Abstract
Penaeid shrimps are euryhaline in nature and have the ability to survive and adapt in a wide range of salinities (3–50 ppt). The shrimps are cultured under a variety of conditions in many tropical and subtropical countries. Osmotic and ionic regulation is an important mechanism of environmental adaptation in crustaceans. However, drastic changes in abiotic and biotic conditions result in stress to the shrimps during the culture period. Salinity and temperature are the two major environmental factors that have huge impact on culture shrimp, affecting their physiological and metabolic parameters, which in turn affect shrimp growth, molting, and survival. Changes in the abiotic factors, chemical and biotic factors result in reduced immunity of shrimp and vulnerability to bacterial and viral diseases. This chapter describes the effects of low and high salinity on the gene profile changes of black tiger shrimp Penaeus monodon, and the functional role of these genes in shrimp salinity stress is discussed.
Keywords
- Penaeus monodon
- Salinity stress
- Differentially expressed genes
1. Introduction
Penaeid shrimps being euryhaline can adapt to thrive and survive in a wide range of salinity conditions. Shrimps are, therefore, cultured and reared under different farming conditions in tropical and subtropical countries. Water quality management is an important criterion in shrimp farming for survival and growth of the shrimp. The optimal salinity conditions for penaeid shrimp ranges differently for different species.
However, the variable climate conditions result in drastic changes in abiotic factors causing stress to the shrimps during the culture period, which influences culture of euryhaline penaeids. In summer months, there is increase in salinity in ponds due to high evaporation rates and in rainy season the salinity decreases. The marine crustaceans are generally osmotic and ionic conformers in nature. The shrimps hypo-osmoregulate above the iso-osmotic point and hyper-osmoregulate below the iso-osmotic point through a osmoregulation mechanism.
In crustaceans, gills which are highly permeable external surfaces are the primary sites involved in osmoregulation. In the larval stages of penaeids, the typical features of osmoregulatory epithelia are present in pleurae and branchiostegites [8]. The overall ion-transport and osmotic regulation process involves ions absorbtion or excretion between the external and internal medium through osmoregulatory organs, such as gills, the antennal glands that mainly function in urine production, and the gut in decapod crustaceans [9-10]
The crustaceans have two well-known important enzymes which are central to osmotic and ionic regulation and ion uptake. The transepithelial movement of monovalent ions requires the action of Na+/K+-ATPase or the sodium pump utilizing ATP as energy source. The other major enzyme involved in osmoregulation is transport-related enzyme carbonic anhydrase, which plays a role in producing H+ and HCO3- through catalysis of respiratory CO2, for counterions in Na+ and Cl− uptake. In penaeids, carbonic anhydrase is reported to be involved in both hyper- and hypo-osmotic regulation and is induced against low and high salinity exposure, indicating its role in ion uptake and excretion process [11].
In our study, we have constructed suppression subtractive hybridization (SSH) cDNA libraries to identify differentially expressed genes in shrimp
Similarly, we obtained several functional categories of genes from the forward SSH cDNA libraries (Figure 3) and reverse SSH cDNA libraries (Figure 4) constructed from gill tissues of shrimp exposed to low (3 ppt) and high (55 ppt) salinity conditions. These differentially expressed genes were subjected to RT-qPCR for gene expression analysis. Based on our study, we discuss herein in this chapter some of the important genes identified as differentially expressed in response to salinity stress in shrimp.
2. Osmoregulatory genes
2.1. Na+/K+-ATPase
Na+/K+-ATPase, a transmembrane protein, contains three subunits, α-, β, and γ- subunit, which are involved in exporting three Na+ from cytosol in exchange for two K+ or NH4+ from extracellular fluid for each ATP hydrolyzed. The crustacean α-subunit, which is 71–74% identical in amino acid sequence to those of vertebrate α-subunit sequences, binds to ATP and functions for the catalytic action of the enzyme [12]. The binding of Na+/K+-ATPase complex to basolateral membrane requires participation of β-subunit and the γ-subunits of enzyme [13]. The activity of Na++K+-ATPase in gill tisues of crustaceans depends on the osmoconcentration gradient occurring between hemolymph and the external medium. In crustaceans, there is an increase in Na+/K+-ATPase activity when transferred from natural seawater to dilute seawater [14-15]. With the lowering of salinity when compared to that of normal seawater, the euryhaline crustacea undergo hyperosmoregulation. Increased enzymatic activity of Na++K+-ATPase and increased α-subunit gene expression has been observed in the gill tissues of crabs [12]. Substantial increase in Na+/K+-ATPase specific activity (300%), Na+/K+-ATPase protein levels (200%), and gene expression level of α-subunit (150%) has been observed in blue crab
At low (3 ppt) salinity conditions stress conditions, significant increase in the Na+/K+-ATPase α-subunit gene expression levels was observed in gill (34.28-fold) tissues of
3. Immune genes
Crustins, belonging to family of antimicrobial peptides (AMPs) are shown to be differentially expressed in response to various immunostimulants and microbes [22]. Different isoforms of crustins have been isolated from a variety of penaeid shrimps [23-25]. The up-regulation of crustin-like AMP in shrimps suggests functional role of AMPs primarily in the shrimp immune response [26]. Under hyperosmotic stress, crustinPm5, crustinPm1, and crustin-like Pm gene levels were found to be up-regulated [27]. In our study, we observed crustin gene was up-regulated in all the three shrimp tissues of gills, gut, and muscle analyzed at low salinity stress [20]. Hence, crustins having antimicrobial activity also functionally respond to salinity stress in shrimps.
Another class of AMPs, the penaeidin gene was found to be down-regulated in gill, gut, and up-regulated in antennal gland tissues of shrimp exposed to high salinity stress (55 ppt) conditions [21]. These changes in the gene expression levels of penaeidin may be regulated through variations in hemocyte numbers in salinity-stressed shrimp. Antibacterial proteins such as lysozymes are involved in nonspecific innate immunity in shrimps [28]. Significant up-regulation of lysozyme gene expression occurred in gill (16.25-fold) tissues of shrimp exposed to low salinity stress [20]. In these shrimps, the anti-lipopolysaccharide factor, which is considered to play an important role in shrimp immune response [29], was significantly down-regulated in gill and gut tissues as compared to up-regulation in the muscle tissues of shrimp.
In general, as a result of environmental stress, the expression of immune-related shrimp genes transcripts gets affected [30]. The shrimp exhibits reduction in immune parameters when exposed to salinity stress conditions, leading to decreased resistance against pathogens [31-32]. White shrimp
4. Cellular-process-related genes
4.1. Ubiquitin-conjugating enzyme
The ubiquitin proteolytic system is involved in various cellular processes such as cell cycle regulation, cellular response to stress, and immune response [33-34]. In shrimps, the ubiquitin-conjugating enzyme E2r (UBE2r) gene isolated from
4.2. Cathepsins
The proteases are distributed into four major classes: aspartyl proteases, metalloproteases, serine proteases, and cysteine proteases [39]. The cathepsins belonging to cysteine proteases in addition to cellular protein degradation and turnover are also involved in numerous other physiological processes. In fishes, the cathepsin La isoform has been implicated in yolk-processing mechanism during oogenesis and embryogenesis [40]. In shrimps (
5. Signal transduction genes
5.1. 14-3-3 protein
The members of the 14-3-3 protein family are dimeric proteins that are expressed in a wide range of organisms and tissues. They are involved in modulation of protein interactions through phosphorylation process. The other diverse functional roles include interaction with a large number of protein kinases, DNA, Raf kinase, and regulation of cell cycle progression [46]. In plants, 14-3-3 protein activates and regulates plasma membrane H+-ATPase through fusicoccin responsive system [47]. Two Na+/K+-ATPase α -subunit forms were detected in the gill transcripts of crab
5.2. Calreticulin
Calreticulin, a versatile lectin-like chaperone and important endoplasmic reticulum luminal resident protein, is involved in Ca2+ homeostasis and molecular chaperoning. Calreticulins, which are highly conserved in most of the eukaryotes, are involved in the synthesis of various molecules and in many other biological and physiological processes of an organism. The highest expression of calreticulin was detected in ovary of
5.3. Innexins
Innexins, which are members of large multigene families, are involved in formation of gap junctions for cell-to-cell communication [52]. In crustaceans, innexin expression has been associated with developing lobster stomatogastric nervous system [53]. In
6. Energy and metabolism genes
6.1. Arginine kinase
Arginine kinase plays a major role in energy metabolism and is a phosphotransferase that catalyzes the reversible transfer of phosphate from phosphoguanidine to ADP, resulting in generation of ATP [56]. In shrimps, Penm2 allergen gene having conserved guanidino specificity region and showing very high sequence similarity with crustacean arginine kinase has been isolated and characterized from
6.2. Ferritin
Ferritin plays a functional role in iron storage and metabolism. In shrimps, this large multifunctional and multisubunit protein gene has been isolated and characterized from
6.3. Intracellular fatty-acid-binding proteins
Intracellular fatty-acid-binding proteins (FABPs) are lipid-binding proteins that help in transport of fatty acids across extra- and intracellular membranes and are involved in various other biological processes such as modulation of signal transduction; gene transcription, especially of lipid metabolism; and cell growth and differentiation [67]. FABPs have been well-characterized in vertebrates as compared to that in invertebrates. In crustaceans, the FABP cDNA having fatty-acid-binding motifs has been cloned and characterized from the freshwater crayfish
6.4. Acyl-CoA binding protein
Acyl-CoA binding protein (ACBP) is a highly conserved protein. In yeast it is involved in transportation of acyl-CoA esters from the fatty acid synthetase to acyl-CoA-consuming process [70]. The protein, which was first identified in mammals, acts as a neuropeptide that prevents binding of diazepam/endozepine to GABA receptor system [71-72] and is also involved in regulation of several acyl-CoA-dependent processes [73]. In addition, ACBP is involved in many other functions, which include regulating biosynthesis of fatty acid, functional regulation of enzymes and genes, intracellular acyl-CoA pool regulation, acyl-CoA esters donation required for β-oxidation and vesicular trafficking [74], and in regulation of m-calpain [75]. In plants
6.5. Catechol-O-methyltransferase
O-methyltransferase (OMT) is an enzyme found in a wide range of organisms such as microbes [90], where it is involved in antibiotic biosynthesis [91], and in fungi, where it is involved in biosynthesis of aflatoxins [92]. The OMT found in plants are well characterized for their functional role in O-methylation during biosynthesis of lignin, stress resistance, and disease tolerance [93]. In crustaceans, farnesoic acid O-methyltransferase (FAMeT) catalyzes farnesoic acid methylation resulting in production of isoprenoid methyl farnesoate, which is involved in metabolic and physiological regulation [94]. Catechol-O-methyltransferase (COMT), which is a type of O-methyltransferases, helps in catalyzing the transfer of methyl group to the hydroxyl group of catechol compounds from S-adenosyl-L-methionine. In higher animals, the COMT helps in catalysis of methylation of various macromolecules that are involved in different functional and regulatory purposes and is present in soluble and membrane-bound forms [95]. In shrimps, the construction of suppression subtractive hybridization (SSH) libraries from
7. Stress genes
7.1. Heat shock proteins
Heat shock proteins (HSPs) initially discovered in
In conclusion, the construction of SSH cDNA library in response to low (3 ppt) and high (55 ppt) salinity stress in shrimp (
Acknowledgments
The authors wish to thank NAIP (ICAR) for the financial support provided under the NAIP project “Bioprospecting of genes and allele mining for abiotic stress tolerance.”
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