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Scientific Reports Volume 11, Article Number: 21180 (2021) Cite this article
Recent studies have shown that the sensory quality of shrimp may be affected by ocean acidification, but we do not know exactly why. Here, we conducted a controlled pH exposure experiment on adult tiger prawns raised in 1,000-liter tanks continuously supplied with coastal seawater. We compared the survival rate, crustacean characteristics and meat sensory characteristics and amino acid composition of shrimps exposed to pH 7.5 and pH 8.0 for 28 days. The amino acid content of shrimp raised at pH 7.5 (17.6% w/w) is lower than that of shrimp raised at pH 8.0 (19.5% w/w). Interestingly, the content of amino acids that cause umami taste, namely glutamic acid and aspartic acid, in pH 7.5 is significantly lower than that in pH 8.0 shrimp, and pH 7.5 shrimp was also rated as less than ideal in the blind quality test . 40 volunteer evaluators. These results indicate that tiger prawns may become less palatable in the future due to the low yield of certain amino acids. Finally, the 28-day survival rate of tiger prawns at pH 7.5 is also lower than pH 8.0 (73% vs. 81%), indicating that ocean acidification may affect the quality and quantity of future shrimp resources.
With increasing attention to environmental changes caused by the increase in the partial pressure of CO2 (pCO2) in the atmosphere, ocean acidification (OA) has become a key issue that has been extensively studied in the past few decades. According to current predictions, by the end of the 21st century, the continuous absorption of atmospheric CO2 by the ocean may cause the average pH of the open ocean surface water to drop by 0.4 to 0.5. In addition to these predictions, the rate of acidification of coastal waters appears to be much faster than that of the high seas2,3. In addition, the downward trend of pH in coastal waters is superimposed on very large natural pH changes. By studying the impact of ocean acidification (OA) on the physiology of marine organisms and how seafood is affected, important insights into the impact of ocean acidification (OA) can be obtained4.
A large amount of evidence indicates that OA is expected to have a negative impact on the survival, growth, calcification, immune response and reproduction of marine organisms. However, until recently, there have been very few experimental studies attempting to estimate the possible socio-economic consequences of OA acidification due to changes in seafood quality5,6,7. A noteworthy study of this type shows that the cultivation of shrimp in acidified seawater can negatively affect its flavor5. In contrast, a study by Lemasson et al. 6 found that high pCO2 (≈ 1000 ppm), low pH (≈ 7.63) and high temperature (20 °C) conditions do not significantly affect the aroma and appearance of Pacific oyster Pacific oyster. Or taste. The flavor of seafood mainly comes from amino acids, nucleotides, sugars and mineral salts8. In particular, amino acids are believed to regulate the sensory qualities of shrimp, including sweetness, bitterness and umami. In humans, amino acids activate specific taste receptors9 and nutritional requirements. Therefore, the concentration and relative proportion of amino acids in shrimp and other seafood will have an important impact on consumers and seafood manufacturers. San Martin et al.7 developed a model to test how OA affects the taste of seafood and its appeal to consumers. They found that the attributes of mussels affected by OA also often determine consumers' preferences. People will only prepare to buy mussels affected by OA when they are 52% cheaper than the current one.
Globally, marine products from capture fisheries and mariculture account for 16% of the animal protein consumed by humans7. From 1960 (≈ 10 kg) to 2014 (≈ 20 kg) 10,11, the per capita consumption of seafood doubled Fan. The total output of marine products from mariculture and capture fisheries in 2018 was 115.2 million tons. By 210013, the world's population may reach 12 billion. Therefore, the demand for seafood will inevitably increase. In view of this growing demand and the mixed results of previous studies on the quality of seafood in the future, there is an urgent need to expand our understanding of the impact of acidification on seafood quality.
Here, we exposed tiger prawns (Penaeus monodon) to pH conditions covering the current (pH 8.0) and the near future (pH 7.5) average pH conditions of the coastal ecosystem. Penaeus monodon (Penaeus monodon) is an important species in the global shrimp industry, with a global trade volume of US$10 billion. Its annual output is about 1.5 million tons, and its texture and flavor are rated as ideal and very good by consumers around the world11,14. Tiger prawns live in brackish, estuarine (larval) and marine (adult) environments that extend from Africa to South Asia15. More and more tiger prawns are farmed in coastal and wetland areas of South Asian countries. These coastal waters are currently affected by rapid ocean acidification, which may threaten or affect the health, productivity and meat quality of tiger shrimp in the future.
We evaluated the changes in survival rate, growth, amino acid concentration of meat, and organoleptic quality of tiger prawns under low pH conditions compared with high pH conditions. Perform a blind tasting test to detect sensory changes, while using amino acid concentration as a proxy for tracking changes. Different amino acids have different main taste qualities. Basically, threonine, serine, glycine, alanine, arginine and proline are responsible for sweetness, valine, leucine, tyrosine and phenylalanine are responsible for bitterness, and glutamic acid and Aspartic acid provides umami taste 16, 18, 19, 19. We hypothesize that the observed difference in shrimp taste can be explained by the concentration of the above-mentioned amino acids.
Throughout the experiment, the average pH values measured in the target pH 8.0 and pH 7.5 test tanks were 7.96 ± 0.03 and 7.51 ± 0.04, respectively. The survival percentages of pH 8.0 and pH 7.5 after 28 days were 80.8% and 72.5%, respectively. The pH 8.0 tank decreased linearly with time throughout the 28-day period. The average mortality rate is 0.7% per day, where% refers to the initial total number of shrimps, not the total number of shrimps on the day of measurement. In the pH 7.5 tank, the shrimp population declined at the same rate as in the pH 8.0 tank until the 18th day. However, from day 18 to day 28, mortality occurred faster-although still at a linear rate of 2.0% per day (Figure 3). 1).
The time course of the pH value and survival percentage of the shrimp during cultivation. Blue circle = source sea water; green circle = sea water in a pH 8.0 tank; orange circle = sea water in a pH 7.5 tank. The green and orange dashed lines are regression lines, representing the percentage of surviving shrimp in the pH 8.0 and pH 7.5 tanks, respectively.
Interestingly, the average shell thickness of the shrimp at the end of the pH 7.5 treatment was 0.57 ± 0.28 mm, which was significantly higher than the 0.46 ± 0.28 mm shell thickness measured after the pH 8.0 treatment (n = 30, p <0.001, Figure 2 ). The contents of total carbon, organic carbon and inorganic carbon in shrimp shells were 297, 262 and 35 mg g-1 at pH 8.0, and 276, 258 and 18 mg g-1 at pH 7.5. The results of unpaired t-test showed that there was no significant difference in carbon content measured after pH 8.0 and pH 7.5 treatments (Figure 2).
The thickness and carbon content of the stratum corneum during pH 8.0 and pH 7.5 treatments. Left: The thickness of the stratum corneum, where the height of each column represents the average ± SE (n = 30), and the asterisk indicates a significant difference at p <0.001. Right: The concentration of total carbon (TC), particulate organic carbon (POC) and particulate inorganic carbon (PIC) in shrimp epidermis, where the column height is the average value ± SE (n = 6). No significant difference was found between the TC, POC or PIC values measured in the pH 8.0 and pH 7.5 treatments.
The total amino acid content in shrimp meat is 19.5 ± 0.69 g 100 g-1 at pH 8.0, and 17.65 ± 0.13 g 100 g-1 at pH 7.5, that is, there is no significant difference between the two treatments (n = 6, p = 0.07) (Figure 3 and Table S1 show the composition of a single amino acid). Among the amino acids, the content of asparagine, threonine, glutamic acid, alanine, cysteine, valine, methionine, and isoleucine in the treatment of pH 8.0 was significantly higher than that of pH 7.5 Treatment (n = 6, p <0.05). Except for glycine and phenylalanine, most other amino acids also show a negative response to increased pCO2 levels.
The concentration of amino acids in tiger shrimp muscle under two different pH treatments (8.0 and 7.5). The value is the mean ± SE (n = 6). Asterisk: statistically significant (*p <0.05, **p <0.01, ***p <0.001). Asp (aspartic acid), Thr (threonine), Ser (serine), Glu (glutamic acid), Gly (glycine), Ala (alanine), Cys (cysteine), Val (valine) Amino acid), Met (methionine), Ile (isoleucine), Leu (leucine), Tyr (tyrosine), Phe (phenylalanine), Lys (lysine), His (Histidine), Arg (arginine).
Sensory tests involving 40 test participants produced similar scores for the color and touch of shrimp raised at pH 8.0 and pH 7.5 (Figure 4). On the other hand, the appearance, texture, and flavor scores of participants at pH 8.0 were higher than pH 7.5 (Figure 4). Although they are semi-quantitative, these ratings are consistent with elevated levels of those amino acids that produce flavors that consumers prefer. The sum of amino acids (glutamic acid and aspartic acid) with a flavor corresponding to umami (salty) is significantly higher than pH 7.5 at pH 8 (n = 6, p = 0.03), but is responsible for sweetness The amino acids (n = 6, p = 0.31) and bitterness (n = 6, p = 0.15) did not show the difference between the two pH exposure groups (Table 1). The production of amino acids representing umami showed a significant pH dependence (F = 5.622, p = 0.045). The concentration of total amino acids and amino acids representing sweetness and bitterness are not affected by pH or salinity (Table 2).
The average score of appearance, color, touch, texture and flavor of two different pH treatments (8.0 and 7.5).
The acidification caused by CO2 represents a serious disturbance in the carbonate system. Most prawns have a strong ion regulation ability in acid-base balance20, and prawns tend to increase the calcification rate in their shells in response to elevated pCO221,22. Generally speaking, Penaeus monodon will complete a molting cycle in 6 to 12 days23. A previous study of shrimp (Lysmata californica)24 reported that inhibition of molting in low pH cultures actually resulted in a thicker stratum corneum, which has also been observed in other decapods25. Studies on other decapod animals also show that when the pH value is significantly lower than 8.026, 28, 28, their feed conversion rate, growth rate and survival rate decrease significantly. Even short-term exposure of crustaceans to low pH may cause the dissolution of their exoskeleton CaCO3 in an attempt to buffer protons and maintain hemolymph homeostasis29,30. Due to OA22,31, the energy cost of shrimp to maintain pH steady state is expected to increase. The energy burden of this acidification may also cause higher mortality in shrimp exposed to lower pH.
In this study, we found that the concentration of several amino acids in shrimp meat exposed to low pH decreased significantly. This may be related to the high concentration of CO2 that changed the chemical composition of seawater, which may limit the ability of the Na/K pump to maintain cell transmembrane potential and limit the transport/detoxification of proteins34,35. Previous studies have shown that when shrimp is under acid stress, the expression of antioxidant proteins and mRNA will decrease. Similarly, it is reported that in low pH water, the digestion and absorption pathways of protein and carbohydrates are significantly inhibited. In view of these findings, it can be speculated that the higher energy consumption of shrimp to maintain metabolism under pH stress conditions may result in lower concentrations of several amino acids observed in shrimp meat.
As far as we know, this is the first evidence that (1) the pH of seawater, (2) the amino acid content in tiger shrimp meat, and (iii) the sensory properties of shrimp may be the first evidence. The expression of amino acids may be affected by salinity 37,38, thus affecting the flavor of tiger prawns. Here, we found that elevated CO2 levels inhibited the production of umami-flavored amino acids (Table 2). Given that amino acids are usually found in artificial seafood seasonings, this is not surprising. In nature, the catabolic pathway of amino acids involves a series of decarboxylation, transamination and deamination reactions to produce carbohydrates, alcohols, aldehydes and carboxylic acids, which add extra flavor to shrimp39. The amino acids in shrimp meat provide strong evidence for observing the effect of acidified water on tiger shrimp. Sulfur amino acids (methionine and cysteine) play an important role in the expression of antioxidant response kinases. When invertebrates are exposed to acidic water, higher oxidative stress (superoxide, reactive oxygen species) is detected in their tissues40,41. In our study, we observed a decrease in methionine, resulting in lower methionine metabolism, which affects the low expression of cysteine42, 43. Failure to metabolize a series of sulfur-containing amino acids can reduce the antioxidant stress of tiger shrimp in an acidified environment. From a consumer's point of view, these reduced amino acids reduce the nutritional value of shrimp.
The results of this study are very compelling and provide insights into possible amino acid changes and corresponding changes in meat flavor and exoskeleton structure of tiger prawns under ocean acidification in the future. However, due to the species-specific response of marine organisms to ocean acidification, we cannot extend these observed changes to other shrimp species. For example, increased calcification was observed in the exoskeleton of Lysmata californica (Red Rock Shrimp)24, while no change in calcification was observed in Hippolyte californiensis (California Grass Shrimp)31. On the other hand, the growth rate of most shrimp species studied under low pH conditions so far has not changed24, 27, 31, 44. Considering these limitations, we strongly recommend extensive research on the impact of ocean acidification on the amino acid composition and taste of other shrimps, especially shrimps with important commercial value.
The first two factors that customers consider when choosing shrimp are appearance and flavor. As ocean acidification intensifies, our results indicate that both qualities may be adversely affected. Decreased customer satisfaction with shrimp farmed or caught under ocean acidification conditions may affect the global seafood aquaculture industry. For example, the current global trade volume of tiger prawns worth US$10 billion may decline if the appearance and taste of the prawns are worse. On the other hand, if our observations are limited to specific shrimps, some other species may find a way to adapt to the expected higher acidity, which will benefit the shrimp and shrimp industry. In this case, due to the expected decline in demand, intensive farming of species such as tiger prawns may be reduced, and more adaptable species may be welcomed by farmers. Therefore, open access may even promote the cultivation of species different from the currently favored species in the world's aquaculture industry.
Wild tiger prawns are widely distributed around the Indian Ocean and the Western Pacific, and are an invasive species in the Gulf of Mexico and the Atlantic coast of the southeastern United States. Its early life history was spent as a larva in an estuary environment, and then moved to deeper (approximately 25 m) shelf waters, where it began to grow at a young age. The wide fluctuation of environmental conditions in the estuary means that tiger prawns can adapt well to changes in salinity, pH and other water chemistry variables, albeit in their early life history45. When shrimp move to deeper water, they will experience much smaller changes in the pH of the environment. For our breeding experiment, the commercial supplier provided us with tiger prawn larvae stored in a low-salinity medium (S = 5), and then we slowly adjusted it until the salinity was the same as the salinity of the nearby coastal waters. Due to many factors affecting pH, especially photosynthesis of phytoplankton and microbial respiration of organic matter, the precise value of pH is more difficult to control, and causes some very large short-term pH fluctuations (7.57-8.63). Our pH 7.5 culture tank. This and other studies have reported on the potential effects of OA on the physiology and morphology of marine organisms, but it should also be remembered that OA may also affect the generation time or reproduction of the entire community51,52. It should also be noted that the exposure time in our experiment was relatively short compared to the life span of adult tiger shrimp. Nonetheless, our results indicate that there is a clear link between acidification and shrimp's amino acid profile and survival.
It is worth mentioning that compared with the white shrimp cultured at pH 8.046, OA at pH 7.5 does not significantly affect the survival rate of adult white shrimp (Penaeus vannamei). If this is the case, in the United States, the impact of OA on tiger shrimp may be greater than that on white shrimp. Given that tiger prawns are not native species in North American waters, OA may mediate the success of this invasive species in the Atlantic and Gulf of Mexico coastal areas.
In 2019, Penaeus monodon was cultivated in the shrimp pond of National Sun Yat-sen University in Kaohsiung, Taiwan for 11 months. The pH control experiment started on March 25, 2020. The changes in salinity and pH during shrimp farming are shown in Figure S1. Individuals with a body length of 19.7 ± 1.4 cm and a weight of 41.8 ± 10.2 g were transferred to four 1000-L fiber-reinforced polymer (FRP) tanks. Each tank received a coastal water input flow rate of 11 L min-1. Duplicate tanks for each pH treatment. There are 60 shrimps per tank, which is equivalent to a stocking density of 53 shrimps per square meter. The tiger prawns were adapted to the tank conditions for a week, and then they were kept at 26-28°C, S = 30-32 psu, and fed with commercial pellets of 5% by weight of the shrimp four times a day. Once a day, remove uneaten feed and debris from the bottom of the water tank.
After a week of domestication, shrimp belonging to the high pH group maintained pH ~ 8.0 (no carbon dioxide added) in natural flowing coastal seawater, and measured pH once a day (WTW ProfiLine pH 3110, accuracy ± 0.005). An automatic pH feedback system (P-LE-08 digital pH controller, Leilih) was used to expose the shrimp in the acidification tank to a gradually decreasing pH value from 8.0 to 7.5 (decrease by 0.1 per day). Before each new feed was provided, the dead shrimp and uneaten feed were taken out of the experimental pond. The survival percentage of tiger prawns is the average of pH 8.0 and 7.5. The equation is described as follows:
ninitial is the initial number of shrimps, ndead is the number of dead shrimps per day. The sensors belonging to the pH controller and WTW meter are calibrated using NIST standard buffers with pH values of 4.01, 7.00, and 10.00 (± 0.02 at 25°C). The air-gas balance technology (accuracy ± 30 ppm) associated with the K30 CO2 sensor is used to continuously measure the pCO2 of seawater. The CO2 sensor is calibrated according to the standard CO2 gas of 600, 3000 and 6000 ppm. The concentration of CO32- and calcium carbonate in the saturated state is calculated using the CO2 SYS computer program 48, using the measured pH and pCO2 as input carbonate system parameters. The dissociation constants (K1 and K2) are from Dickson and Millero49.
After 28 days of exposure, the shrimp shell thickness was measured with a thickness gauge (AICE, China) with an accuracy of 0.05 mm. The carapace was then washed with deionized water to remove large particles, and then sonicated in 1 N NaOH for 10 minutes to remove proteins and pigments. The washed stratum corneum is dried and homogenized into a powder, which is used to measure total carbon (TC) and particulate organic carbon (POC) by elemental analysis (Elementar vario EL cube, Germany). The content of particulate inorganic carbon (PIC) in the stratum corneum is estimated as the difference between TC and POC.
At the end of the 28-day exposure experiment, 3 shrimps were drawn from each tank for free amino acid content analysis. A sub-sample of 0.05 g shrimp meat was processed by AOAC Method 50, digested in 1 mL 6 N HCl, then dried and reconstituted in 1 mL 0.02 N HCl. The digested sample is filtered through a 0.2 µm Supro membrane disc filter. The amino acid analyzer L-8900 (Hitachi, Japan) was used to measure and quantify the total amino acids in these extracts.
After 28 days of exposure, 40 shrimps were harvested from each tank and soaked in cold sea water for several minutes until they died. These shrimps are immediately boiled in boiling sea water (salinity = 30) for 3 minutes. After natural cooling, 40 volunteer evaluators composed of 23 men and 17 women from 7 countries conducted a blind test on the sensory quality of the shrimp. They all like to eat shrimp and have eaten shrimp more than 5 times in the past 6 months. Shrimp from each experimental group was randomly provided to the participants. In short, four shrimps (two from pH 7.5 and two from pH 8.0) were placed on four different plates and sent to each participant at random (Figure S2). The exact nature of the study was not revealed to the participants, they were only asked to rate four shrimps (two shrimps each at pH 8.0 and two at pH 7.5) based on appearance, color, touch, texture, and flavor. For each category, they scored the shrimp specimens from 1 (worst) to 5 (best).
The taste of the amino acids in tiger prawns is calculated by summarizing all the amino acids known to cause a particular taste. Therefore, amino acids are divided into three categories. Glycine, alanine, threonine, proline, serine and glutamine contribute to sweetness. Glutamic acid and aspartic acid bring umami taste, while the bitter taste comes from phenylalanine, tyrosine, arginine, leucine, isoleucine, valine, methionine and histidine16,17 , 18, 19.
Use IBM SPSS software (version 24.0) for statistical analysis. A statistical significance level of 0.05 was selected for all statistical tests. Before performing any other statistical analysis, use the Shapiro-Wilk normality test to check the normality of all data. Linear regression was used to estimate the survival rate of tiger shrimp under different pH treatments. A Student's t test was performed to determine whether there were any significant differences in water chemistry, the thickness and carbon content of the shrimp skin, and the amino acid content of the shrimp meat under two different pH exposures. Two-way analysis of variance is used to examine the combined effects of salinity and pH and their interactive effects on the expression of total amino acids and the different flavors provided by amino acids.
All data can be found in the main text or supplementary materials.
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Thanks to CJ Chen, SY Huang, MH Chuang, JY Chen, MMPN Piyawardhana and RDDW Kulathunga for the shrimp farming during the experiment; Professor Lin Yaohua from Pingtung University of Science and Technology measured the total amino acids in shrimps and mussels. We would also like to thank CTA Chen, Peter Santschi, Laodong Guo and Professor James Liu for their valuable comments on our manuscript.
This work was funded by Taiwan’s Ministry of Education and the Ministry of Science and Technology (MOST) for funding projects (MOST-108-2611-M-110-019-MY3, MOST-110-2621-M-110-005 and MOST-110- 2119-M-110-001).
Department of Oceanography, National Sun Yat-sen University, Kaohsiung, 80424, Taiwan, ROC
Hsueh-Han Hsieh, Veran Weerathunga, W. Sanjaya Weerakkody, Wei-Jen Huang, François LL Muller, and Chin-Chang Hung
Department of Fisheries and Aquaculture, Faculty of Fisheries and Marine Science and Technology, Matara Ruhuna University, Sri Lanka
Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, 70803, Los Angeles, USA
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CC provided the initial idea. HH and WJ developed this method and conducted experiments. HH and SW combine data. CC, HH, and VW wrote the original manuscript, which was then thoroughly revised by CC, FM, and MB. All authors reviewed the manuscript.
The author declares no competing interests.
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Hsieh, HH., Weerathunga, V., Weerakkody, WS etc. The effect of low pH on the taste and amino acid composition of tiger prawns[J]. Scientific Representative 11, 21180 (2021). https://doi.org/10.1038/s41598-021-00612-z
DOI: https://doi.org/10.1038/s41598-021-00612-z
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