Abstract
Shrimp aquaculture is the rapidly growing sector of fish culture producing sectors in the world due to its rising demand in developed countries. Moreover, the intensive and extensive shrimp culture systems are affected mainly by infection diseases caused by several pathogenic agents and resulting in high economic losses. Nowadays, controlling and preventive infection diseases are the major concern to develop this sector. Besides, the highly extensive usage of chemotherapeutics and antibiotics induced numerous drawbacks in shrimp farming, developed antibiotic resistance bacterial strains, and threatens the aquatic life. Recently, improving the immunity status and controlling infectious diseases using biological methods have become beneficial, environment friendly, and risk-free options in aquaculture. Probiotics have gained much attention as immunostimulants in aquaculture owing to their inhibitory properties on pathogenic microorganisms via creation of an unfriendly atmosphere to cease their growth. Lactobacillus species as probiotics was used in shrimp aquaculture to prevent viral infections due to their positive promoting effects on survival and health. Additionally, Lactobacillus species possesses sturdy antimicrobial activity against various pathogenic microorganisms such as Photobacterium and Vibrio infections. This review threw the light on the applications of Lactobacillus sp. as probiotics in cultured shrimp which could be of great impact from a sustainable, intensive, and ecofriendly aquaculture opinion.
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Introduction
Shrimp culture is one of the most important subsectors of aquaculture that gains more attention due to shrimp vulnerability to stressful situations and undesirable environmental conditions and its high economic value (Al-Hakim et al. 2013). However, the development of intensive shrimp cultured systems has several drawbacks and economical losses because of diseases which are the main restriction on the productivity of several types of shrimp. As a result, large amounts of specifically antimicrobial compounds have been used in shrimp farming to manage and control diseases (Lakshmi et al. 2013; Mahrose et al. 2019). Nevertheless, several kinds of probiotics showed high efficiency towards diminishing the risk of diseases in addition to their economical properties such as Lactobacillus sp. (Iyapparaj et al. 2013; Ayyat et al. 2020).
In aquaculture, Litopenaeus vannamei (Pacific white shrimp) is considered the main important crustacean species and represents about 70% of the total shrimp production worldwide. Also, many species of probiotics could be isolated from L. vannamei, such as Lactobacillus spp. which is a widely applicable probiotic belonging to the Lactobacillus and Bifidobacterium genera (Chauhan and Singh 2019). Besides, they are classified as Gram-positive lactic acid–producing bacteria that modulate the majority of normal gut microbiota in humans and animals (Abd El-Naby et al. 2020; Arif et al. 2020). Characteristically, Lactobacilli are rod-shaped, non-spore forming bacteria (El-Shall et al. 2020). Their nutritional requirement is complex, and they are strictly fermentative, anaerobic or aerotolerant, and acidophilic or aciduric (Alagawany et al. 2018; Abd El-Aziz et al. 2020). In addition, Lactobacilli are found in various habitats particularly the substrates rich with carbohydrate such as animal and human mucosal membrane, plants or other plant-derived materials, fermented milk, spiled food, and sewage (de Vrese and Schrezenmeir 2008; Naiel et al. 2020b). Most of Lactobacillus species have the ability to produce strong antimicrobial molecules against many pathogenic microorganisms. The antibacterial activities of Lactobacilli may be due to their ability to produce a variety of antimicrobial substances including hydrogen peroxides, antimicrobial peptides, and organic acids (Fooks and Gibson 2002; Vieira et al. 2008; Abdel-Latif et al. 2020). For instance, Li et al. (2018) found that supplemented L. vannamei diets with Lactobacillus spp. significantly improved the performance, through enhancing the dominance of beneficial intestinal microorganisms and preventing the development of pathogenic bacterium. Awareness about the shrimp defense mechanisms is prospective to be useful in developing and adopting new effective strategies to resolve the current and future pathogen-related problems (Naiel et al. 2020c). For this purpose, there are various kinds of living microorganisms utilized for biocontrol typically applied in shrimp cultures. Currently, there are few commercial “intestinal” probiotics utilized specifically for the larval stage of different aquatic organisms (Vine et al. 2006; Abdel-Latif et al. 2020; Elgeddawy et al. 2020).
This review will discuss the recent findings of the vital roles of probiotics particularly; lactic acid species specifically Lactobacillus spp. in promoting the shrimp immune responses against common pathogens and understanding their impacts against ammonia production in rearing environment. In addition, the functional characterization of lactic acid bacteria on the sustainability of shrimp farming, biodiversity modulation action, and controlling pathogenic disease in aquatic environment.
The immunomodulatory role of lactic acid bacteria
There are several immune responses induced in shrimp like physical barriers, encapsulation, bacteria clearance, antimicrobial activity, pro-phenol-oxidase system, clotting reactions, and reactive oxygen intermediates. The innate immune response was induced under a diversity of PRR (pattern recognition receptors) on the hemocyte membranes to discover the PAMP (pathogen-associated molecule pattern) and reduce signals during the attack of pathogens. Then, hemocytes are activated, and the defense molecules are degranulated against the defined pathogens (Song and Li 2014).
Nowadays, there is recent trend towards using immunostimulatory natural products in the prevention and controlling diseases outbreaks in aquatic invertebrates, farmed shrimps, and fish (Abd El-Ghany et al. 2020; Khafaga et al. 2020). They have an extensive margin of safety than chemotherapeutics, and their spectral of efficacy is more than vaccination (Abdullateef et al. 2016; Naiel et al. 2020a).
Several kinds of lactic acid bacteria (LAB) have immunomodulatory properties and could be utilized as probiotics (Alagawany et al. 2020), in which common lactic acid bacterial strains have been presented in Table 1. Chomwong et al. (2018) found that the use of L. lactis and L. plantarum could promote the shrimp immune response against VPAHPND infection and increase survival rate. Also, Le and Yang (2018) reported that L. sakei induced higher coaggregations and immunomodulatory activities than L. plantarum in gastrointestinal tract. Besides, Maeda et al. (2014) investigated the immunomodulatory role of LAB in the enhancement of the kuruma shrimp (Marsupenaeus japonicus) immune system and recommended its use as active probiotics in shrimp aquaculture.
In shrimp, some bacterial strains stimulated both the humoral and cellular immune defense systems. Fed white shrimp, Litopenaeus vannamei, supplemented diets with 1010 CFU (kg diet−1) of Lactobacillus plantarum enhance the immune responses and upregulated immune relative gene expression for 168 h. This may be attributed to the role of L. plantarum in activation of the pro-phenol-oxidase (Pro. PO), phenol-oxidase (PO), and superoxide dismutase (SOD) activities, respiratory bursts (RB), and peroxinectin mRNA transcription and increased the rate of survival after V. alginolyticus challenge (Chiu et al. 2007). Also, Lactobacillus bulgaricus improved both the humoral and cellular immune defense activities in the white shrimp, Litopenaeus vannamei, in terms of increasing hemocyte counts, PO, and RB activity and reduced shrimp mortality after challenged with V. parahaemolyticus (Roomiani et al. 2018). Huynh et al. (2018) suggested that Lactobacillus plantarum could modulate the immune system of Litopenaeus vannamei by increasing the levels of several metabolites such as inosine monophosphate (IMP), valine, and betaine.
Likewise, feeding of Penaeus vannamei on diets supplemented with the LAB (Bacillus subtilis and Lactobacillus rhamnosus) enhanced the antioxidative status by increasing the antioxidant enzymes activity in shrimps (Kumar et al. 2013). Thus, shrimp diets treated with bio-friendly agents such as Lactobacillus spp. could be used as effective alternatives to antibiotics for treating bacterial infections especially V. harveyi infection in shrimp aquaculture (Ahmmed et al. 2018). In addition, feeding of kuruma shrimp (Marsupenaeus japonicus) at larval and post-larval stages on diets supplemented with heat-killed Lactobacillus plantarum (HK-LP) could reduce the harmful impacts induced by unsuitable manipulation and environmental conditions (Thanh Tung et al. 2010). The improvement of survivability in both larvae and post-larval stages and the growth performance in the post-larvae may be due to the effect of HK-LP administration in promoting the uncompleted innate immune defense at the early stages. Besides, Zheng et al. (2017) suggested that dietary administration of Lactobacillus plantarum, particularly cell-free extract, could enhance the capacity of L. vannamei shrimp against stress and upregulate the Pro. Po, SOD, and lysozyme gene expression, thereby helping shrimp to counteract the surrounding environmental stressors. The immunostimulatory role of Lactobacillus plantarum as a probiotic makes it to be recommended as a dietary supplement to enhance the shrimp defense against pathogenic agents such as Vibrio harveyi (Vieira et al. 2010).
The protective role of lactic acid bacteria against viral diseases
Viral diseases are one of the major problems which lead to economic losses and decrease the productivity in shrimp farms (Israngkura and Sae-Hae 2002). Probiotics in addition to be beneficial bacteria they also have antiviral activities. Therefore, the exploitation of probiotics in the prevention and treatment of viral infections in shrimp aquacultures is an efficient novel method. Besides, the immunological and protective effects of lactic acid bacterial strains against infection diseases had been illustrated in Table 2.
The antiviral activity of probiotic lactic acid bacteria mainly depends on bacterial strain. Also, the antiviral affects may be attributed to the interaction between bacterial cell and virus, to the ability of bacterial cell to produce the antiviral bacterial derivatives, or to the immunomodulatory role of probiotic towards activation of the immune system (Al Kassaa et al. 2014). The interaction between bacterial cell and virus could be possible through absorbed and/or trapped mechanisms which inhibited virus’s proliferation (Al Kassaa et al. 2014). Furthermore, the probiotics are well verified to exert several compounds such as interleukins, natural killer cells, macro-phages, immunoglobulins, and T helper cells action that can promote the defensive immune system defenses against the virus (Cha et al. 2012). Besides, the bacterial strains could produce several constitutes including hydrogen peroxide (H2O2), lactic acid, bacteriocins and bacteriocin-like substances, short-chain fatty acids, and polysaccharides that helped for detecting viral infection and enhanced the antiviral activity (Conti et al. 2009; Arena et al. 2018). All the above-mentioned molecules are exerted into culture intermediate; thus, the bacterial cell-free supernatant (CFS) might include such products. Certainly, CFSs are commonly defined to preliminarily illustrate the probable antagonistic ability of bacteria (Wang et al. 2013; Arena et al. 2016).
One of the most important virulent pathogens in penaeid shrimps is the WSSV (white spot syndrome virus). It caused strong economic losses in the shrimp industry worldwide because it can induce up to 100% accumulative mortalities within 3–10 days. Peraza-Gómez et al. (2009) indicate that the LAB and yeast could protect the Litopenaeus vannamei culture against the WSSV infection. Moreover, Jiravanichpaisal et al. (1997) recommended the use of Lactobacillus sp. as probiotic in Penaeus monodon Fabricius (the giant tiger shrimp) as an effective treatment against white spot diseases and vibriosis.
Pooljun et al. (2020) confirmed that enriched juvenile shrimp (Penaeus vannamei)-fed diets with L. acidophilus and S. cerevisiae mixture (1:1, at 108 and 109 CFU kg diet−1) impaired the adverse effects induced by Vibrio parahaemolyticus infection (acute hepatopancreas necrosis disease, AHPND) via improved hemocyte parameters, including the total hemocyte count, granular hemocytes percentage, and phenol-oxidase activity as well as highly upregulated hemocytes genes (Crustin and penaeidin) and led to high survival rate. Recently, de Souza et al. (2020) investigated that allocated pacific white shrimp, Litopenaeus vannamei, in biofloc system (water contain beneficial bacterial strain) improved immune response against white spot syndrome virus (WSSV) infection through upregulated calreticulin, β-tubulin, and pro-phenol-oxidase genes in hepatopancreas cells. Besides, Li et al. (2020) amplified that fortified pacific white shrimp, Litopenaeus vannamei, diets with 4 mg/kg arabinoxylan-oligosaccharide (AXOS) increased lactate production levels in gastrointestinal tract thus enriched Bacillus, Pseudomonas, Bacteriovorax, and Lactobacillus development and subsequently remarkably upregulated immune-related genes (chitinase, cathepsin L, chymotrypsin, MyD88, and PO) in shrimp infected with Vibrio alginolyticus (white spot syndrome virus).
Various Lactobacillus species exerts extracellular glycoproteins and inhibiting pathogen from attachment with intestinal epithelia cells (Liu et al. 2020). Moreover, attachment, while diminishing mobility, is vital for biofilm formation process (surface cell–attached microbial communities) (Johnson-Henry et al. 2007). The development of adherent cells in biofilms can also encourage the fast elimination of nonadhesive cells from the microbiota (Knipe et al. 2020). For instance, fed penaeid shrimp with L. plantarum strains (at 107 CFUs ml−1 seawater)–supplemented diet protected shrimp against V. parahaemolyticus infection (acute hepatopancreatic necrosis disease, AHPND) (Thammasorn et al. 2017).
Antibacterial role of the lactic acid bacteria
In addition to viruses, bacterial diseases are one of the major infectious agents that cause high mortality and morbidity in shrimp industry. Gram-negative bacteria and several Vibrio species are more virulent than others in shrimp aquaculture (Vieira et al. 2008). (Abdullateef et al. 2016). Thus, improving the health status of culture organisms using beneficial microbes as probiotic is the better method to control the pathogens (Karthik et al. 2014).
Several studies had proved the antibacterial role of Lactobacillus pentosus) AS13( dietary administration against vibriosis and its efficiency on enhancing performance, feed utilization, and the activities of digestive enzymes in the white shrimp, Litopenaeus vannamei (Zheng and Wang 2017). Additionally, Nguyen et al. (2018) presented the evidence on the positive effects of the probiotic Lactobacillus plantarum on growth and resistance of Litopenaeus vannamei against Vibrio parahaemolyticus which causes acute hepatopancreatic necrosis disease (AHPND). Similarly, Le and Yang (2018) stated that Lactobacillus strains could prevent Vibrio infection in the shrimp cultures. In addition, Chomwong et al. (2018) confirmed the antimicrobial activity of two LAB (Lactococcus lactis strain SGLAB02 and Lactobacillus plantarum strain SGLAB01) against gram-negative and gram-positive bacteria, including the Vibrio parahaemolyticus (VPAHPND) which cause the virulent acute hepatopancreatic necrosis disease (AHPND). Likewise, L. acidophilus exhibited antibacterial activities against Vibrio cholera, Vibrio parahaemolyticus, and Vibrio Harveyi (Natesan et al. 2012).
Moreover, Rengpipat et al. (2000) showed that Bacillus Sll provided protection against diseases by activating P. monodon immunological responses. Also, Maeda et al. (2014) indicated that LAB induced or increased the expressions of innate immune genes and enhanced the resistance of kuruma shrimp (Marsupenaeus japonicus) to bacterial pathogens. The Lactobacillus spp. (JK-8 and JK-11) was reported to be able to completely remove both nitrogen and pathogens (Ma et al. 2009). Furthermore, Lactobacillus plantarum has already been reported to decrease the rate of mortality of Litopenaeus vannamei larvae and improved their resistance against Vibrio harveyi infection (Vieira et al. 2007).
The supplementation of diet with Lactobacillus plantarum reduced the mortality rate, modified the intestinal microbiota, decreased the abundance of Vibrio spp., and increased the abundance of LAB in shrimp raised in a commercial farm (Vieira et al. 2016a). This mode of action may be due to that the prevalent bacteria can survive by exerting antimicrobial molecules which may kill or prevent all their bacterial competitors (Sivakumar et al. 2014). Huynh et al. (2019) found that feeding of white shrimp on Lactobacillus plantarum supplemented diets encouraged the colonization of Lactobacillus plantarum and decreased the prevalence of pathogenic microorganisms, such as Vibrio and Photobacterium in gastrointestinal tract. The dietary supplementation of Lactobacillus increased their count in the L. vannamei intestine and significantly reduced the load of pathogenic bacteria (e.g., Vibrio) (Karthik et al. 2014). At the same trend, Vieira et al. (2016b) confirmed the ability of Lactobacillus plantarum to modify the microbiota in the L. vannamei shrimp mid gut by increasing the number of LAB and decreasing Vibrio spp. Phianphak et al. (1999) also stated that Lactobacillus sp. reveals potential of control Vibrio harveyi infection in the shrimp gut and provides healthy shrimp protected against such diseases.
The inhibition of Vibrio alginolyticus by dietary LAB (Lactobacillus acidophilus, Streptococcus cremoris, Lactobacillus bulgaricus, and Lactobacillus bulgaricus) may be related to their roles in promoting the nonspecific immune activities resulting in resistance to disease in Penaeus indicus shrimp (AJITHA et al. 2004). Consequently, it could be concluded that several Lactobacillus strains such as Lactobacillus acidophilus will be of great importance in the management of Vibrio alginolyticus and other related bacterial diseases in juvenile, Penaeus monodon, tiger shrimp (Uma et al. 1999).
In addition, fortified L. vannamei shrimp diets with Lactobacillus developed the Lactobacillus sp. count in gastrointestinal tract and subsequently reduced the total pathogenic bacterial count (e.g., Vibrio) (Li et al. 2018). Thus, the Lactobacillus sp. (AMET1506) strain can be a probable probiotic for L. vannamei to prevent and control vibriosis infections in shrimp farming; this phenomenon arises partially by enhancement of gastrointestinal microbiota biodiversity (Kumar et al. 2016).
The application of LAB in shrimp cultured systems
The concentration of total ammonium nitrogen (TAN) is often a key limiting water quality parameter in the intensive systems of aquaculture. Therefore, removing of ammonia (NH3) by biological activities is thus an important aim in recycled and conventional aquaculture system designs (Grommen et al. 2002). In shrimp pond, controlling the ammonia production depends on other water quality elements such as pH, dissolved oxygen, and water temperature. Herein, fortified shrimp-fed diets with probiotic would be a beneficial strategy to promote shrimp health under several aquatic stressful conditions (Wongsasak et al. 2015). Lactobacillus species have been recognized for their nutritional and health benefits in addition to their fermentative ability. In all respect, Sivakumar et al. (2014) stated that the utilization of Lactobacillus sp. is beneficial in improving the water quality and the environment in the shrimp aquaculture. Additionally, Ma et al. (2009) investigated that both Lactobacillus strains (JK-8 and JK-11) had the ability to remove up to 400 μM from NH4+, NO2−, and NO3− in vitro. The Lactobacillus species could exerts several compounds during the lactic fermentation process, such as organic acids, di-acetyl-hydrogen peroxide, and bactericidal proteins that subsequently led to decrease the pH value from 7 to 5.4, which might be adequate to prevent the development of many pathogenic bacteria and nitrification process (Farzanfar 2006; Ma et al. 2009). Also, Zubaidah et al. (2012) revealed that the charpness decreased in pH values may be due Lactobacillus spp. activity which is naturally occurring during fermentation process (fermented carbon resource such as rice bran).
With regard to the harmful effects of ammonia, Liu and Chen (2004) stated that ambient ammonia reduced the resistance of Litopenaeus vannamei to Vibrio infection by decreasing the phagocytic and SOD activities and increasing the superoxide anions which may be toxic to the host (Ma et al. 2009). Hence, supplemented L. vannamei diet with 1010 CFU (kg diet−1) L. plantarum enhanced immune response and promoted the immune activity towards V. alginolyticus infection via stimulating PO and SOD activity (Chiu et al. 2007). Therefore, Lactobacillus spp. (JK-8 and JK-11) will be helpful for improving the quality of water, facing bacterial infections and highly reduced nitrogen content in shrimp farms.
Furthermore, the application of lactic acid bacteria on shrimp rearing water, gastrointestinal microbiota, and decreasing the water salinity levels are a wide spreading methods having importance in controlling pathogens in shrimp farming (Krishnaprakash et al. 2009). At the same trend, supplied rearing water with 1 × 103 CFU/ml Bacillus vallismortis W120 showed the ability to control pathogenic bacteria, Aeromonas hydrophila WS1, in fairy shrimp culture (Purivirojkul 2013). Treated shrimp ponds with lactic acid bacteria had less prevalence of pathogenic bacterium such as Vibrio as well as reduced toxic gases production like ammonia, nitrite, and hydrogen sulfide, compared with untreated ponds (Jha 2011). Also, Kumar et al. (2014) reported the synergistic effects between two probiotic bacteria strains that promoted growth and biochemical and immunological status of Litopenaeus vannamei.
With regard to the aquamimicry systems, it needs to sustain the beneficial heterotrophic bacterial stains such as Bacillus spp. to maintain the desired water quality parameters, fermented the available carbon resource, and suspended high amount of biofloc farming. Despite of the heterotrophic bacteria should not be dominated in this system. Some farmers have noticed that adding lower quantities of fermented rice bran daily (2 mg/l) could enrichment the development of some zooplankton, microalgae, and flocs that daily regulate the pH instabilities (Romano 2017). The higher concentration of heterotrophic bacteria led to rapidly convert dissolved free nitrogen into natural microbial biomass. Actually, heterotrophic bacteria can be developed fastly up to 10 times more than nitrification bacterium and thus markedly minimized the time required to remove the toxic from of ammonia-N (reduced nitrite-N levels) (Hargreaves 2006). The aggregates floc community produced by heterotrophic bacteria may lead to higher fish performance, amplified the activity of digestive enzyme, and/or improved the resistance against infectious disease (Dauda et al. 2018). In addition, De Paiva-Maia et al. (2013) showed that the probiotics (Bacillus spp. and Lactobacillus yeasts) caused alterations in the total heterotrophic microbiota in the sediments and percentages of Pyrrophyta concentrations and improved the environmental quality of water and sediment in grow-out intensive shrimp ponds (Litopenaeus vannamei) with closed recirculation system. In another study, the biodiversity of bacterial community in aquacultures and the relationships between potential pathogenic bacteria and aquacultures environment in sediment and water samples from culture ponds of L. vannamei were analyzed by sequencing of the 16S rRNA gene through Illumina MiSeq and Roche 454 sequencing platforms, and this provided novel information about improving the microflora in aquaculture environment and inhibition of pathogen to reduce the infection by L. vannamei disease through the regulating of the environmental conditions (Zhang et al. 2016).
Conclusion
This review provided useful insights for the use of Lactobacillus sp. in cultured shrimp. Enhancing the health status of cultured shrimp by using beneficial microbes as a probiotic is the best approach to control pathogens. Lactobacillus sp. showed an effective role in producing resistance to infectious agents and in creating antibacterial substances that stop pathogenic microorganisms from getting into the organism. Thus, administration of Lactobacillus sp. in cultured shrimp can improve the quality of rearing water and enhance the immune response of the shrimp. Future studies need to be further extended by investigating the involvement of Lactobacillus sp. in the modulation of adaptive immune response.
Data availability
The data that support the findings of this study are available on request from the corresponding author.
References
Abd El-Aziz AH, El-Kasrawy NI, Abd El-Hack ME, Kamel SZ, Mahrous UE, El-Deeb EM, Atta MS, Amer MS, Naiel MA, Khafaga AF (2020) Growth, immunity, relative gene expression, carcass traits and economic efficiency of two rabbit breeds fed prebiotic supplemented diets. Ani. Biotechnol: 1-12
Abd El-Ghany MF, El-Sawy HB, Abd El-hameed SA, Khames MK, Abdel-Latif HM, Naiel MA (2020) Effects of dietary Nannochloropsis oculata on growth performance, serum biochemical parameters, immune responses, and resistance against Aeromonas veronii challenge in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 107:277–288
Abd El-Naby AS, Al-Sagheer AA, Negm SS, Naiel MA (2020) Dietary combination of chitosan nanoparticle and thymol affects feed utilization, digestive enzymes, antioxidant status, and intestinal morphology of Oreochromis niloticus. Aquac. 515:734577
Abdel-Latif HM, Soliman AA, Sewilam H, Almeer R, Van Doan H, Alagawany M, Dawood MA (2020) The influence of raffinose on the growth performance, oxidative status, and immunity in Nile tilapia (Oreochromis niloticus). Aquac Rep 18:100457
Abdullateef A, Sabri M, Babatunde DA, MY IS, Hasliza A (2016) Immunoprophylaxis: a better alternative protective measure against shrimp vibriosis–a review. PJSRR 2:58–69
Ahmmed F, Ahmmed MK, Shah MS, Banu GR (2018) Use of indigenous beneficial bacteria (Lactobacillus spp.) as probiotics in shrimp (Penaeus monodon) aquaculture. Agric Liv Fish 5:127–135
Ajitha S, Sridhar M, Sridhar N, Singh ISB, Varghese V (2004) Probiotic effects of lactic acid Bacteria against Vibrio Alginolyticus in Penaeus (Fenneropenaeus) Indicus (H.Milne Edwards). Asian Fisheries Sci 17:71–80
Al Kassaa I, Hamze M, Hober D, Chihib N-E, Drider D (2014) Identification of vaginal lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb Ecol 67:722–734
Alagawany M, Abd El-Hack ME, Farag MR, Sachan S, Karthik K, Dhama K (2018) The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ Sci Pollut Res 25:10611–10618
Alagawany M, Abd El-Hack ME, Farag MR, Shaheen HM, Abdel-Latif MA, Noreldin AE, Khafaga AF (2020) The applications of Origanum vulgare and its derivatives in human, ruminant and fish nutrition–a review. Annals Ani Sci 20:389–407
Alavandi S, Vijayan K, Santiago T, Poornima M, Jithendran K, Ali S, Rajan J (2004) Evaluation of Pseudomonas sp. PM 11 and Vibrio fluvialis PM 17 on immune indices of tiger shrimp, Penaeus monodon. Fish Shellfish Immunol 17:115–120
Al-Hakim A, Nabil F, Al-Azab A-DA, Allam HY, Gewida AG (2013) Effect of stocking density and probiotic dietary supplementation on growth performance, feed conversion and survival of postlarvae of the freshwater prawn (Macrobrachium Rosenbergii). Egy J Aquatic Biol Fish 287:1–22
Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D (2016) Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464
Arena MP, Elmastour F, Sane F, Drider D, Fiocco D, Spano G, Hober D (2018) Inhibition of Coxsackievirus B4 by Lactobacillus plantarum. Microbiol Res 210:59–64
Arif M, Iram A, Bhutta MA, Naiel MA, El-Hack A, Mohamed E, Othman SI, Allam AA, Amer MS, Taha AE (2020) The biodegradation role of Saccharomyces cerevisiae against harmful effects of mycotoxin contaminated diets on broiler performance, immunity status, and carcass characteristics. Animals. 10:238
Ayyat MS, Ayyat AM, Naiel MA, Al-Sagheer AA (2020) Reversal effects of some safe dietary supplements on lead contaminated diet induced impaired growth and associated parameters in Nile tilapia. Aquac. 515:734580
Balcazar J (2002) Use of probiotics in aquaculture: general aspects, Memorias del Primer Congreso Iberoamericano. Virtual de Acuicultura, Zaragoza, pp 877–881
Cha M-K, Lee D-K, An H-M, Lee S-W, Shin S-H, Kwon J-H, Kim K-J, Ha N-J (2012) Antiviral activity of Bifidobacterium adolescentis SPM1005-a on human papilloma virus type 16. BMC Med 10:72
Chauhan A, Singh R (2019) Probiotics in aquaculture: a promising emerging alternative approach. Symbiosis. 77:99–113
Chiu C-H, Guu Y-K, Liu C-H, Pan T-M, Cheng WJF, Immunology S (2007) Immune responses and gene expression in white shrimp, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish Shellfish Immunol 23:364–377
Chomwong S, Charoensapsri W, Amparyup P, Tassanakajon AJD, Immunology C (2018) Two host gut-derived lactic acid bacteria activate the proPO system and increase resistance to an AHPND-causing strain of Vibrio parahaemolyticus in the shrimp Litopenaeus vannamei. Dev Comp Immunol 89:54–65
Conti C, Malacrino C, Mastromarino P (2009) Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J Physiol Pharmacol 60:19–26
Dauda AB, Romano N, Ebrahimi M, Teh JC, Ajadi A, Chong CM, Karim M, Natrah I, Kamarudin MS (2018) Influence of carbon/nitrogen ratios on biofloc production and biochemical composition and subsequent effects on the growth, physiological status and disease resistance of African catfish (Clarias gariepinus) cultured in glycerol-based biofloc systems. Aquac. 483:120–130
De Paiva-Maia E, Alves-Modesto G, Otavio-Brito L, Vasconcelos-Gesteira T, Olivera A, Vasconcelos-Gesteira T (2013) Effect of a commercial probiotic on bacterial and phytoplankton concentration in intensive shrimp farming (Litopenaeus vannamei) recirculation systems. Latin Am J Aquatic Res 41:126–137
de Souza VC, Ortiz KO, Depperschmidt R, de Medeiros Fraga AP, do Nascimento Vieira F, Marques MRF (2020) Transcription of defense related genes in Pacific white shrimp, Litopenaeus vannamei, kept in biofloc and in clear seawater and challenged with the white spot syndrome virus. Aquac Int 28:293–307
de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. In: Stahl U, Donalies UEB, Nevoigt E (eds) Food biotechnology. Springer Berlin Heidelberg, Heidelberg, pp 1–66
Elgeddawy SA, Shaheen HM, El-Sayed YS, Abd Elaziz M, Darwish A, Samak D, Batiha GE, Mady RA, Bin-Jumah M, Allam AA (2020) Effects of the dietary inclusion of a probiotic or prebiotic on florfenicol pharmacokinetic profile in broiler chicken. J Anim Physiol Anim Nutr 104:549–557
El-Shall NA, Awad AM, El-Hack MEA, Naiel MA, Othman SI, Allam AA, Sedeik ME (2020) The simultaneous administration of a probiotic or prebiotic with live Salmonella vaccine improves growth performance and reduces fecal shedding of the bacterium in Salmonella-challenged broilers. Animals. 10:70
Farzanfar A (2006) The use of probiotics in shrimp aquaculture. FEMS Immunol Med Microbiol 48:149–158
Fooks L, Gibson GR (2002) Probiotics as modulators of the gut flora. Br J Nutr 88:s39–s49
Grommen R, Van Hauteghem I, Van Wambeke M, Verstraete W (2002) An improved nitrifying enrichment to remove ammonium and nitrite from freshwater aquaria systems. Aquacu. 211:115–124
Hargreaves JA (2006) Photosynthetic suspended-growth systems in aquaculture. Aquac Eng 34:344–363
Huynh T-G, Cheng A-C, Chi C-C, Chiu K-H, Liu C-H (2018) A synbiotic improves the immunity of white shrimp, Litopenaeus vannamei: Metabolomic analysis reveal compelling evidence. Fish Shellfish Immunol 79:284–293
Huynh T-G, Hu S-Y, Chiu C-S, Truong Q-P, Liu C-H (2019) Bacterial population in intestines of white shrimp, Litopenaeus vannamei fed a synbiotic containing Lactobacillus plantarum and galactooligosaccharide. Aquac Res 50:807–817
Israngkura A, Sae-Hae S (2002) A review of the economic impacts of aquatic animal disease. FAO fisheries technical paper: 253-286
Iyapparaj P, Maruthiah T, Ramasubburayan R, Prakash S, Kumar C, Immanuel G, Palavesam A (2013) Optimization of bacteriocin production by Lactobacillus sp. MSU3IR against shrimp bacterial pathogens. Aquatic. Biosystems 9:12
Jha AK (2011) Probiotic technology: an effective means for bioremediation in shrimp farming ponds. J Bangladesh Acad Sci 35:237–240
Jiravanichpaisal P, Chuaychuwong P, Menasveta P (1997) The use of Lactobacillus sp. as the probiotic bacteria in the giant tiger shrimp (Penaeus monodon Fabricius), poster session of the second Asia-Pacific marine biotechnology conference and third Asia-pacific conference on algal Biotechnology, pp. 7–10
Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM (2007) Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157: H7 adhesion to epithelial cells. Cell Microbiol 9:356–367
Karthik R, Hussain AJ, Muthezhilan R (2014) Effectiveness of Lactobacillus sp (AMET1506) as probiotic against vibriosis in Penaeus monodon and Litopenaeus vannamei shrimp aquaculture. Biosci Biotechnol Res Asia 11:297–305
Khafaga AF, Naiel MA, Dawood MA, Abdel-Latif HM (2020) Dietary Origanum vulgare essential oil attenuates cypermethrin-induced biochemical changes, oxidative stress, histopathological alterations, apoptosis, and reduces DNA damage in common carp (Cyprinus carpio). Aquat Toxicol 228:105624
Knipe H, Temperton B, Lange A, Bass D, Tyler CR (2020) Probiotics and competitive exclusion of pathogens in shrimp aquaculture. Rev. in Aquac.N/A. https://doi.org/10.1111/raq.12477
Kongnum K, Hongpattarakere T (2012) Effect of Lactobacillus plantarum isolated from digestive tract of wild shrimp on growth and survival of white shrimp (Litopenaeus vannamei) challenged with Vibrio harveyi. Fish & Shellfish Immunology 32(1):170–177
Krishnaprakash R, Saravanan R, Murugesan P, Rajagopal S (2009) Usefulness of probiotics in the production of high quality shrimp (Penaeus monodon) seeds in hatcheries. World J Zool 4:144–147
Kumar PNJ, Jyothsna R, Reddy MH, Sreevani SPR (2013) Effect of Bacillus subtilis and Lactobacillus rhamnosus incorporated probiotic diet on growth pattern and enzymes in Penaeus vannamei. Int J Life Sci Pharm Res 3:6–11
Kumar A, Suresh Babu P, Roy S, Razvi S, Charan R (2014) Synergistic effects of two probiotic bacteria on growth, biochemical, and immunological responses of Litopenaeus vannamei (Boone, 1931). Isr J Aquac-Bamidgeh 66:1–8
Kumar V, Roy S, Meena DK, Sarkar UK (2016) Application of probiotics in shrimp aquaculture: importance, mechanisms of action, and methods of administration. Rev Fish Sci Aquac 24:342–368
Lakshmi B, Viswanath B, Sai Gopal D (2013) Probiotics as antiviral agents in shrimp aquaculture. J Pathogens 2013:1–13
Le B, Yang SH (2018) Probiotic potential of novel Lactobacillus strains isolated from salted-fermented shrimp as antagonists for Vibrio parahaemolyticus. J Microbiol 56:138–144
Li E, Xu C, Wang X, Wang S, Zhao Q, Zhang M, Qin JG, Chen L (2018) Gut microbiota and its modulation for healthy farming of Pacific white shrimp Litopenaeus vannamei. Rev Fish Sci Aquac 26:381–399
Li Y, Yuan W, Zhang Y, Liu H, Dai X (2020) Single or combined effects of dietary arabinoxylan-oligosaccharide and inulin on growth performance, gut microbiota, and immune response in Pacific white shrimp Litopenaeus vannamei. J Oceanol Limnol: 1-14
Liu C-H, Chen J-C (2004) Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus. Fish Shellfish Immunol 16:321–334
Liu Q, Yu Z, Tian F, Zhao J, Zhang H, Zhai Q, Chen W (2020) Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier. Microb Cell Factories 19:23
Ma C-W, Cho Y-S, Oh K-HJA (2009) Removal of pathogenic bacteria and nitrogens by Lactobacillus spp. JK-8 and JK-11. Aquac. 287:266–270
Maeda M, Shibata A, Biswas G, Korenaga H, Kono T, Itami T, Sakai M (2014) Isolation of lactic acid bacteria from kuruma shrimp (Marsupenaeus japonicus) intestine and assessment of Immunomodulatory role of a selected strain as probiotic. Mar Biotechnol 16:181–192
Mahrose KM, Elhack ME, Mahgoub SA, Attia FA (2019) Influences of stocking density and dietary probiotic supplementation on growing Japanese quail performance. An Acad Bras Ciênc 91:e20180616
Moriarty D (1998) Control of luminous Vibrio species in penaeid aquaculture ponds. Aquac. 164:351–358
Naiel MA, Ismael NE, Abd El-hameed SA, Amer MS (2020a) The antioxidative and immunity roles of chitosan nanoparticle and vitamin C-supplemented diets against imidacloprid toxicity on Oreochromis niloticus. Aquaculture 523:735219
Naiel MA, Ismael NE, Negm SS, Ayyat MS, Al-Sagheer AA (2020b) Rosemary leaf powder–supplemented diet enhances performance, antioxidant properties, immune status, and resistance against bacterial diseases in Nile tilapia (Oreochromis niloticus). Aquaculture 526:735370
Naiel MA, Shehata AM, Negm SS, Abd El-Hack ME, Amer MS, Khafaga AF, Bin-Jumah M, Allam AA (2020c) The new aspects of using some safe feed additives on alleviated imidacloprid toxicity in farmed fish: a review. Rev. in Aquac. N/A. https://doi.org/10.1111/raq.12432. Accessed 14 Aug 2020
Natesan S, Muthuraman S, Gopal S (2012) Probiotic effect of Lactobacillus acidophilus against vibriosis in juvenile shrimp (Penaeus monodon). Afr J Biotechnol 11:15811–15818
Nguyen TTG, Nguyen TC, Leelakriangsak M, Pham TT, Pham QH, Lueangthuwapranit CJTM (2018) Promotion of Lactobacillus plantarum on growth and resistance against acute hepatopancreatic necrosis disease pathogens in white-leg shrimp (Litopenaeus vannamei). Thi J Sci 48:19–28
Olmos J, Ochoa L, Paniagua-Michel J, Contreras R (2011) Functional feed assessment on Litopenaeus vannamei using 100% fish meal replacement by soybean meal, high levels of complex carbohydrates and Bacillus probiotic strains. Marine Drugs 9:1119–1132
Pacheco-Vega JM, Cadena-Roa MA, Leyva-Flores JA, Zavala-Leal OI, Pérez-Bravo E, Ruiz-Velazco JM (2018) Effect of isolated bacteria and microalgae on the biofloc characteristics in the Pacific white shrimp culture. Aquaculture Reports 11:24–30
Peraza-Gómez V, Luna-González A, Campa-Córdova ÁI, López-Meyer M, Fierro-Coronado JA, Álvarez-Ruiz P (2009) Probiotic microorganisms and antiviral plants reduce mortality and prevalence of WSSV in shrimp (Litopenaeus vannamei) cultured under laboratory conditions. Aquac Res 40:1481–1489
Phianphak W, Rengpipat S, Piyatiratitivorakul S, Menasveta P (1999) Probiotic use of Lactobacillus spp. for black tiger shrimp, Penaeus monodon. J Sci Res Chula Univ 24:41–58
Pooljun C, Daorueang S, Weerachatyanukul W, Direkbusarakom S, Jariyapong P (2020) Enhancement of shrimp health and immunity with diets supplemented with combined probiotics: application to Vibrio parahaemolyticus infections. Dis Aquat Org 140:37–46
Purivirojkul W (2013) Application of probiotic bacteria for controlling pathogenic bacteria in fairy shrimp Branchinella thailandensis culture. Turk J Fish Aquat Sci 13:187–196
Ramírez NCB, Rodrigues MS, Guimarães AM, Guertler C, Rosa JR, Seiffert WQ, Vieira FDN (2017) Effect of dietary supplementation with butyrate and probiotic on the survival of Pacific white shrimp after challenge with Vibrio alginolyticus. Revista Brasileira de Zootecnia 46(6):471–477
Rengpipat S, Phianphak W, Piyatiratitivorakul S, Menasveta P (1998) Effects of a probiotic bacterium on black tiger shrimp Penaeus monodon survival and growth. Aquac. 167:301–313
Rengpipat S, Rukpratanporn S, Piyatiratitivorakul S, Menasaveta P (2000) Immunity enhancement in black tiger shrimp (Penaeus monodon) by a probiont bacterium (Bacillus S11). Aquac. 191:271–288
Romano N (2017) Aquamimicry: a revolutionary concept for shrimp farming. Global Aquac. Adv. Retrieved: August 14, 2020. http://courseware.cutm.ac.in/wp-content/uploads/2020/06/Lecture-10.pdf
Roomiani L, Ahmadi S, Ghaeni MJAÜVFD (2018) Immune response and disease resistance in the white shrimp, Litopenaeus vannamei induced by potential probiotic Lactobacillus. Unk Uni Vet Fak Der 65:323–329
Sha Y, Wang L, Liu M, Jiang K, Xin F, Wang B (2016) Effects of lactic acid bacteria and the corresponding supernatant on the survival, growth performance, immune response and disease resistance of Litopenaeus vannamei. Aquaculture 452:28–36
Sivakumar N, Selvakumar G, Varalakshmi P, Ashokkumar B (2014) Lactobacillus sp. a potent probiotic for disease free shrimp aquaqulture. Inte J Recent Sci Res 5:1031–1045
Song Y-L, Li C-Y (2014) Shrimp immune system-special focus on penaeidin. J Mar Sci Technol 22:1–8
Thammasorn T, Jitrakorn S, Charoonnart P, Sirimanakul S, Rattanarojpong T, Chaturongakul S, Saksmerprome V (2017) Probiotic bacteria (Lactobacillus plantarum) expressing specific double-stranded RNA and its potential for controlling shrimp viral and bacterial diseases. Aquac Int 25:1679–1692
Thanh Tung H, Koshio S, Ferdinand Traifalgar R, Ishikawa M, Yokoyama S (2010) Effects of dietary heat-killed Lactobacillus plantarum on larval and post-larval kuruma shrimp, Marsupenaeus japonicus Bate. J World Aquacult Soc 41:16–27
Uma A, Abraham TJ, Sundararaj V (1999) Effect of a probiotic hacterium, Lactobacillus plantarum on disease resistance of Penaeus indicus larvae. Indian J Fish 46:367–373
Vieira FN, Pedrotti FS, Buglione Neto CC, Mouriño JLP, Beltrame E, Martins ML, Ramirez C, Arana LAV (2007) Lactic-acid bacteria increase the survival of marine shrimp, Litopenaeus vannamei, after infection with Vibrio harveyi. Braz J Oceanogr 55:251–255
Vieira FN, Buglione Neto CC, Mouriño JLP, Jatobá A, Ramirez C, Martins ML, Barracco MAAM, Vinatea LAJPAB (2008) Time-related action of Lactobacillus plantarum in the bacterial microbiota of shrimp digestive tract and its action as immunostimulant. Pesq Agrop Brasileira 43:763–769
Vieira F, Buglione CC, Mourino JPL, Jatobá A, Martins ML, Schleder DD, Andreatta ER, Barraco MA, Vinatea L (2010) Effect of probiotic supplemented diet on marine shrimp survival after challenge with Vibrio harveyi. Arquivo Brasileiro de Med Vet e Zootecnia 62:631–638
Vieira FN, Jatobá A, Mouriño JLP, Buglione Neto CC, Silva JS, Seiffert WQ, Soares M, Vinatea LA (2016a) Use of probiotic-supplemented diet on a Pacific white shrimp farm. J Rev Brasileira de Zootecnia 45:203–207
Vieira GRAS, Soares M, Ramírez NCB, Schleder DD, Silva BC, Mouriño JLP, Andreatta ER, Vieira FN (2016b) Lactic acid bacteria used as preservative in fresh feed for marine shrimp maturation. J Pesquisa Agropecuária Brasileira 51:1799–1805
Vine NG, Leukes WD, Kaiser H (2006) Probiotics in marine larviculture. FEMS Microbiol Rev 30:404–427
Wang Z, Chai W, Burwinkel M, Twardziok S, Wrede P, Palissa C, Esch B, Schmidt MF (2013) Inhibitory influence of Enterococcus faecium on the propagation of swine influenza a virus in vitro. PLoS One 8:e53043
Wongsasak U, Chaijamrus S, Kumkhong S, Boonanuntanasarn S (2015) Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp. Aquac. 436:179–187
Zhang H, Sun Z, Liu B, Xuan Y, Jiang M, Pan Y, Zhang Y, Gong Y, Lu X, Yu D, Kumar D, Hu X, Cao G, Xue R, Gong C (2016) Dynamic changes of microbial communities in Litopenaeus vannamei cultures and the effects of environmental factors. Aquac. 455:97–108
Zheng CN, Wang WJAR (2017) Effects of Lactobacillus pentosus on the growth performance, digestive enzyme and disease resistance of white shrimp, Litopenaeus vannamei (Boone, 1931). Aquac Res 48:2767–2777
Zheng X, Duan Y, Dong H, Zhang J (2017) Effects of dietary Lactobacillus plantarum in different treatments on growth performance and immune gene expression of white shrimp Litopenaeus vannamei under normal condition and stress of acute low salinity. Fish Shellfish Immunol 62:195–201
Zubaidah E, Nurcholis M, Wulan SN, Kusuma A (2012) Comparative study on synbiotic effect of fermented rice bran by probiotic lactic acid bacteria Lactobacillus casei and newly isolated Lactobacillus plantarum B2 in wistar rats. APCBEE Procedia 2:170–177
Zuo ZH, Shang BJ, Shao YC, Li WY, Sun JS (2019) Screening of intestinal probiotics and the effects of feeding probiotics on the growth, immune, digestive enzyme activity and intestinal flora of Litopenaeus vannamei. Fish & Shellfish Immunology 86:160–168
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Naiel, M.A.E., Farag, M.R., Gewida, A.G.A. et al. Using lactic acid bacteria as an immunostimulants in cultured shrimp with special reference to Lactobacillus spp.. Aquacult Int 29, 219–231 (2021). https://doi.org/10.1007/s10499-020-00620-2
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DOI: https://doi.org/10.1007/s10499-020-00620-2