Michael J. Miille Abstract Uptake of Amino Acids by Metridium senile ABSTRACT 1. Metridium senile incorporated between 30% and 60% of the 7C-labeled glysine, valine, glutamic acid, lysine, and an algal mixture when they were present at natural concentrations. 33% of the glysine and 66% of the glutamic acid incorporated by the anemone was metabolized to C0.. This could account for 12% to 24% of the animals total CO, pbduction. The rates of release for glysine and glutamic acid are calculated. There is a net loss of glysine and a net uptake of glutamic acid by the anemone. In starved versus fed anemones, the starved animals take up glysine and produce 1700, in significantly higher amounts. The advantage of this to Metridium senile is discussed. Michael J. Miille Page 2 Uptake of Amino Acids by Metridium senile INTRODUCTION Since the early 1960's many marine organisms have been shown to take up dissolved organics such as amino acids and glucose. Stephens gives a good summary of this work (Stephens 1968) and concludes that it can be energetically significant to the animal. The major work on coelenterates has been done over the past 4 years by Schlichter on Anemonia sulcata. He has found that there is active uptake of the amino acids from sea water, that this uptake is through the ectoderm, and suggests that the animal could satisfy much of their energy requirements in this way (Schlichter, 1974). However, it still remains to be demonstrated that there is a net uptake of amino acids, and the amounts which are removed from sea water are nutritionally significant. The animal used in the study reported here was Metridium senile, (Linnaeas, 1767) collected in Monterey Bay from an area of high dissolved organic content, little water movement necessary for particle feeding, and therefore, from a situation in which direct uptake of dissolved organics would be a benefit Michael J. Miille Page 3 Uptake in Amino Acids by Metridium senile to the animal. These anemones were used to measure uptake, and release of amino acids, and the contribution of such materials to C02 production by fed and starved animals. MATERIALS AND METHODS Metridium senile were maintained in the laboratory in running water. They were fed squid every three days prior to use. Animals weighing approximately 2 grams were placed in a 250 ml. Erlenmeyer flask with 100 ml. of filtered sea water and allowed to settle 24 hours prior to the start of an experiment. Filtered instant ocean containing 170-labeled amino acids or glucose at concentrations found in coastal waters were used, i.e. 60/m/1 for amino acids (Clark, Jackson, North, 1972) and 804g/1 for glucose (Riley, Chau, 1970). These preparations were maintained at 11 to 12 C. The decrease in dissolved organic material was measured by removing iml. samples from the flask after thorough mixing by transfer to a scintillation vial. 1002 was removed by the addition of IN H»SO4. One hour was allowed for the loss of volatile 0 before restoring the Page Michael J. Miille Uptake of Amino Acids by Metridium senile origidnal pH by addition of IN NaoH prior to the addition of New England Nuclear Aquasol and counting. To measure the amounts of 1700, given off by the animal, a 50ml. Erlenmeyer flask stoppered with Top stoppers, K-882310, fitted with plastic center wells, K-882320, both from Kontes Glass Co. Viveland, N.J. was used as a trap. The well contained a filter paper wick wet with .15 ml. of ß-phenalethylamine. Two 1002 was ml. samples were used in these determinations. released by lowering the pH with the addition of IN H,SO). This system was allowed to stand for 24 hours before removal of the wick for counting. Gaseous 100, released by the animal during incubation was trapped and measured in a similar way. Samples were counted using a Nuclear-Chicago Unilux II scintillation counter. RESULTS Uptake The following materials at sea water concentrations were studied: glucose, imCi/12mg; lysine, 312 mCi/mmole; valine, Michael J. Miille Page 5 Uptake of Amino Acids by Metridium senile 260 mCi/m mole; glutamic acid.1 mCi/27mg; glysine, .imCi/7.2 mg; and New England Nuclears Amino Acid -70 (u.1.) Mixture, which contains amino acids present in the same relative proportions as found in a typical algal protein hydrolysate..Each ofthese materials was tested for rates of uptake on two separate animals. At the end of 12 hours exposure to the 70-labeled materials, the animal was dried, weighed, and ground in a mortar before extraction with 5 ml. of 70% ethanol for 24 hours to obtain free amino acids and other extractable substances. An additional 5 ml. of ethanol was added and the mixture centrifuged at 2,000 r.p.m.'s. A sample of both the supernatent and insoluble residue wascounted. The results are shown in Table #1. C0,, alcohol soluble, and insoluble portions are expressed as percent of the total 'C taken up. Figure l shows the rates of uptake over the entire 12 hours. Uptake for the first 2 hours is linear. Also, 20%-50% of the amino acids taken up were metabolized to C0.. were selected Glysine and glutamic acidfor further study because of the difference in their conversion to C0, and incorporation into the amino acid pools. Michael J. Miille Page 6 Uptake of Amino Acid by Metridium senile Bacterial Affects on Uptake The contribution to catabolism by bacteria associated with the anemone was assessed by observing uptake and conversion to CO, in the presence and absence of Streptomyocin at a concentratio of 50/g/ml. Uptake by 5 different animals in the presence of this antibiotic was compared with the uptake by 5 animals in the absence of the bacteristatic substance. Incubation was for only Whours. The results are presented in Table f2. Streptomyocin had no significant affect on the amount of C-labeled amino acids taken up or catabolized. In this experiment which utilized a larger number of animals, a correlation between body weight and percent uptake, r-.85, p.01, was observed and permitted percent uptake to be expressed in terms of the gram dry weight of the anemone. Note that almost twice as much glutamic acid was converted to labeled CO, as glysine. To further substantiate the minimal involement in the effects observed, 4canemones were shaken in 50ml. of sea water to release bacteria attached to their outer surfaces.. The anemone was then removed, labeled glysine and glutamic acid added, and the decrease in specific activity measuredover 24 hours. Results are shown in Table f3. During the first 4 hours bacteria had little affect Michael J. Miille Page 7 Uptake in Amino Acids by Metridium senile on the amount of labeled material removed from solution. After reult 24 hours in the presence of streptomyocin a similiar/was found. In the absence of the antibiotic a significant affect apparently due to bacteria, was observed. Release of Amino Acids from Metridium senile In this experiment six animals, described in Table #2, were incubated in the labeled substrate solutions for 4 days to permit equilibration of labeled and unlabeled amino acids in the animals tissue. At the end of this period the animal was washed four times in sea water and then placed in 100ml. of filtered sea water. The release rates of labeled material were then measured as a function of the increase in non-CO, carbon-14 in the sea water. At the end of the experiment the anemones were extracted i in 70% ethanol, and the levels of 170 -labeled amino acids determined. The results are shown in Table #4. The anemone exhibits a net release of glysine over the 4 hour period, and a net uptake of glutamic acid. Uptake in Fed versus Starved Anemones Ten Metridium senile, varying in weight by no more than .2 grams wet weight, were collected from the same clone. They were placed in beakers and maintained in running filtered sea water for two weeks. During the following two weeks, only 5 of the 10 Michael J. Miille Page 8 Uptake of Amino Acids by Metridium senile were fed squid three times a week. At the end of this period, all ten were put in 10ml. of 170-labeled gylsine, and uptake and CO, release were measured as before. The results are shown in Table #5. The difference in results was assessed significant. In both cases the starved animals removed amino acids and catabolized them at a significantly higher rate, p(.05, p(.Ol respectively. DISCUSSION The results of the experiments performed indicate that Metridium senile is capable of absorbing amino acids and glucose from sea water at natural concentrations. The rates of uptake are similar to those found by Schlichter an Anemonia sculcata (Schlichter, 1974). The figures show that uptake is linear for the first two hours, followed by a leveling off to a final concentration. One possible explanation for the results is that a minimum concentration was reached, below which the animal could no longer absorb the amino acids. These minimal values range from 1.2 x 10"' moles/liter for valine to 6.9 x 10 moles/li Page 9 Michael J. Miille Uptake of Amino Acids by Metridium senile for glysine. These results can be explained by the reports that uptake rates exhibit enzyme kinetics. (Taylor, 1969; Shick, 1975; Stephens 1963). The observed uptake of amino acids and conversion to CO, cannot be attributed to bacteria because of the high uptake rates in the presence of streptomyocin. Twice as much of the incorporated glutamic acid was converted to C02 as compared to glysine. To compare the 10,/ 1200, ratio in the animal, and determine the nutritional contributions of dissolved glysine and glutamic acid, the CO, excretion values for Metridium as determined by Parker were used. (Parker, 1923). This shows glysine could account for 12.5% of the animals CO, and glutamic acid 24.4%. These values suggest that dissolved organics may account for substantial amounts of the anemone's nutrition in some situations. The release rates from the anemone were calculated for glysine and glutamic acid following the guidelines established by Johonnes, Coward, and Webb, (1969). A net release of glysine was found, while there was a net uptake of glutamic acid. This is energetically resonable if one compares the amounts which are used in metabolism, and it demonstrates the same results which Ferguson found in starfish (1971). Because of the high concentratio gradient, 102:1, the uptake of glutamic acid may be explained Michael J. Miille Page 10 Uptake of Amino Acids by Metridium senile by active transport, as found by Schlichter (1974). The increased utilization of dissolved amino acids by starved Metridium was demonstrated, showing the possible selective advantage to uptake of dissolved organics during food deprivation. A similar increase in 00, production by starved Aurelia aurita was shown by Shick (1975), who reached the same conclusion. One possible explanation for this result would be a difference in the freedamino acid pools of fed and starved animals. However, in the same experiment, Shick (1975) showed that the total free amino acid poncentration in the pools is little affected by starvation, supporting the theory that increased uptake is a response to starvation. The possible importance of dissolved organics to Metridium senile has been demonstrated by this study. However, no conclusive statement as to their quantitative contribution to the animals nutrition can be made until the 100,/1200, ratio for an animal over a long period of time has been measured. Further studies of this aspect are anticipated. Page 11 Michael J. Miille Uptake of Amino Acids by Metridium senile ACKNOWLEDGMENTS Iwould like to express my sincere thanks to the faculty and staff of Hopkins Marine Station, especially to Dr. John Phillips and Dr. Robin Burnett for their advice during this study and assistance in preparing this paper. My thanks also to Susan Ball for typing this paper and to Kim Suelzle and Carol Rodgers for their assistance in running two of the experiments. Michael J. Miille Page 12 Uptake of Amino Acids by Metridium senile LITERATURE CITED Chau, Y. K., J. P. Riley 1970. Amino acid concentration found in sea water. Deep Sea Res. 13:1115-1121 Clark, M. E.; G. A. Jackson, and W. J. North Dissolved Free Amino acids in Southern California Coastal Waters. Limnol. & Ocean. 17(5):749-756 Ferguson, J. C. 117 Uptake and release of free amino acids by starfish. Bio. Bull. 141:122-129 Johannes, R. E., S. J. Coward, K. L. Webb 1969 Are dissolved amino acids an energy sourde for marine invertebrates? Comp. Biochem. Physiol. 29:283-288 Schlichter, D. 1274 The influence of physical and chemical factors on the uptake by Actinians of amino acids dissolved in sea water. Mar. Biol. 25:279-290 Shick, M. J. 1475 Uptake and utilization of dissolved organics by Aurelia aurita scyphistomae: temperature effects on the uptake process; nutritional role of dissolved Amino acids. Bio. Bull. 148:117-140 Parker, G. H. 723 he excretion ot cnbon dioxide sy velaxes contracted sen anemones. J. 6en, Physiol. S: 45-64. Page 13 Michael J. Miille Uptake of Amino Acids by Metridium senile Stephens, G. 1963 Uptake of Organic Molecules by Aquatic Inverts.- II. Accumulation of amino acids by the bamboo worm, Clymenella Torquata. Comp. Biochem. Physiol. 10:191-202 Stephens, G. 1968 Dissolved organic matter as a source of nutrition for marine organisms. Am. Zoo. 8:95-106 Taylor, A. G. 1969 The direct uptake of amino acids and other smallmolecules from sea water by Neres virens sars. Comp. Biochem. Physiol. 29:243-250 Michael J. Miille Page /4 Uptake of Amino Acids by Metridium senile Figure Caption Decrease in the counts-per-minute of a given substrate Fig. 1. during the experimental period. Each point represents the counts in 1 ml. of solution. Circled numbers correspond to the animals number in Table f1. Michael J. Miille Page 15 Uptake of Amino Acids by Metridium senile Table Captions Percent uptake (calculated as nitial - final g.p.M.) Table 1. initial and distribution of 10-labeled materials in Metridium senile. Distribution of the 170 is given as percent of total incorporated 170. Table 2. Percent uptake and 1002 production by Metridium senile in solutions with C-labeled glysine and glutamic acid, with and without an antibiotic present. Table 3. Percent uptake of 1C-labeled glysine and glutamic acid by bacteria, with and without an antibiote present. Table 4. Net movement of glysine and glutamic acid is calculated by determing the total uptake to total release ratio. All values for uptake, release, 170. Amino acids, and total amino acids are given in mMol/gm. dry wt. Percent uptake of glysine and 100, production Table 5. is shown for fed and starved Metridium senile. Michael J. Miille Uptake of Amino Acids by Metridium senile TABLE f1 % Alcohol % Alcohol Substrate Soluble % Uptake % C02 Insoluble 41.5 27.3 8.3 Glucose 1 3.1 44.3 1.6 Glucose 2 25.9 2.5 44.4 20.8 26.0 Lysine 1 1.3 2.6 27.0 22.7 Lysine 2 31.4 29.4 Valine 1 34.4 38.0 2.3 46.0 Valine 2 42.0 7.1 29.7 3.4 Glutamic acid 1 75.0 22.0 38.6 53.0 Glutamic acid 2 39.2 25.0 9.3 49.0 Glysine 1 67.0 6.5 12.5 Glysine 2 49.5 7.0 67.0 37.0 33.4 Algal mix 1 57.0 22.6 5.1 2.5 Algal mix 2 20.6 39.1 30.0 Michael J. Miille Uptake of Amino Acids by Metridium senile TABLE #2 Substrate Weight % Uptake (grams) Glysine 1 33.8 .72 38.4 .90 10 3 32.8 .71 29.3 .85 29.7 .47 X =32.8 Glysine + Strept. 1 37.0 52.9 13.2 1.07 27.9 .60 -31.9 X=38.4 Glutamic Acid 1 44.1 1.78 39.0 1:65 39.0 1.60 44.7 1.80 31.8 1.20 X=39./ Glutamic acid+ 46.3 Streptomyocin 41.6 29.1 36.5 1.36 49.3 1.12 6-40.5 Kused for mensure ofrat of relense. men 7002 Percent of Total Uptake 33 41 34 30 67 68 62 Michael J. Miille Uptake of Amino Acids by Metridium senile TABLE #3 % Uptake Substrate L hours 0.6 Glysine Glysine + Streptomyocin 1.1 Glutamic acid 1.8 Glutamic acid + Streptomyocin 0.6 % Uptake 24 hours 24.0 1.3 37.0 2.6 0 Qo- + + 0 O 8 5 5 0 3 5 ON — ON N 8 3 oo 21 a S O 5 8 O 5 N S —5 o 80 — 0 X 9 10 5 55 2. o la 5 Michael J. Miille Uptake of Amino Acids by Metridium senile TABLE 15 % Uptake Anemone of Glysine 24.6 Non-fed 1 35.4 32.8 3 36.3 33.6 30.5 Mean 27.2 Fed 24.7 25.6 3 24.8 21.2 24.7 Mean 1002 Percent of Total Uptake 56.9 58.2 49.6 55.8 60.4 56.2 44.4 40.9 43.4 15.5 44.1 43.7 e Michael S. mitte Uptnke of Amino Heid by Meteidium sente 100 22o,00 looc 2og Glucose 000 oo Tizood 0000 10.000 140,000 6000 120,000 Tme Goas) loc oo 10,000 000 oo,o00 400 Valine. Eo000 500 Oo,000 700 00 O 70,000 1000 4 2 6 Tme (houzs) 2o 3400 300 270 Glysine 2000 99000 330000 E22oo 500 210,000 60 1400 140000 1000 o 2 — Fioage 21 LySINE — Time (hoans) Glufmic Heid O àp Choues) Time Algal Mixtuge 10 72.