Table Of Content

Reference: Biol. Bull. 198: 29-33. (February 2(1(10) Parasitic Diatoms Inside Antarctic Sponges GIORGIO BAVESTRELLO1-*, ATTILIO ARILLO2, BARBARA CALCINAI2. RICCARDO CATTANEO-VIETTI2 CARLO CERRANO2 ELDA GAINO3 . , , ANTONELLA PENNA4 AND MICHELE SARA2 . [stitiito di Science del Mure University di Ancona, Via Brecce Blanche. 1-60131 Ancona. Italy; Dipartimento per lo Studio del Territorio c delle sue Risorse Universita di Geneva, Viale Benedetto XV, 5 1-16132 Genova, Italv; and Dipartimento di Biologia animate ed Ecologia Universita di Perugia, Via Elce di Sotto 1-06123 Perugia, ltal\; and 4lstituto di Biochinu'ca Universita di Urbino. 1-60118. Italv Antarctic sponges may host large populations ofplank- benthic diatoms, and these microorganisms are actively tonic and bentliic diatoms. After settling on the sponge. taken up by the pinacoderm and thus enter the sponge these diatoms enter its body through pinacocytes (1) and choanosome (1). This couldbe an adaptive supplementation form, there, large mono- orpaiici-specific assemblages. Yet of the food supply in the Antarctic ecosystem, because the total amount ofcarbohydrates in the invaded sponge diatoms produce extracellular polysaccharides (8, 9) that tissue is inverselv correlated with that ofchlorophyll-^.. We sponges might use as energy substrates. On the other hand, suggest, therefore, that endobiont diatoms utilise the prod- the integrity ofthe diatom shells, the presence ofcytoplasm ucts ofthe metabolism oftheir host as an energy source. inside the shells, and the formation of large mono- or This is the first evidence indicating that an endobiotic pauci-specific assemblages inside a single sponge suggest autotrophic organism mayparasiti-e its animal host. More- that diatoms are able to complete their entire biological over, this unusualsymbiotic behavior couldbe a successful cycle inside the sponge body. strategy that allows the diatom to survive in darkness. The aim ofthis study was to investigate the energy source Heterotrophic bacteria, autotrophic cyanobacteria, that symbiotic diatoms might provide to Antarctic sponges. zoochlorellae, and zooxanthellae are common symbionts To this end, we evaluated the variation in the total carbo- in Porifera, where they may actually constitute most of hydrate content of sponges as a function of the biomass of the sponge tissue. Sponges can also harbor fungal popu- endobiotic diatoms; biomass was estimated from chloro- lations, the significance of which has been poorly inves- phyll-o concentration. tigated (2). The association of sponges with autotrophic We examined 39 specimens representing 17 species of symbionts occurs mainly in tropical (3) and temperate sponges (Table 1 ). The material wascollectedatTerraNova m waters (4); it is a fruitful strategy, allowing the sponges Bay (Ross Sea), between 100 and 120 depth, during the to utilize the symbionts as a food source complementary XIII Italian Antarctic Expedition (Austral Summer 1997- to filter feeding (5, 6). 1998). The sponges were prepared for ultrastructural study Diatoms in sponge tissues have rarely been recorded (7), as follows. Immediately after collection, small pieces from but such associationsare widespread in Antarctic waters (1 ). each specimen were fixed for 2 h in 2.5% glutaraldehyde in In fact, most sponges from Terra Nova Bay (Ross Sea, artificial seawater (ASW). The fixed tissues were rinsed, Antarctica) host large populations of both plunktonic and stored in ASW, and then dehydrated in a graded series of ethanol concentrations. Critical point drying was achieved R*eTcoeiwvehdom29cJournreesp1o99n9d;enaccecesphtoeudld5bNeoavdedmrbesesred1.99E9-.mail: bavestrellofs1 ewixtahmianedCOw,ithPabaisPhhilCipPsDEM75051a5ppsacraatnunsi.ngSaelmepcltersomiwcerroe- popcsi.unian.it scope, and several species of diatoms were observed (Fig. 29 H 30 G. BAVliSTRKU.O Al.. I..I.I. 1 Chlorophyll-aconcentration andcarbohydratecontentforthesponge specimensanalyzed Chlorophyll-a Total sugars Specimens dwaf) (mg/g d\val) Artemisina rubulosa DIATOMS PARASITIC ON SPONGES 31 Figure 1. Diatoms living inside Antarctic sponges, (a) Several specimensofFragilariopsiscitrta (arrows) and a Fragilariopsis sp. disposed under the exopinacoderm of Tedania charcoti (Scale bar, 50 /j.m (b) Fragilariopsissp.(arrows)embeddedinsidethesamesponge(scalebar. 50jim). (c)LargecentricPorosira sp. (arrows) and numerous pennate Achnanthes sp. (arrow heads) in Pseudosuberites antarcticus (scale bar. 100 /uni). (d) Transmission electron micrograph of Fragilariopsis citrta inside the sponge body showing intact cytoplasm (c) and thylocoid (t) (scale bar, 10 /u,m). s, sponge spicules. facultative heterotrophy. Mixotrophy, a combination of not only by photosynthesis, but also by utilizing organic autotrophy and heterotrophy, is widespread among cer- carbon derived from their host. Although some Antarctic tain protists and, in particular, among flagellates such as diatoms are considered among the most shade-adapted mi- haptophytes (13), dinoflagellates (14, 15, 16, 17), cryp- croalgae (23), the mixotrophy assumed in this report ex- tophytes (18), and diatoms (19, 20, 21). Previous docu- plains the surprising presence of dense diatom populations m mentation of mixotrophy in diatoms was obtained by inside sponges living at 100-120 depth, where the level observations in vitro. of irradiance is very low (24). The relationship between myxotrophic diatoms and Ant- Finally, the mechanism that causes a sponge to actively arctic sponges can be considered as a sort of symbiosis incorporate diatoms is unclear. However, some studies (22) shifting to parasitism: i.e., the algae can get nourishment. have revealed a tendency of demosponges to incorporate 32 G. BAVESTRELLO tT AL Literature ( ited All specimens 5 R2=0,5767 1. Gaino, K.. G. Bu\estrello. R. Cattam-i>-\ii-tti. and M. Sara. 1994. TJ spuming electron microscope evidence tor diatom uptake by two 5" ^1 Antarctic sponges. PolarBid. 14: 1-4. k 15 2. Sara.M..G.Ba\estrello.R.Cattanco-Vivtti.andC.Orrano. 1998. a Endosymbiosis in sponges: relevance for epigenesis and evolution - ~ : Symbiosis 25: 5 o 5 < \\ilkmson.C. R. 1980. Cyanobacteriasymbiotic inmarinesponges. Pp.553-563inEndocytobiology,Endosymhio.ti*mulCellBiology.W. SchwemmlerandH.L:.A.Schenk.eds.WalterDCGruyter.New York. 4 Sara, M. 1971. Ultrastructuralaspectsofthesymbiosisbetweentwo M speciesofthegenusAphanocapsa (Cyanophyceae)andIrcinia \'uria- Dendrilla membranosa bilis. Mar. Bio/. 11: 214-221. zs R2= 0,6736 5. Wilkinson, ('. R. 1983. Nel primary productivity in coral reef 20 sponges. Science 219: 410-412. (>. Arillo, A.,G. Bavcstrello. B. Burlando. and M. Sara. 1983. Met 16 abolic integration between symbiotic cyanohacteria and sponges: a possible mechanism. Mar. Bin/. 117: 159-162. 10 7 Co\. (i.. and \. W. I). I arkuni. 1983. A diatom apparently living in symbiosis with a sponge. Bull. Mar. .Sri. 33: 943-945. E S. Myklestad, S.. (>. llolm-llansen. K. M. \aruin. and B. \olcani. 1989. Rale nt it-lease ofextracellular ammoacids and carbohydrates 20 30 40 50 from Ihe marine diatom Cliiu'innim iilliiin. J. Plankton Res. 11: 20 763-773. Pseudosuberitesnudus 9. Mykk-st.id. S. 1995. Release ol extracellular products by phyto- Di 16 R2= 0,7157 planktonwithspecialemphasisonpohsacchandcs .SVi. Tnhill-jn-iron. O) 165: 155-164. Hi. llfllfhusl, .1. A., and .1. I.ein. 1997. Heterotrophic nutrition I'p 10 169 197 in The Bitilngy ofDiatoms. D. Werner, ed. University of 01 California Cress. Berkeley. I 5 II. While. A. \\. 1974. Growthof2facultativelyheterotrophii marine centri< diatoms / /'/,i,,./. Id: 242-300. 12 I.ein.,|. ('..and.1. A. Helli-hust. 1976. Heterotrophic nutrition of 10 20 30 40 5Q maniK- peiinau- ihaiom Nilzschioangularis\rar. a/finis. Mar. Biol. 36: 313 ^20. Chlorophyll-a (pg/g dwaf) 13. I illin.iiiii. I'. 1998. Chagotrophy by a plastidic haptophyte. Prym- 2. Concentration ofchl-o as a function of Ihe total annum! ul nesiutnpatellifemm, Ai/tmt \liti<>h. /-(</. 14: Iss Uto carbohydrate. Datafromallthespongespecimenstestedla), fromditu-u-m 14 i.1.mi Ir K., I). M. Anderson. P. Carlsson. and S. V. Muestrini. specimensofDendrillamembranosa(b),and from Pseudosuberites nu,ln\ 1997. Lightandcarbon uptake by Dinonhysisspecies incomparison (C). Each point represents a sponyc specimen The analyses \\crc tamed to oilier pliotosyntlielic and lietcrotrophit dinotlagellutes. Ai/uat. Mi- out on three samples ofsponge tissue inmi eat h specimen. Samples were cn>h. !:,,>!. 13: 177 IS6 cylindricalcoresofchoanosomal tissue. I cm in diametei. 2 cm in height. 15 Lcyrand. ('., K. (iraiu-li. and P. Carlsson. 1998. Induced phago- Cores were longitudinally cut. and the two hall pmiiiiiis weie lesied to tiophy in the photosynthetic dinoflagellate Heterocapsa iriqueini. evaluate the chl-i; concentration (as an estimate ol diatom population \,/ii,ii \h, rob Ecol 15: 65-75. bioma.ss).aswell asthetotal amount ot taibuln.li.iii- ( im- Mibsample was lii Skn>Kiiiird. \. 1996. \li\oiiophy in Fragiliiliiun siihglohosum IDi- extracted in 90% acetone. The chl-rt was then assayed by speclrolluonm- noph\ceael: growth and gra/ing responses as functions oflight inten- etry with excitation at 43(1 nm and emission nic.i m >l al i'iiS nm. On ilk- sitj Wai B ol Prog Sei 143: M7-253. obatanhsdeerdD(os+unb)tshgaelmupcclooels.oentmwheaetsrtiouctsareledaccaatsribotonhheoyldsrtsaautngedasairsdwwe(rH2eh6).pahsseanyoeld:andthseulmpehtuhriocdaewiads. 17. odIifiaml.oaInrNiIinsepIu's.n,n;'oawnhdalonMod.mt.hKiepiihrloyeltieoipsotlfiaihn'ekrttneaor.not1sr9po9ep6ch.iiecsdCitunooomfwploiasgheilialinaodtne.sd.eclJlo.innIne'altouinfokn-a t,m Ki's. 18: 133-155. I (,cr\ais. !. 1997. Light dependent growth, dark survival and glu- coseuptakebycryptophytes isolated fromafreshwaterchemocline./ siliceous particles, and the diatoms, with their siliceous Phycol 33: is 25. shells, may thus "deceive" the sponge. I" V/ani. I., and I!. 1. \iilcani. 1974. kulr nl silico..... diaioin In conclusion, ourdala widen the ecological role ofdiatoms metabolism VI. Active transport ofgermanic acid in thehelerotrophic which, by exploiting the niche ptmidcd In sponges une ol M dhiaartlocym.N\iVl.zfMc.hi,oBt.ilhBt.i.\A\ricmh.peMei.craonbdiolC.. 1I0.1O:li1lmSa.n. 1981. lletero- (he most important Antarctic henthic organisms illusiiate .1 trophic and pliotohclerolrophic utili/alion of lactate by the diatom strong functional link between plankton and benthos (25). CylimJmthecafusifiirmn. Hi. I'ltycul. ./. 16: 423-428. DIATOMS PARASITIC ON SPONGES 33 21. Tan, C. K., and M. R. Johns. 1996. Screening of diatoms for 24. Vanucci,S.,and M. Innamorati. 1997. Availableradiationprofiles heterotrophic eicosapentaenoic acid production. J. Appl. Phycol. 8: recorded in the Ross Sea. Pp. 2X1-290 in Rossmi;e /W-95 Data 59-64. ReportI. F. M. Faranda. L. Guglielmo and P. Povero. eds. Lang Arti 22. Bavestrello, G., A. Arillo, U. Benatti. C. Cerrano, R. Cattaneo- Grafiche. Genoa. Italy. Vietti,L.Cortesogno,L.Gaggero,M.Giovine,M.Tonetti,and M. 25. Marcus, N. H., and F. Boero. 1998. The importance of benthic- Sara. 1995. QuartzdissolutionbythespongeChondrosiareniforinis pelagic coupling and the forgotten role of the life cycles in coastal (Porifera, Demospongiae). Nalnir 378: 374-378. aquatic systems. Linmol. Oceanogr. 43: 763-768. 23 Palmisano, A. C., J. B. SooHoo, D. C. White, G. A. Smith, G. R. 26 Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Stantun, and R. H. Burckli'. 1985. Shade-adapted benthic diatoms Smith. 1956. Colorimetric method of determination of sugars and beneath Antarctic sea ice. J. Pliviol. 21: 664-667. related substances. Anal. Clu'iii. 28: 350-356.