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A Laboratory Study on Digestive Processes in the Antarctic Krill, Euphausia Superba, with Special Regard to Chitinolytic Enzymes

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A Laboratory Study on Digestive Processes in the Antarctic Krill, Euphausia Superba, with Special Regard to Chitinolytic Enzymes Polar Biol (1999) 21: 295±304 Ó Springer-Verlag 1999 ORIGINAL PAPER Reinhard Saborowski á Friedrich Buchholz A laboratory study on digestive processes in the Antarctic krill, Euphausia superba, with special regard to chitinolytic enzymes Accepted: 4 October 1998 Abstract Feeding experiments of 9, 14 and 20 days Sayed and Weber 1982) and, potentially, E. superba can duration were carried out on the Antarctic krill, Eu- also change to carnivorous feeding at low phytoplank- phausia superba. Two groups were fed with the chitinous ton densities or during the Antarctic winter (Price et al. diatom Cyclotella cryptica and the non-chitinous green 1988; Lancraft et al. 1991; Huntley et al. 1994; Atkinson algae Dunaliella bioculata, respectively. A control group and SnyÈ der 1997; Pakhomov et al. 1997). Krill are able remained unfed. The time courses of the activities of to graze on patchy food sources very eciently (Hamner endo- and exochitinase in the stomach and the midgut et al. 1983). Appropriate activity levels of digestive en- gland were compared with those of the digestive en- zymes are a prerequisite to ensure rapid digestion and zymes protease, cellulase (1,4-b-D-glucanase) and lami- resorption under a variable food regime. narinase (1,3-b-D-glucanase). Speci®c activities of all In addition to several glucanases and proteases enzymes were higher in the stomach than in the midgut (Mayzaud et al. 1985; McConville et al. 1986), high gland. Characteristic time courses of activity were evi- activities of endo-chitinase (poly-b-1,4-(2-acetamido- dent after 4 days. In starved animals, enzyme activities 2-deoxy)-D-glucosid-glucanohydrolase) and N-acetyl-b- decreased to a minimum after 4 days and recovered D-glucosaminidase (here NAGase) have been found in within 14 days to initial values. In the stomach, the ac- the digestive tract of krill (Buchholz 1989). Both en- tivities of endo- and exochitinase increased when krill zymes are also present in the integument, where they were fed on Cyclotella. For animals fed with Dunaliella, show moult-related patterns of activity (Buchholz and activities stayed constant or decreased slightly. The re- Buchholz 1989). In the stomach and the midgut gland sults con®rm chitinases as digestive enzymes and, (hepatopancreas), however, the activities are not aected therefore, the capability of krill to utilize various food by the moult cycle. Previous ®eld investigations support sources. the hypothesis of a digestive function of both enzymes (Buchholz and Saborowski 1996). Chitin consists of amino sugars and is, therefore, of considerable nutritive value. Diatoms of the genus Introduction Thalassiosira contain substantial amounts of chitin as ``spines'' (McLachlan et al. 1965) and at certain times The Antarctic ocean is an extreme environment and can dominate the Antarctic phytoplankton (Johansen organisms living there require biological specializations and Fryxell 1985; V. Smetacek, personal communica- and, particularly, physiological and biochemical adap- tion). Krill could, therefore, make use of this rich food tations. An important organism in the Antarctic eco- source, and the presence of a set of readily available system is the Antarctic krill, Euphausia superba. Krill enzymes would enhance their physiological capability. A represent the main food source for predators such as possible induction of the chitinases, similar to that re- whales, seals and birds. As ®lter feeders, krill feed ported for other enzymes (Mayzaud and Conover 1976; mainly on phytoplankton. Primary production in Ant- Cox and Willason 1981), would demonstrate their rela- arctic waters is, however, characterized by high seasonal tion to the food supply, and identify them as digestive and spatial variation (El-Sayed and Taguchi 1981; El- enzymes. The aim of the present work was to study the re- R. Saborowski (&) á F. Buchholz sponse of chitinases in the krill's digestive organs to Biologische Anstalt Helgoland-AWI, Meeresstation, D-27483 Helgoland, Germany dierent feeding conditions in comparison to various e-mail: [email protected], typical digestive enzymes. The protocol included feeding Tel.: +49-4725-819326, Fax: +49-4725-819369 chitinous and non-chitinous algae, respectively. The 296 activity patterns of the chitinases were investigated in assayed for amino sugars according to Morgan and Elson (1934), relation to protease, cellulase, laminarinase, gut fullness modi®ed by Saborowski et al. (1993). Blanks were run in parallel as and the gross composition of the diet. The results are well as standards containing puri®ed chitin (Sigma C-3641). discussed in relation to the digestion physiology of krill and Antarctic ecological conditions. Collection of krill Antarctic krill, E. superba, were caught north of the Antarctic Materials and methods peninsula during the cruise Met 11/4 (21 December 1989 to 18 January 1990). Sampling was carried out with a Bongo net (2 ´ 63 cm, mesh width 320 lm) near Elephant Island (60 °S57.75 Phytoplankton cultures 27 °W07.50) and a Rectangular Midwater Trawl, RMT 1 + 8 (Roe and Shale 1979) near King George Island (62 °S05.95 Strains of the chitinous diatom Cyclotella cryptica (Ba- 57 °W39.00 and 62 °S44.77 59 °W06.43). All samples were ob- cillariophyceae, Centrales) and the green alga Dunaliella bioculata tained from depths between 60 m and the surface. Immediately (Chlorophyceae) were obtained from the algal collection of the after capture, the animals were transferred into tanks containing University of GoÈ ttingen (Dr. SchloÈ sser). Both species were cultured fresh, aerated seawater. After 24 h the most active animals were during the expedition Met 11/4 (21.12.1989±18.01.1990) on board selected for the feeding experiments. the research vessel FS Meteor. Semi-batch cultures were main- tained at 20±25 °C in a seawater/nutrient solution according to Guillard and Ryther (1962) and were exposed to a 16:8 h light:dark cycle. Feeding experiments For the determination of the dry weight of algae, 800 ml of the culture was centrifuged for 10 min at 4000 g. Several pellets were In order to cover a maximum range of experimental time scales, transferred into 1.5-ml reaction tubes and were again centrifuged three feeding experiments of dierent duration were carried out. for 10 min at 8000 g. The supernatants were removed and the re- Within each experiment, three groups of animals were maintained maining material was lyophilized to constant weight (Christ, Beta separately in aerated tanks. One group was fed with the diatom A). C. cryptica, the second with the green alga D. bioculata, and the third group was not fed. The experiments were carried out at 0± 2 °C and illumination was provided on a 16:8 h light:dark cycle. Determination of substrate concentrations in the cultured algae The maintenance tanks (closed systems) had been ®lled with fresh seawater from the ship's seawater supply system. This surface water Soluble protein and the substrates cellulose and laminarin were had been ®ltered through 3-lm membrane ®lters (Sartorius, 11302- determined and expressed relative to the dry weight of algae sam- 293-G) using a pressure ®lter system (Sartorius, SM 16277). During ples. Lyophilized samples of algae were resuspended in a total the experiments the water in the tanks was exchanged at least every volume of 1 ml 0.2 M Citrate-Phosphate Buer (CPB), pH 5.5, and other day. Faecal pellets and moults were removed frequently. Krill homogenized on ice by ultrasonication (Branson, Soni®er B12) for were frozen and stored at )75 °C until analysis. Feeding with algae 3 ´ 15 s with a break of 20 s each time. The cell-disrupter was started 1 day after the tanks had been stocked with krill. Fifty adjusted to 30% of maximal energy. Algal chitin as ``spines'' was millilitres of algal culture (approximately 1.75 mg dry weight, DW) isolated from fresh cells according to McLachlan et al. (1965) and were added per animal per day. stored at )80 °C for further analysis. For D. bioculata, which does Experiment 1 lasted for 20 days and was carried out in three not contain chitinous spines, lyophilized algae were analysed. tanks of 40 ´ 60 cm and 20-cm height. Each tank was equipped Soluble protein was determined according to Bradford (1976) with 24 PVC containers (volume 1 l), each containing 1 animal. using the BioRad microassay. The bottoms of the containers were punctured to ensure equal Cellulose (1,4-b-D-glucan) was hydrolysed by cellulase (Sigma water levels in all containers and to expose the animals to the same C-2415). The reducing sugars were determined using 3¢5¢-dinitro- water conditions. Experiment 2 (14 days) was carried out with 45 salicylic acid. In order to denature algal enzymes, the samples were krill in each of 3 basins of 40 ´ 30 ´ 30 cm. The animals were not heated for 10 min at 100 °C prior to analysis. A 100-ll sample was separated as described above. In experiment 3 (9 days), 135 krill added to 100 ll of 0.2 M CPB, pH 5.5 in 1.5-ml reaction tubes. The were maintained in each of 3 basins of 40 ´ 60 ´ 60 cm. A sub- reaction was initiated with 100 ll cellulase solution (1 U ml)1 in sample of 15 animals was removed after 2, 4, 6 and 9 days. The 0.2 M CPB, pH 5.5). The tubes were incubated for 2 h at 37 °C, volume of the water was reduced proportionally after each sam- with continuous stirring. After incubation, the tubes were centri- pling in order to maintain a constant density of krill. fuged for 5 min at 15,000 g. The supernatant (250 ll) was added to Only a representative number of animals from each feeding 250 ll of 0.1 M K/Na-P-Buer, pH 6.8.
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