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Release of Dissolved Amino Acids by Flagellates and Ciliates Grazing on Bacteria

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Release of Dissolved Amino Acids by Flagellates and Ciliates Grazing on Bacteria OCEANOLOGICA ACTA - VOL. 21 - No3 J Release of dissolved amino acids by flagellates and ciliates grazing on bacteria Christine FERRIE:R-PAGlb a, Markus KARNER b, Fereidoun RASSOULZADEGAN ’ a Observatoire Oceanologique Europeen, Centre Scientifique de Monaco, avenue Saint-Martin, MC-98000 Monaco, Principaute de Monaco bUniversity of Hawaii, SOEST Dept. Oceanography, 1000 Pope Road, Honolulu, Hawaii 96822, USA ‘Observatoire OcCa.nologique, URA-CNRS 716, Station Zoologique, BP 28,06230 Villefranche-sur-Mer, France (Received 25/01/97, revised 21/08/97, accepted 29108197) Abstract - Release of amino acids was examined in the laboratory in the form of dissolved primary amine (DPA) by two marine planktonic protozoa (the oligotrichous ciliate, Strombidium sulcatum and the aplastidic flagellate Pseudobodo sp.) grazing on bacteria. DPA release rates were high (19-25 x 1O-6 and 1.8-2.3 x 10m6pmol DPA cell-’ h-l for flagellates and ciliates, respectively) during the exponential phase, when the ingestion rates were maximum. Release rates were lower during the other growth phases. The release of DPA accounted for 10 % (flagellates) and 16 % (ciliates) of the total nitro- gen ingested. Our data suggest that the release of DPA by protozoa could play an important role in supporting bacterial and ‘consequently autotrophic pica- and nanoplankton growth, especially in oligotrophic waters, where the release of phyto- planktonic dissolved organic matter is low. 0 Elsevier, Paris amino acids / protozoa / excretion rates I dissolved organic matter RCsumC - ExcrCtion d’acides amin& par des ciliCs et des flagell&s. Les taux d’excretion d’acides amines par deux pro- tozoaires planctoniques marins (un cilie oligotriche, Strombidium sulcatum, et un flagelle heterotrophe, Pseudobodo sp.), nourris avec des batteries inactivees (par choc de temperature) ont etC quantifies exptrimentalement. Les valeurs maxi- males sont mesurees en debut de phase exponentielle et sont comprises entre 19 et 25 x 10m6pmolcellule-‘K’ pour les fla- gel&, entre I,8 et 2,3 x 10v6 ymolcellule~‘X’ pour les cilits. Elles correspondent aux valeurs maximales des taux d’ingestion. Les flagelles et cilits excretent au maximum 10 et 16 % de l’azote ingCrC sous forme d’acides amints. Les aci- des amines provenant des protozoaires pourraient jouer un role important dans la croissance des batteries et du pica- et nanoplancton autotrophe, notamment dans les milieux oligotrophes ou l’excretion phytoplanctonique de mat&e organique dissoute est faible. 0 Elsevier, Paris acides amin& I protozoaires I taux d’excrktion I mati&e organique dissoute 1. INTRODUCTION protozoa are still !jcarce and conflicting. Some authors reported high release rates [2, 26, 341 whereas others esti- It is now clear from recent studies that protozoa (both cil- mated that this release is negligible [3, 9, 121. Protozoa iates and phagotrophic flagellates) regenerate ammo- can also take up clolloidal DOM, when it is available in nium and phosphorus in significant quantities while the medium [13, 15, 36, 381. grazing [l, 10, 121. It has been suggested that they can also release dissolved organic matter (DOM) [16, 19, 25, The bulk of the DOM pool is composed of complex and 26, 3.5, 391. However, data on release rates of DOM by refractory material, but a significant proportion includes Oceanologica Acta 0399 1784/98/03/O Elsevier, Paris 485 C. FERRIER-PAGl% et al. biologicaiIy active organic compounds such as dissolved during control experiments to measure the bacterial free amino acids (DFAA). DFAA play an important role release of dissolved primary amine (DPA). in oceanic waters since they are quickly taken up by het- All cultures were simultaneously run in triplicate, with erotrophic bacteria [14, 321. Hollibaugh et al. [17] samples taken once or twice a day from each culture to showed a rapid turnover of the DFAA pool in enclosed determine protozoan and bacterial abundances as well as water column, which suggested high DFAA release rates DPA concentrations. Ciliates were fixed using a Lugol’s in sea water. Release of DFAA by phytoplankton and solution (2 % vol/vol final concentration) and counted macrozooplankton has been well studied [4, 6, 221, but with an inverted Zeiss microscope. Heterotrophic bacte- few studies investigated DFAA release rates by flagel- ria and flagellates were preserved with borax-buffered lates [3, 24,251 and very little information is available on formaldehyde (0.3 % vol/vol final concentration), stained ciliates [16, 39]. with DAPI [27], and counted with a Zeiss Axiophot epif- The objective of the present study is to investigate the luorescence microscope. DPA bulk concentrations were role of ciliates and flagellates as a source of dissolved determined using a Spex spectrofluorimeter and a fluoro- free amino acids in the sea. The release of amino acids (in genie reagent (o-phthalaldehyde) according to Strickland the dissolved primary amine form, DPA) by two protozoa and Parsons [33]. Fluorescence produced by the OPA- (a flagellate and a ciliate) was therefore measured. ammonium complex has been subtracted from total fluo- rescence. In order to avoid an increase in DPA concentra- tions due to cell disruption, samples were prefiltered: 2. MATERIAL AND METHODS 1) through 0.1 urn Millipore filters at 5 70 mm.Hg (0.1 bar) vacuum in the flagellate experiment; greater Experiments were performed with the oligotrichous cili- pore size filters may have induced high linear water ate, Strombidium sulcatum, and the heterotrophic velocities and high shear [l 11; moreover, gentle vacuum nanoflagellate, Pseudobodo sp., fed with either live or filtration (<70 mm.Hg) has a minor effect on DFAA heat-killed bacteria. Protozoa were both isolated from the concentrations 1241; 2) through syringe filtration using North-West Mediterranean Sea and grown on a mixed Acrodisc (Gelman) in the ciliate experiment, according to bacterial assemblage as prey [28]. Cultures were incu- Nagata and Kirchman [24]. Disc filters are indeed more bated in darkness at 12 “C. Heat-killed bacteria were pre- adapted to ciliates than classical membrane filtration pared as described by Sherr et al. [31]: a mixed bacterial units because ciliates are structurally less rigid and more assemblage was harvested in the stationary growth phase susceptible to breakage during filtration than flagellates. and heated for 4 h at 60 “C until no enzyme activity (ami- We observed no significant filtration damage due to cell nopeptidase and glucosidase, measured by spectroflo- rupture: this would have increased DPA concentration rometry) could be detected in the incubation medium. with increasing protozoan number. The heat-killed bacteria were filtered through a 4 pm Protozoan growth rate (p, h-l) was obtained as follows: Nuclepore membrane to remove bacterial aggregates and stirred for 10 min. These suspensions were then used as a p = (In C, - In C&t, - to) (1: food source at a final concentration of ca. 2 x lo7 cell.mL-‘. Two sets of bacterial suspensions (heat-killed where C, and C, are the ciliate or flagellate concentra- and live bacteria) were used in flagellate experiments. tions (cell mL-‘) at the beginning (to) and the end (ti) of Only heat-killed bacteria were used in ciliate experi- the incubation time (h). ments. Ciliates and flagellates were inoculated into the bacterial media at a final concentration of ca. 1 and IO3 DPA release rates by protozoa (RR, pmol protozoa-’ h-r) cell.mL-‘, respectively. Both flagellates and ciliates were were estimated for bottles containing heat-killed or live previously grown on heat-killed bacteria, in order to bacteria as follows : avoid the carry-over of live bacteria. According to Landry et al. [21], flagellates selectively graze live bacteria com- R, = (DPA, - DPA,) / [C . (t, - to)] (21 pared to heat-killed ones. Therefore, after sub-culturing protozoa in heat-killed bacteria for several generations, where DPA, and DPA, are the dissolved primary amine contamination by live bacteria was assumed to be mini- concentrations (PM) at the beginning (ts) and the end (tr) mal. Bacteria (heat-killed and live) were also incubated of incubation (h). C (cell mL-t) is the average concentra- 486 AMINO ACID RELEASE BY PROTOZOA tion of protozoa during incubation which was defined maximal during the exponential phase (2 to 4 x 1O-5 pmol assuming exponential growth : N cell--’ h-‘,$gure lb) when the bacterial food was still abundant. DPA concentrations varied from 0 to 2.5 pM C = (Cl - Co) / (lnCI - lnC,) (3) from the beginning to the end of the incubation cfigure la). Maximum DPA release rates occured during In the ‘live bacteria’ vessels, release rates (R,) repre- the lag and early exponential phase and varied from sented ‘net’ rates (i.e. the difference between protozoan 1.80 to 2.30 x lo4 pmol N cell-’ h-’ figure 2). These excretion and bacterial uptake). In the vessels containing rates were lower at the end of the exponential growth heat-killed bacteria, these rates (R,,,) should represent phase (0.02 to 0.1 lo4 ymol N cell-’ h-l) and dropped actual protozoan release rates. during the stationary phase (2 x lo-’ to 0.9 x 1O-9 pmol Protozoan specific nitrogen ingestion rates were calcu- cell-’ h-l). lated as follows : I, = QN . (B, -B,Y [C 01 - to)1 (4) 3.2. Flagellate experiment Flagellates exhibited growth patterns similar to those where: I,, is the particulate organic nitrogen ingestion rate obtained for ciliates (figure 3, 4~). When fed heat-killed (ymol N protozoa-’ h-l); QN is the bacterial nitrogen cell bacteria, flagellates exhibited a lag but no stationary quota (pm01 N cell-‘); B, and B, are the bacterial concen- phase and their concentrations sharply decreased after the trations (cell mL-‘) at the beginning (to) and at the end peak (figure 3a). However, the highest concentrations (tl) of the incubation (h). The N content of heat-killed were similar in live and heat-killed bacterial cultures (ca.
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