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Sphaerechinus Granularis) FOLIA PARASITOLOGICA 54: 1–12, 2007 Didymium-like myxogastrids (class Mycetozoa) as endocommensals of sea urchins (Sphaerechinus granularis) Iva Dyková1,2, Jiří Lom1, Helena Dvořáková1, Hana Pecková1 and Ivan Fiala1,2 1Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic; 2Faculty of Biological Sciences, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Key words: Didymium-like myxogastrids, Myxogastrea, sea-urchin amoeba strains, SSU rDNA, flagellar apparatus, phylogeny Abstract. This paper sums up the results of light microscopical, ultrastructural and molecular studies of five strains of amoeboid organisms isolated as endocommensals from coelomic fluid of sea urchins, Sphaerechinus granularis (Lamarck), collected in the Adriatic Sea. The organisms are reported as Didymium-like myxogastrids. Of the life-cycle stages, the attached amoeboids, flag- ellated trophozoites, cysts and biflagellated swarmers are described. Formation of fruiting bodies was not observed. Although phylogenetic analyses of SSU rDNA sequences indicated a close relationship with Hyperamoeba dachnaya, our sea-urchin strains have not been assigned to the genus Hyperamoeba Alexeieff, 1923. The presence of either one or two flagella reported in phylogenetically closely related organisms and mutually distant phylogenetic positions of strains declared as representatives of the genus Hyperamoeba justify our approach. Data obtained in this study may be useful in future analyses of relationships of the genera Didymium, Hyperamoeba, Physarum and Pseudodidymium as well as in higher-order phylogeny of Myxogastrea. The interest in amoebic diseases of invertebrates re- able “self-filling” syringes with needles of 23 gauge designed cently renewed by outbreaks associated with mass mor- for bleeding in pigs. Modified malt and yeast extract seawater talities in American lobsters in Long Island Sound, USA agar (MY75S in the Catalogue of the UK National Culture (Mullen et al. 2004, 2005), as well as continuing re- Collection 2001) was used for isolation attempts as well as for search of Amoebic Gill Disease (AGD) in farmed fish, subculturing of primary isolates, strains and clones. The inspired isolation attempts focused on Paramoeba/ strength of artificial seawater (Sea salts Sigma S9883) was Neoparamoeba spp. as potential agents of infections in lowered to 30% and the doses of the extracts to 0.05 g per litre invertebrates including sea urchins. Mass mortalities of in agar used for primary isolations and initial phases of sub- echinoids attributed to Paramoeba invadens Jones, 1985 culturing. When the growth of bacteria, contaminating all infections were reported in the green sea urchin cultures, was balanced, seawater agar with full doses of ex- tracts was used (0.1 g per litre). Cultures were kept at 20ºC. Strongylocentrotus droebachiensis along the Atlantic About 20 passages were executed before the clonal procedure coast of Nova Scotia, Canada, between 1980 and 1983 was completed. Subculturing was done in 10-day intervals. (Jones 1985). Our study was aimed at establishing the identity of isolated Since the number of amoeboid organisms isolated strains. Morphology of cultured trophozoites, excystment and from invertebrates and stored in culture collections is flagellate transformation were studied in hanging drop prepa- rather limited, we have characterized several strains rations using fluid component of the agar medium (30% artifi- isolated from the first set of sea urchins we have sam- cial seawater) and directly in seawater overlay of agar plate pled thus far. None of the isolated strains could be as- cultures. Nomarski differential interference contrast was used signed to Paramoeba/Neoparamoeba species searched to document trophozoites attached to coverslips. (Cultures for; most of isolated strains were mutually similar and with no signs of humidity on the surface of agar, in which interesting enough to be presented in this study. seawater used for subculturing completely soaked into agar, are in this paper termed “dry” cultures). In order to compare obviously inactive trophozoites (as ob- MATERIALS AND METHODS served in agar-plate cultures through Petri dishes), attached Five strains of amoeboid organisms presented in the study cells possessing flagella (as observed in hanging drop prepara- were isolated from 5 out of 34 sea urchins Sphaerechinus tions), and small flagellate cells displaying fast movements, granularis (Lamarck, 1816) screened for the presence of material for transmission electron microscopy was prepared amphizoic amoebae in their coelomic fluid. Strains were under two different conditions: 1) Agar plate cultures were denominated as follows: ECH1, ECH14, ECH43, ECH 49, fixed in situ with cacodylate buffered 2.5% glutaraldehyde, and ECH54. Sea urchins were collected in the Adriatic Sea, in pelleted, postfixed with 1% osmium tetroxide and embedded the nearshore area of the Brać Island (Croatia), in June 2005. in Spurr resin. 2) Agar plate cultures were flooded with 5 ml Sampling of sea urchins was performed using sterile dispos- of 30% seawater and then fixed in two steps at four time inter- Address for correspondence: I. Dyková, Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic. Phone: ++420 387 775 423; Fax: ++420 385 310 388; E-mail: [email protected] 1 vals after their flooding: 5 ml of cacodylate buffered 3% glu- The density of culture increased gradually up to day 10, taraldehyde were added to the culture flooded with seawater when the cysts usually started to outnumber the tropho- and left to work for 15 min. After that, cells were pelleted, zoites. The formation of fruiting bodies was not ob- fixed in 2.5% glutaraldehyde for 15 min and postfixed in 1% served, not even in attempts to culture SUS using me- osmium tetroxide for 45 min. In the course of dehydration, the dium recommended for myxogastrids (Emerson YpSs cells were treated with 1% uranyl acetate dissolved in 75% agar 2% with modified contents of yeast protein and acetone. soluble starch). The procedures for cell harvesting and DNA extraction as Slight but constant difference in the size of tropho- well as conditions of PCR amplification with universal eu- zoites was observed during the long period of subcultur- karyotic primers ERIB1 and ERIB10 and sequencing of ing in one strain (ECH14/I), compared to the remaining cloned PCR products have been described earlier (Dyková et four. The diameter of rounded cysts was 7.5 ± 0.9 µm al. 2005a, b). The composition of SSU rDNA sequences set (strain ECH14/I), 7.7 ± 1.1 µm (ECH 1/I, ECH 43/I and (alignment A) prepared to learn phylogeny of strains under study was based on results of our own comparison of light ECH54/I) and 8.0 ± 1.1 (ECH49/I), respectively. The microscopical and ultrastructural features and data obtained percentage of slightly oval cysts was not significant in from studies of similar organisms (Michel et al. 2003, Walker any of the strains studied. et al. 2003, Walochnik et al. 2004). After initial analysis, a Morphological similarity of the strains as assumed refined dataset consisting of 13 most closely related sequences from observation of agar-plate cultures was confirmed and 3 outgroup sequences was assembled (alignment B). SSU when hanging drop preparations were studied. Contrary rDNA sequences were aligned using Clustal_X program to trophozoites in “dry” agar-plate cultures, those (Thompson et al. 1997). Ambiguously aligned positions in- washed off the agar surface and left to attach to cover- cluding large introns in sequences of Fuligo septica slips possessed flagella (Fig. 1). In addition to the at- (AJ584697), Pseudodidymium cryptomastigophorum tached, large flagellated forms, individual, small flagel- (AY207466), Didymium anellus (AM231292), D. squamulo- lated stages that moved very fast were present in hang- sum (AM231293), D. nigripes (AF239230), D. iridis ing drop preparations. While the number of flagella (AJ938150), D. iridis (AJ938151), D. iridis (AJ938153) and could be easily distinguished in attached cells, the small D. iridis (AJ938154) were removed from analyses. The phy- size and high speed of locomotion of small flagellated logenetic reconstruction of the SSU rDNA sequence data stages did not permit to reveal whether they possessed using methods of maximum parsimony (MP), maximum like- more than one flagellum. The study of changes, induced lihood (ML) and Bayesian inference (BI) followed the practice by adding 30% seawater in seven-week-old culture of applied in previous studies (Dyková et al. 2005a, 2006). MP strain ECH49/I (containing exclusively cysts) repeated (heuristic search with three bisection-reconnection branch three times, revealed details of transformation of the swapping; gaps as missing data; transition/transversion life-cycle stages. A minimum of one third of rounded (Ts:Tv) ratio=1:2; bootstrap statistical support with 1 000 cysts changed their shape into oval within 1 hr after the replications) and ML (GTR+I+Γ model of evolution; bootstrap seawater was added to the culture. Simultaneously, statistical support with 500 replications) analyses were per- formed in the program package PAUP* version 4.0b10 (Swof- conspicuous movements inside these cysts were ob- ford 2001). Bayesian analysis using Markov Chain Monte served. Subsequent liberation of flagellated stages from Carlo
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