyanelles of Paulinella chromato-phora still remains to be determined using amolecular approach. What is very likely, though,is that the cyanelles of P. chromatophora origi-nated by a separate endocytobiotic event than thecyanelles of the Glaucoplantae, irrespective ofwhether they are genetically reduced (such asplastids) or not (in which case they may representan intracellular cyanobacterial symbiont such asNostoc punctiforme in Geosiphon). This conclu-sion is based on the fact that the host, the testateamoeba, has been firmly placed within theEuglyphidae (Bhattacharya et al. 1995), whichtogether with other filose amoebae, zooflagellates,foraminifera, polycystines and acantharia form anew superassemblage of eukaryotes, the Rhizaria(Cavalier-Smith 2002), and thus that Paulinella isnot monophyletic with the Glaucoplantae. Thealternative hypothesis, although unlikely, namelythat the cyanelles of the Glaucoplantae and thoseof Paulinella are indeed monophyletic and thatPaulinella received its cyanelles through a sec-ondary endocytobiosis involving a glaucoplantsymbiont should not a priori be dismissed.

Geitler (1927), Pascher (1929b) and Kies (1974)have all concluded that the cyanelles of

ARTICLE IN PRESS258 M. Melkonian and D. Mollenhauer

P. chromatophora are closely related to free-livingcyanobacteria and Pascher (1929b) even sug-gested that the cyanelle of Paulinella may repre-sent a species of the extant genus Synecho-coccus (Lukavsky and Cepak 1992 studied thenucleoids of P. chromatophora by DAPI fluores-cence and concluded that they most closelyresembled those of Synechococcus elongatusf. thermalis). And what did Robert Lauterbornconclude?

In his description, Lauterborn (1895) cautiouslyreferred to the blue-green endosymbionts of P.chromatophora as ‘‘chromatophore-like struc-tures’’ (chromatophorenartige Gebilde). He ob-served an outer pigmented part and a central non-pigmented part in the cyanelle, the latter contain-ing fine granules often arranged like a string ofpearls in the center of the cyanelle (Fig. 4). Aboutthe possible nature of the cyanelles Lauterbornwrote ‘‘A priori the following possibilities can betaken into consideration about the nature of thesaid inclusions. Either the blue-green structuresrepresent algae from the division Cyanophyceaewhich are taken up as food or they are indepen-dent organisms — in this case again Cyanophy-ceae — that live with the rhizopod in an intimatesymbiosis, or finally they are integral components,real organs of the rhizopod cell body. The firstassumption is untenable, because their universalpresence in over 200 individuals studied, theabsence of such structures in the natural environ-ment, and the ability of the structures to dividewithin the plasma rule out the possibility that saidstructures are only accidental components of thecell body of the rhizopod. More difficult, andperhaps currently impossible, is the decisionbetween the last two possibilities. In favor of asymbiosis one may refer to many known examplesin which algae from the group of the Cyanophy-ceae enter intimate associations with other organ-isms — for example one may think of the lichenswhich are nothing else than fungi (mostly asco-mycetes) living intimately together with certainblue-green (more rarely green) algae. Also theabove-mentioned fine structure of the ‘‘chroma-tophores’’ can be regarded as support for theirindependent status, the central non-pigmentedpart representing the nucleus (or ‘‘central body’’)of typical Cyanophyceae (e.g. Oscillatoria, Mer-ismopedia, etc.). In support of the chromatophorenature of the blue-green inclusions, one may referonly to the fact that, as far as I am aware, no free-living Cyanophyceae exists or at least occurs inthe natural environment of Paulinella that resem-bles the ‘‘chromatophores’’ of Paulinella in shape

and structure.’’ Lauterborn then goes on (p. 541)with an interesting comparison ‘‘Perhaps thedifference between a symbiotic alga and achromatophore may not be so significant after allbecause it may not be impossible that thechromatophores in general exist in a symbioticrelationship with the cells containing them.’’ Here,he seems to touch on the possible endosymbioticorigin of the chromatophores (i.e. plastids) withoutexplicitly advancing this hypothesis (as did Mer-eschkovsky 10 years later). Finally, Lauterbornconcludes ‘‘A decision about this question (thenature of the chromatophores of Paulinella) mustbe left to the future, however, there can presentlybe no doubt that the blue-green inclusions in theplasma of Paulinella function as real chromato-phores, i.e. the products of their assimilationnourish the rhizopod body. I reach this conclusionbecause in none of the 200 studied individuals ofthe rhizopod, I observed any uptake of foodparticles, although I focused my attention speci-fically on this aspect.’’ Lauterborn’s remarkablyinsightful conclusions still hold today!

It is noticeable that the older literature is largelysilent about the type of habitat in which Paulinellachromatophora thrives. Penard took over Lauter-born’s description ‘‘in diatom mats’’ and providedno further information. Similarly, Kies (1974),Grospietsch (1958), Schonborn (1966), Thomas-son (1952), Skuja (1964), and Canter-Lund andLund (1995) all made only very general statementsabout the occurrence of Paulinella. However, ourown experience suggests that the habitat ofPaulinella chromatophora can be described moreprecisely. Lauterborn’s location already givessome hints. The old riverbeds in the fertile plainof the Rhine often lead water with low oxygencontent, which ascends from the soaked andoxygen-depleted subsoil. In addition, oxygen islargely consumed by saprobial organisms, leadingto anoxic or microaerophilic conditions includingtrace amounts of hydrogen sulfide near thesediment surface. Paulinella chromatophora oc-curs as part of a very characteristic community oforganisms that include (as already noticed byLauterborn) Gymnodinium aeruginosum, Glauco-cystis nostochinearum, Chroomonas nordtstedtiiand several cyanobacteria (Lauterborn mentions‘‘Merismopedia elegans’’, ‘‘Microcystis spp.’’,‘‘Spirulina spp.’’ and others). These organismsare adjusted to this peculiar environment and maybe adversely affected when transferred to oxygen-rich conditions. In addition, their habitat is rich inorganic compounds, the salinity is higher (up tobrackish conditions; see also Pankow 1982 who

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Figure 4. Plate 30 with 7 figures of various aspects of Paulinella chromatophora taken from RobertLauterborn’s original description published in Zeitschrift fur 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), asurface 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).

Paulinella chromatophora and Robert Lauterborn 259

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found P. chromatophora in the shallow bays of theDarss and Zingst in the Southern Baltic Sea; otherspecies of Paulinella, e.g. P. ovalis, have beenfound in the marine environment feeding oncyanobacteria: Hannah et al. 1996; Johnson etal. 1988; Vørs 1993) and often the pH is low. It isapparently difficult to reproduce these conditionsin the laboratory and this may be one of thereasons for the failure to grow some of theorganisms of this community ex situ.

Acknowledgement

DM would like to thank B. Lechner (librarian, Max-Plank-Institute for Limnology, Plon, Germany) forproviding photographs of Robert Lauterborn,which are here reprinted as Figures 1—3.

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