Tunas are the athletes of the fish world. They are endothermic, maintaining high metabolic rates that are approximately 3-5 times those of other active teleosts (Brill and Bushnell, 1991) and more like those of small mammals (Keen et al., 1991). The anatomy of tuna allows them to keep their swimming muscles warm. Tunas have a retia mirabilia, a system of countercurrent heat exchangers composed of a masses of intertwined arteries and veins that prevent heat loss and shunt metabolic heat back to the tissues (Carey. 1973). The result of increased temperature in their muscles is increased power output of the swimming muscles. While their swimming muscles are maintained at high temperatures, their hearts are at the ambient temperature. Tuna sustain delivery of oxygen to their tissues though a wide range of temperatures. The thermal niche of the more tropical yellowfin tuna is between 12° and 28° C while that of a bluefin tuna is between 2 and 30°C (Block, pers. comm). Tuna hearts produce high cardiac outputs to sustain delivery of oxygen to their swimming muscles. The maximum cardiac output of yellowfin tuna is 97.6 mls/kg/min (Blank et al, 2001) whereas the maximum cardiac output of a rainbow trout (Oncorhynchus mykiss) is 17.6 ml/min/kg. (Kiceniuk and Jones, 1977). The regulation of cardiac output in tunas has been suggested to be primarily through heart rate (Farrell et al, 1992). Tunas have heart rates that exceed 120 bpm (Farrell and Jones, 1992) and have been measured as high as 240 bpm (Kanwisher et al,1974). The heart rates of tunas exceed those of other lower vertebrates. A high heart rate may be a prerequisite for high cardiac output and concommitant oxygen delivery to their powerful swimming muscles. Calcium cycling, which is necessary tension generation in the heart, is essential to contraction and relaxation of the heart. The sarcoplasmic reticulum is an internal store of calcium in muscle cells that plays an important role in cardiac muscle contractility by regulating intracellular calcium concentration. (Fig. 1) (Tibbits et al, 1992). Release of calcium from the SR through the ryanodine receptors initiates muscle contraction whereas uptake of calcium by an SR CaATPase (SERCA) results in muscle relaxation. Cardiac cells have a unique isoforms of these proteins (Brandle et al, 1986; Franck et al, 1998). Mammals rely primarily on SR release and uptake of calcium during the contraction and relaxation cycle (Tibbits et al, 1992). The primary reliance of SR stores of calcium in mammals creates a shorter diffusion distance for calcium. This permits an increased rate of relaxation of the heart, a higher heart rate, and thus, an increased cardiac output. With an increased cardiac output, mammals and birds can deliver oxygen to their tissues at a higher rate, sustaining their high metabolic rates. This suggests that the high metabolic rates of mammals are correlated with the reliance on SR calcium cycling in heart cells. In contrast to mammals, in most fish, tension is developed primarily through calcium derived from the extracellular space. Calcium entry into the cytoplasm is mediated by the plasma membrane voltage gated channel, or dihydropuridine receptor (DHPR) (Tibbits et al, 1992). Calcium is removed from the heart by a plasma membrane calcium ATPase (PMCA) and the sodium-calcium exchanger during relaxation of the heart. The sarcoplasmic reticulum is thought to play minor role in the cardiac contraction and relaxation cycle. The decreased use of the SR in calcium cycling may explain the lower cardiac outputs and metabolic rates of fishes. Because tuna maintain the high heart rates necessary to sustain their high cardiac outputs and metabolic rates, I hypothesized in this study that the tuna myocyte has an internal SR with calcium ATPase and calcium release channels. A tuna that is able to maintain a high metabolic rate may have an increased reliance on SR calcium cycling, which permits a higher heart rate and cardiac output. Examination of the SR in teleosts has been done mainly on salmonids (Tibbits et al, 1991); however, little work has been done examining calcium cycling in tunas. It has been shown that skipjack tuna heart derives a large portion of its calcium required for contraction from the release of calcium from intracellular SR stores (Keen et al, 1992). Moreover, rates of relaxation and contraction in yellowfin tuna hearts have been shown to be impaired by ryanodine, a natural plant alkaloid that blocks SR calcium release, suggesting that SR calcium plays a role in initiating contraction (Shiels and Farrell, 1999). In this study, we examined the presence of sarcoplasmic reticulum with calcium ATPase and calcium release channel in two species, the yellowfin tuna and bluefin tuna. Methods and Materials SR isolation Wild tunas were obtained in the Atlantic and Pacific oceans during routine collections. Tissues were freeze clamped after the fish were caught on hook and line and sacrificed by pithing. Additionally, tunas were maintained in captivity at the Tuna Research and Conservation Center as described by Altrinham and Block, 1997 For purification of sarcoplasmic reticulum from the tuna hearts, between 3.5g and 30.0 g of liquid nitrogen freeze-clamped tissues from bluefin tuna (Thunnus thynnus) or yellowfin tuna (Thunnus albacares) heart muscle was homogenized using a Tekmar homogenizer in 10 volumes of ice-cold homogenization buffer containing 0.3 M sucrose and 20 mM potassium-piperazine-N, N’-bis[2-ethanesulfonic acid (K-PIPES), pH 7.6, and a protease inhibitor cocktail containing 1.0 M pepstatin A, 1.0 mM iodoacetamide, 0.1 mM phenylmethylesulfonylflouride (PMSF), 1.0 M leupeptin, 1.0 mM benzamidine, 0.1 M aprotinin, and 6.0 mg/ml trypsin inhibitor. The protease inhibitors were re-added to each buffer at every step of the procedure. Äfter homogenization the slurry was centrifuged for 20 minutes at 2600 g (4670 RPM) in a Sorval SL5OT rotor. The supernatant was passed through two layers of cheesecloth, and the crude microsomes pelleted by centrifugation at 100,000 g (35,000 RPM) for one hour in a Beckman Ti50.2. The pellets were resuspended in the resuspension buffer containing 0.3 M sucrose and 5 mM potassium-piperazine-N, N'-bis[2-ethanesulfonic acid] (K-PIPES), pH 7.3. A portion of the resulting microsome preparation was frozen in liquid N2 and stored at - 80°C until use. The remaining material was layered on top of discontinuous sucrose gradients (2.0 ml 45%, 3.0 ml 35%, 3.0 ml 25%) containing 0.4 M KCl, 0.1 mM NazEGTA, O.1 mM CaCl, and 5.0 mM K-PIPES, pH 6.8, and centrifuged 16 hours at 23,000 rpm in a Beckman SW41 rotor. Heavy SR (HSR) membrane vesicles were recovered from the 35%-45% interface and pelleted at 100,000 g. Light SR (LSR) membrane vesicles were recovered from the 30-35% interface and pelleted at 100,000 g. Vesicles were resuspended in 200 mM sucrose and 5.0 mM K-PIPES, pH 7.0, frozen in liquid N», and stored at -80°C until use. Calcium ATPase (SERCA 2) antibody production and purification Isoform specific antibodies were raised against a peptide of SERCA 2 by Research Genetics Inc. (Huntsville, AL). The peptide corresponding to amino acids (192-205) of rabbit Serca 2 were synthesized and used to immunize four rabbits. Serum IgG purification was performed using ImmunoPure Affinity Pak protein A columns following the instructions provided (Pierce, Rockford, IL). Two affinity columns were made by immobilization of the 5 mg of the synthesized peptides provided by Research Genetics using a EDC/Diaminodipropylamine Immobilization Kit and the included protocol (Pierce, Rockford, IL). 1 ml of the IgG fractions from the protein A columns followed by 2 ml of PBS (phosphate buffered saline) were applied to the appropriate affinity column and incubated for 1 hour at room temperature. The columns were washed with an additional 14 ml of PBS after which the antibodies were eluted with 0.1 M glycine pH 3.0. 1 ml fractions were collected and their absorbance at 280 nm was monitored to determine the protein peak. Peak fractions were pooled, brought back to neutral pH and stored at -80°C until use. Gel Electrophoresis and Western Blots Heart SR microsomes, HSR, and LSR fractions were run on 7.5% or 3-12% SDS polyacrylamide gels according to the method of Laemmli, 1970. Gels were either stained with Coomassie blue or blotted onto PVDF membranes which were subsequently blocked in 5% nonfat milk, 0.2% Tween, and 0.02% NaAzide in PBS for 1 hour. Blots were incubated in 1:750 SERCA 2 antibody overnight at room temperature. Blots were washed 3x in PBS and subsequently incubated with a goat anti-rabbit secondary antibody/alkaline phosphatase conjugate diluted 1:1000 for 1.5 hours. Blots were developed with BCIP/NBT. Calcium Flourimetry Sarcoplasmic reticulum calcium uptake in heart SR preparations was measured using the calcium-sensitive dye fura-2 and a Shimadzu RF 5301 spectroflourophotometer. SR microsomes were added at a final concentration of 1.5 mg/ml to a cuvette containing 1.4 ml calcium transport buffer (95.0 mM KCl, 20 mM H¬ MOPS, 7.5 mM NaPyrophosphate), 5.0 mM creatine phosphate, 0.01 mg/ml creatine phosphokinase and 1.5 uM fura-2. Extravesicular calcium was monitored as a ratio of the fura-2 fluorescence emission intensity at 510 nm at excitation wavelengths 340 nm and 380 nm. Calcium uptake was initiated with the addition of 2.5 mM MgATP and allowed to proceed to equilibrium. Subsequential 15 nmol additions of CaClz were added to the cuvette to load the vesicles. At the end of the experiment, 1 mM CaClz was added followed by 20 mM EGTA. Results Purification of sarcoplasmic reticulum The homogenate, microsomal, light sarcoplasmic reticulum (LSR) and heavy sarcoplasmic reticulum (HSR) fractions of bluefin and yellowfin ventricle were run on a 3-12% SDS-PAGE that was stained with Coomassie blue (Fig. 2). The homogenate retains contractile filaments, as evidenced by the band at the 207 kDa molecular weight marker, myosin. In the microsomal, LSR, and HSR preparations, the band at 207 kDa is less dense, demonstrating the removal of contractile proteins during the purification process. Also in these fractions, there is an enrichment of a band at about 110 kDa, which, from previous work, has been shown to be SERCA 2 (Brandl et al, 1986). Western blot To determine if the band at 1 1OkDa was SERCA 2, a Western blot analysis was conducted using a SERCA 2 specific primary antibody (Fig. 3). A band appears at 110 kDa in yellowfin tuna atria and ventricles and bluefin tuna ventricles, confirming the presence of SERCA 2 in these tissues. Densitometric comparison of bluefin and yellowfin, atrium and ventricle SERCA 2 A band at 110kDa appears in all lanes in 3-12% SDS-PAGE comparing bluefin and yellowfin atrium and ventricle microsomal fractions (Fig. 4). A thin band at about 500 kDA also appears on the stained gels, demonstrating the existence of the ryanodine receptor in tuna heart. Previous work has demonstrated that the molecular weight of the fish ryanodine receptor is 576 kDa (Franck et al, 1998). Densitometry performed on the SDS gels using NIH Image suggests that tuna atrium has more SERCA 2 than ventricle. The ratio of SERCA 2 band intensities between bluefin atrium and bluefin ventricle is 2.5 + 0.7 (n-2). The ratio between yellowfin atrium and ventricle is 1.5 + 0.2 (n—4). Densitometry also suggests that yellowfin and bluefin tuna heart have similar amounts of SERCA 2. The ratio between yellowfin atrium and bluefin atrium is 1.5 + 1.0 (n-2). The ratio between yellowfin ventricle and bluefin ventricle is 0.9 + 0.2 (n-4). Flourimetry SR vesicles take up calcium when ATP is added to the cuvette containing BFT fast twitch SR vesicles, creatine phosphate, creatine phosphokinase, mitochondrial inhibitors and fura 2 (Fig. 5). At t =O, ATP is absent in the cuvette and the level of calcium in the extravesicular space, as evidenced by the ratio of fluorescence at 340 nm to 380 nm, is high. Upon addition of ATP, the amount of calcium in the extravesicular space decreases as the SR sequesters calcium. Upon the addition of CaCl, the amount of calcium in the extravesicular space quickly increases and then declines back to baseline as the SERCA 2 pumps are activated. The rates of uptake of calcium by the SR can be calculated given the known amount of calcium added. The experiment is repeated with bluefin and yellowfin atria and ventricles. (Fig. 6) Bluefin fast twitch muscle SR sequesters calcium at a rate of 3.2 nmol Ca“/mg/s. Bluefin tuna slow twitch muscle SR sequesters calcium at a slower rate of 0.094 nmol Ca“/mg/s. Bluefin atrium SR sequesters calcium at a rate of 0.020 nmol/mg/s and bluefin ventricle SR sequesters calcium at a rate of 0.014 nmol/mg/s. Yellowfin atrium and ventricle sequester calcium at an identical rate of 0.012 nmol/mg/s (Table 1). Discussion In this study, I have shown the presence of proteins associated with the sarcoplasmic reticulum in tuna atrial and ventricle tissues. I have examined the content of SERCA 2 and found it slightly higher in the atrium in both tunas. The results may indicate that the high metabolic rates of the tunas are correlated with the presence of sarcoplasmic reticulum and the machinery for calcium cycling. In mammalian and avian lineages, the metabolic rates require high cardiac outputs, which are enhanced by the short diffusion distance for calcium from the internal SR stores to the contractile filaments. This allows for an increased relaxation rate, heart rate, cardiac output, and delivery of oxygen to the demanding muscles. In the classic view of fish, tension generation relies primarily on extracellular calcium, thus lengthening the diffusion distance and decreasing fish heart rates. Tunas are powerful, highly metabolic, endothermic fishes that maintain high muscle temperatures through a wide range of ambient temperatures. The heart, at ambient temperature, somehow fulfills the high oxygen demand of the working tuna muscle. The use of an internal specialized structure, such as the SR, could explain how tuna maintain a cardiac output high enough to supply oxygen to the swimming muscles. Tuna atrium may have more SERCA 2 than ventricle. Densitometry shows that the ratio of SERCA 2 in bluefin atrium to bluefin ventricle is 2.5 + 0.7 (n-2), which correlates with the faster rates of calcium uptake in bluefin atrium than bluefin ventricle. Bluefin atrium SR sequesters calcium at a rate of 0.020 nmol/mg/s and bluefin ventricle sequesters calcium at a rate of 0.014 nmol/mg/s. Moreover, the ratio between yellowfin atrium and ventricle is 1.5 + 0.2 (n—4). The ratio between yellowfin atrium and ventricle, which is not as high as the ratio between bluefin atrium and ventricle, is reflected in rates of uptake; yellowfin atrium and ventricle SR sequester calcium at an identical rate of 0.012 nmol/mg/s. The calcium uptake assay may not be sensitive enough to detect differences in rates of uptake in yellowfin heart SR. The greater amount of SERCA 2 in tuna atrium and ventricle, and the faster rate of uptake by the bluefin atrium than ventricle, can be explained by the roles of the different chambers in the cardiac cycle. The atrium contracts and ejects its volume of blood into the ventricle; the ventricle subsequently contracts and must sustain its contraction against a load. While the ventricle must be able to sustain its contraction, the atrium must contract and relax quickly before the ventricle contracts. The speed of contraction of the atrium is critical during cardiac contraction whereas the force generated in the ventricle is critical. An increased amount of SERCA 2 in atrium may permit faster uptake of calcium into the SR and faster relaxation rates. There is not a substantial difference in the amount of SERCA 2 between bluefin and yellowfin hearts. Densitometry shows that the ratio of yellowfin atrium and bluefin atrium is 1.5 + 1.0 (n=2). The ratio between yellowfin ventricle and bluefin ventricle is 0.9 +0.2 (n=4). The similar amounts of SERCA 2 between the two species of tuna can be explained by the following: Both bluefin and yellowfin tuna live in warm waters for part of the year. This period, where muscles are warm and demand an abundance of oxygen, sets the maximum limit of oxygen delivery to the tissues. For the heart to deliver oxygen to warm, highly demanding swimming muscles at 30°C, both yellowfin and bluefin tuna hearts must have high frequency contractions. Thus, both species have the calcium cycling machinery necessary to deliver these high frequency contractions; both species are equipped with high amounts of SERCA 2. How bluefin tuna can maintain their high metabolic rates and high cardiac outputs to sustain their aerobic performance necessitates fürther research. Perhaps the SERCA pumps are at a high concentration in cold waters and are pumping just as much calcium into the SR in cold waters as they do in warm waters. Other proteins in the calcium cycle may be responsible for high bluefin tuna cardiac outputs through a wide range of temperatures. Instead of increasing heart rates to maintain a high cardiac output to deliver oxygen to their swimming muscles, perhaps bluefin tuna rely on an increased stroke volume to supply their high cardiac outputs. This could be caused by the surface membrane voltage gated channels (DHPR), which may let calcium into the myocyte for a longer period of time. An increased flow of calcium into the cell would sustain the contraction and increase the contractile power of the heart. Investigation into the role of other calcium cycling proteins may provide insight into the ability of bluefin tuna to maintain their cardiac outputs in both cold and warm waters. Calcium uptake assays show that bluefin white muscle SR sequesters calcium more quickly than slow twitch or heart muscle. There are more SERCA pumps in white muscle than red muscle. White muscle also has the SERCA 1 isoform of the pump while red muscle and cardiac cells have the SERCA 2 isoform (Brandl et al, 1986). The white muscle in tuna swimming muscle must contract quickly to generate the power necessary to for tuna to swim at exceptionally high speeds. Red muscle and cardiac muscle cells, on the other hand, contract more slowly with their smaller diameter and their high concentration of mitochondria. Although uptake of calcium by the SR in tuna hearts is slow, the uptake is ATP mediated, suggesting that tuna hearts use SERCA 2 as a means of removing calcium from the cytoplasm. Conclusions The existence of SR in tuna cardiac cells is a factor in explaining the high cardiac outputs and metabolic rates of tuna. Calcium cycling in the SR is crucial in determining rates of contraction and relaxation. Tunas, the athletes of the fish world, have the ability to coordinate the release and uptake of calcium by the SR and deliver oxygen to their working muscles in a wide range of ambient temperatures. How tunas evolved this extraordinary ability and the physiological mechanisms that allow them to do so is an interesting question. The uptake of calcium by SERCA 2 hints at the paramount role of the SR in contributing to their high metabolic rates. Further research possibilities include an investigation of the role of other calcium cycling proteins, such as DHPR, the ryanodine receptor, and myosin ATPase, which may contribute to the high cardiac outputs of tuna. Acknowledgements Towe an incredible amount of gratitude to my advisor, Barbara Block, for her dedication and excitement about my project. I thank her for sparking my interest in research and for contributing to my critical thinking on this project. l’ve learned a little bit about what science is about and couldn’t have done it without her. I had never thought as tuna as amazing organisms until I met Barb! I also am so grateful to Jeffery Morrissette for the amount of work and time he invested in this project. I thank him for answering all my questions and being a wonderful teacher and I could not have done this without him. 1 want to thank Jason Blank for also being an incredible teacher and for his willingness to drop everything to help me. I thank him for furthering my excitement about physiology. l’ve learned so much about being in a lab, research, and science from these two gentlemen. l’d also owe a special thanks to everyone in the Tuna Research and Conservation Center for their wonderful help. 12 Literature Cited Blank, J. et al. 2001. Effects of temperature, adrenaline and calcium on the hearts of yellowfin tuna (Thunnus albacares). Tuna Research and Conservation Center. Stanford University, Hopkins Marine Station, Oceanview Blyd, Pacific Grove, CA 93950. Brandl, C. J. et al. 1986. Two Ca2+ATPase genes: homologies and mechanistic implications of deduced amino acid sequences. Cell 44: 597-607. Brill, R.W. and Bushnell, P.G. 1991. Metabolic and cardiac scope of high energy demand teleosts, the tunas. Can. J. Zool 69: 2002-2009 Carey, Francis G. Feb 1973. Fish with warm bodies. Sci. Am. 228 No 2. Farrell A.P. and Jones, D.R. 1992. The heart. pp.1-88 in Fish Physiology, Vol XIIA, Academic Press, San Diego, CA. Franck , J. et al. 1998. Cloning and characterization of fiber type-specific ryanodine receptor isoforms in skeletal muscles of fish. American Physiological Society Kanwisher, J. et al. (1974). Acoustic telemetry from fish. Fish. Bull., U.S. 72: 251-255. Keen, J. E. et al. 1992. Cardiac physiology in tunas II. Effect of ryanodine, calcium and adrenaline on force-frequency relationships in atrial strips from skipjack tuna, Katsuwonus pelamis. Can J. Zool. 70: 1211-1217. Kiceniuk, J.W. and Jones, D.R. 1977. The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. J. Exp. Biol. 69: 247-260. Korsemeyer, K. E. et al. 1977. Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna Thunnus albacares. J. Exp. Biol. 200: 1987-1997. Shiels, H. A. and Farrell, A. P. 1999. The sarcoplasmic reticulum plays a major role in isometric contraction in atrial muscle of yellowfin tuna. J. Exp. Biol. 202: 881-890. Tibbits, G. F. et al. 1991. Calcium transport and the regulation of cardiac contractility in telesosts: a comparison with higher vertebrates. Can. J. Zool. 69: 2014-2019. Tibbits, G. F. et al. 1992. Excitation-contraction coupling in the teleost heart. pp. 267- 304 in Fish Physiology Vol XIIA, Academic Press, San Diego, CA. Table I. Rate of calcium uptake in BFT fast twitch and slow twitch muscle and BFT and yFT atrium and ventricle SR vesicles. 75 nmol of CaClz were added to BFT fast twitch SR vesicles. The concentration of protein was 0.5 mg/ml. 15 nmol of calcium were added to BFT slow twitch muscle and BFT and YFT atrium and ventricle SR vesicles. The concentration of these proteins was 1.5 mg/ml. Ti/ is the amount of time required for the SR to take up half the amount of calcium added. Type of Muscle Ca Uptake (nmollmgs Tia (seconds) BFT Fast Twitch Muscle 3.2 15.7 0.094 BFT Slow Twitch Muscle 105.9 BFT Atrium 0.020 196.1 227 231. BFT Ventricle 0.014 YFTAtrium 0.012 YFT Ventricle 296.1 0.012 14 Figure Legend Fig 1. The heart cell. Calcium from the extracellular space enters the heart cell through a voltage-gated channel, DHPR. This causes calcium induced calcium release by the ryanodine receptors in the SR membrane. Tension can then be generated by the contractile filaments. During relaxation of the heart cell, calcium is removed by plasma membrane calcium ATPase (PMCA), the sodium-calcium exchanger, and SR calcium ATPase (SERCA). (from Tibbits et al, 1992). Fig 2. Purification of sarcoplasmic reticulum. A 3-12% SDS gel was loaded with different fractions of the SR isolation preparation in YFT and BFT ventricle. The homogenate contains the contractile filaments. Microsomes, light SR and heavy SR fractions are enriched in SR. Fig 3. Western blot with a SERCA 2-specific antibody. Tuna hearts express SERCA 2. Fig. 2A indicates that BFT and YFT ventricle have SERCA 2, as evidenced by the bands at 110 kDa. Fig. 2B indicates that YFT atrium and ventricle have SERCA 2, as evidenced by the bands just below the 118 kDa molecular weight marker. Fig. 4. A comparison between bluefin and yellowfin atrium and ventricle. SERCA 2 (110 kDa), myosin (200 kDa), and ryanodine receptor (576 kDa) can be visualized on this 3-12% SDS gel. Tuna hearts have SERCA 2. Fig 5. Calcium uptake by BFT fast twitch muscle SR. Uptake of calcium by BT fast twitch muscle SR is ATP mediated. The amount of calcium in the extravesicular space decreases when ATP is added and the SR sequesters calcium. When CaCl» is added, the extravesicular calcium increases is followed by an immediate sequestration of calcium by the SR. Fig. 6. Calcium uptake in BFT atrium and ventricle. BFT atrium (2A) and ventricle (2B) SR sequester calcium in the presence of ATP when CaCl, is added. S1 co co 6 ADP 3N0 T-TUBULE AT SR SR C Ve — — — — — — COR CNOICOX DRNOR Fig. 1 17 7 kDa 8 kDa- BFT Ventricle Fig. 2 YFT Ventricle 4 Serca 2 A. BFT Ventricle 110 kDa B. 118 kDa Fig. 3 YFT Ventricle YFT 207 kDa - 118 kDa- BFT YFT Fig. 4 RyR Myosin Serca 2 0 2.5 mM MgATP 75.0 nmols CaCl, X 5 5 UM A23187 — 200 400 600 800 1000 1200 1400 Time (seconds) Fig. 5 B. 1 15O nmols Ca 12 2.5 mM MgATP 200 400 600 800 1000 12 Time (seconds) 15.0 nmols CaCl, x2 2.5 mM MgATP 200 400 600 800 1000 1200 1400 Time (seconds) 5.