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© 2007 American Society for Nutrition J. Nutr. 137:2763-2768, December 2007

Nutritional Immunology

Dietary Supplementation of Short-Chain Fructooligosaccharides Influences Gastrointestinal Microbiota Composition and Immunity Characteristics of Pacific White Shrimp, Litopenaeus vannamei, Cultured in a Recirculating System1,2

Peng Li3,7, Gary. S. Burr3,7, Delbert M. Gatlin, III3,*, Michael E. Hume4,5, Susmita Patnaik6, Frank L. Castille6 and Addison L. Lawrence3,6

3 Department of Wildlife and Fisheries Sciences, Texas A&M University System, College Station, TX 77843-2258; 4 USDA, Agricultural Research Service, Food and Feed Safety Unit, College Station, TX, 77845; 5 Department of Poultry Science, Texas A&M University, College Station, TX, 77845; and 6 Texas Agricultural Experimental Station Shrimp Mariculture Project, Texas A&M University System, Port Aransas, TX 78373

* To whom correspondence should be addressed. E-mail: d-gatlin{at}tamu.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Supplementation of prebiotic compounds, including short-chain fructooligosaccharides (scFOS) has been shown to confer benefits on nutrient utilization, growth, and disease resistance of various animal species through improved gastrointestinal (GI) microbiota. However, potential uses of prebiotics for shrimp have not been defined. A 6-wk feeding trial was conducted in a recirculating system to determine the effects of scFOS supplementation on growth performance, immune functions, and GI microbiota composition of Pacific white shrimp (Litopenaeus vannamei). scFOS was supplemented in a nutritionally complete diet (35% crude protein) at 0.025, 0.0500, 0.075, 0.100, 0.200, 0.400, and 0.800% by weight. After 6 wk of feeding, shrimp fed 0, 0.1, and 0.8% scFOS were sampled for assays of immune function and GI microbiota. Dietary supplementation of scFOS did not improve weight gain, feed conversion ratio, or survival of shrimp. Denaturing gradient gel electrophoresis analysis suggested the intestinal tract microbial community from shrimp fed the basal diet was different from that of shrimp fed the scFOS diets [similarity coefficient (SC) = 74.9%)], although the intestinal tract microbial community from shrimp fed the scFOS-supplemented diets was very similar (SC = 92.3%). All the bacterial species contributing to the GI microbial differences were identified, although most of them are uncultured species. Both total hemocyte count and hemocyte respiratory burst increased (P < 0.05) by incremental dietary supplementation of scFOS (0–0.8%). This study is the first to our knowledge to show that dietary scFOS can selectively support growth of certain bacterial species in the GI tract of shrimp and enhance immunity, which may facilitate development of alternative strategies, including novel probiotics and synbiotics, for shrimp growth and health management.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Global farmed shrimp production has grown phenomenally into a prosperous industry producing nearly 1.8 million metric tons/y worth $9.3 billion and it is expected to double in the next 20 y (1). Despite rapid expansion, the industry has been negatively affected by infectious diseases, including viruses, rickettsiae, bacteria, fungi, and parasites causing billions of dollars in losses (2). Traditional uses of antibiotics have been criticized due to the potential development of antibiotic-resistant bacteria, presence of antibiotic residues in seafood, destruction of microbial populations in the aquacultural environment, and suppression of the aquatic animal's immune system. As an alternative strategy to antibiotic use in aquatic disease management, probiotics have recently attracted extensive attention in aquaculture. Many reports have been published regarding successful application of probiotics in the aquatic environment (3–6). Due to cost, potential impact on the environment, regulatory issues, and product safety, large-scale application of probiotics in the water has been limited. Alternatively, it appears more economically efficient to manipulate the gastrointestinal (GI)8 microbiota in aquatic animals by application of dietary prebiotics that alter the conditions of the GI tract to favor certain bacterial species that may enhance growth efficiency and disease resistance of the host organism (5,7). Compared to progress made with fish, research on dietary supplementation of probiotics and prebiotics for shrimp is still in its infancy, although some encouraging reports have shown that supplementation of probiotics such as Bacillus sp. can enhance shrimp growth and resistance to Vibrio harveyi (6,8–10).

Prebiotics have been defined by Gibson and Roberfroid (11) as "a nondigestible food ingredient which beneficially affects the host by selectively stimulating the growth of and/or activating the metabolism of one or a limited number of health-promoting bacteria in the intestinal tract, thus improving the host's intestinal balance." One of the most common prebiotics studied in humans and terrestrial animals is the group of carbohydrates known as fructooligosaccharides (FOS). The general term FOS may include all nondigestible oligosaccharides composed of fructose and glucose units (12). Specifically, FOS refers to short and medium chains of ß-D- fructans in which fructosyl units are bound by ß-(2–1) osidic linkages and attached to a terminal glucose unit. Because of a lack of ß-fructosidases, mammalian digestive systems cannot hydrolyze the ß-(2–1) osidic linkages (13). However, FOS can be fermented by certain bacteria expressing this enzyme, such as lactobacilli and bifidobacterial species (14,15) and, thus, can selectively support the growth and survival of such bacteria in the GI tract of animals. Despite occasional inconsistent results in terrestrial animal species, FOS has been shown to influence protein digestion and intestinal morphology (13,16). These modifications might contribute to improved growth, feed efficiency, and disease resistance. In addition, dietary supplementation of FOS has been shown to enhance growth rate of aquatic animals such as soft-shell turtle (Trionyx sinensis) (17) and turbot larvae (Psetta maxima) (18). Information on potential dietary supplementation of prebiotics such as FOS for shrimp growth and health management is extremely limited at this time (19). This study was designed to determine the potential influences of incremental FOS supplementation on growth performance, feed utilization, intestinal microflora, and immunity of Pacific white shrimp (Litopenaeus vannamei).


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Experimental diets. The diets were based on marine animal protein, soy protein, purified lipid, and wheat starch (Table 1). The basal diet was supplemented with cholesterol, phospholipids, vitamins, and mineral premixes (20) to meet or exceed all known nutritional requirements of penaeid shrimp (21). Growth of L. vannamei fed the basal diet was shown to equal or exceed the growth of L. vannamei fed the nutritionally high-quality commercial diet. The short-chain FOS (scFOS) product (Fortifeed) was obtained from GTC Nutrition and was supplemented in the diet at 0.025, 0.050, 0.075, 0.100, 0.200, 0.400, and 0.800%, respectively. This scFOS product is characterized as having a typical composition of 34% l-kestose, 53% nystose, and 10% lF-ß-fructofranosylnystose. The experimental diets were processed as described previously (22). Briefly, all dry ingredients were mixed thoroughly for at least 40 min. Then, purified lipid was slowly added and mixed for an additional 30 min. Finally, hot water was added to form a dough that was immediately extruded through a 2-mm orifice die using a Hobart A-200 extruder (Hobart). Extruded diets were dried in an oven at 45°C for 12 h, ground to appropriate sizes for juvenile shrimp, and stored at –10°C in sealed plastic bags until used.


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  		TABLE 1 Ingredient and nutrient values of the basal diet (as-fed basis)1

 
    Feeding trial. Specific pathogen-free L. vannamei postlarvae (virus susceptible Kona strain, PL 06–02, SR062), obtained from the Oceanic Institute in Hawaii, were reared at the Texas Agricultural Experiment Station Shrimp Mariculture Project, Texas A&M University System (Port Aransas, TX). Rearing conditions were maintained at 30 ± 2°C, 26–36 parts per thousand salinity, and 5.2 ± 0.2 mg dissolved oxygen (DO)/L. Shrimp were fed a commercial postlarval diet (Rangen) and supplemented with live Artemia nauplii twice daily until the feeding trials began. The growth trial was conducted in 100 30-L rectangular tanks (bottom area 0.1 m2) in a recirculating water system. Seawater was pumped through a sand filter, biological filter, 50-µm cartridge filter, heat exchanger, and UV disinfection unit to achieve a recirculating rate of 0.76 L·min–1·tank–1 (3634% exchange·tank–1·d–1) to ensure an optimum environment. Continuous dim lighting was provided during daytime from windows with a small increase in indirect lighting provided by overhead lighting for 1–2 h daily when filling automatic feeders.

Groups of 10 shrimp of similar size [75.4 ± 0.8 g (SE)] were blotted dry and weighed before being stocked into each tank. Also, all shrimp from each tank were blotted dry and weighed as a group at the end of the feeding trial. There were 10 replicate groups of shrimp for each dietary treatment. Shrimp initial weights (either group weight or mean weight) did not differ in the various dietary treatments. Shrimp were fed the experimental diets 15 times/d using automatic feeders. The feeding rate was maintained at 2.5 g feed·shrimp–1·wk–1 (0.357 g feed·shrimp–1·d–1) so that the juvenile shrimp were fed to slight excess. Uneaten feed, fecal waste, and molted exuviae were not removed to prevent disturbance of the shrimp and resulted in limited organic matter loading. Shrimp were monitored daily for molting activity as well as to assess mortality. Temperature, salinity, and DO were monitored daily using a YSI 85 Meter (YSI). Total ammonia-nitrogen, nitrite nitrogen, nitrate nitrogen, and pH were monitored weekly using methods as previously described (20). The feeding trial was conducted for 6 wk.

    Intestinal tract samples. The intestinal tract immediately posterior to the stomach from 10 shrimp per tank was aseptically removed and pooled to characterize the microbial populations. A total of 7 replicate tanks were sampled for the following treatments: basal (0% scFOS); 0.1%, and 0.8% scFOS. The intestinal tract contents were removed and stored at –20°C until analyzed.

    DNA isolation and PCR. Genomic DNA was isolated from ~0.2 g of dried feces with the Bio-Rad Aqua Pure DNA Isolation kit using the method supplied by the manufacturer with the following modifications: the pellets were suspended in 800 µL of the DNA lysis buffer. Twenty microliters of lysozyme (Sigma Chemical) was added and mixed with a sterile pestle. The solution was incubated at 37°C for 2 h after which it was centrifuged at 20,800 x g; 3 min and the supernatant was removed and placed into a clean 1.5-mL microcentrifuge tube. Then 1.5 µL of the RNAse solution (4 g/L) was added and the mixture was incubated at 37°C for 45 min. Then PCR was conducted using the method of Hume et al. (23). The use of bacteria-specific PCR primers to conserved regions flanking the variable V3 region of 16S rDNA was used.

    Denaturing gradient gel electrophoresis. Denaturing gradient gel electrophoresis (DGGE) was conducted following the method of Hume et al. (23) as modified from Muyzer et al. (24). The fragment analysis pattern relatedness was determined with Molecular Analysis Fingerprinting software (v 1.6; Bio-Rad). This analysis is based on the Dice similarity coefficient (SC) and the unweighted pair group method using arithmetic averages for clustering. Comparisons between sample band patterns are expressed as a percentage SC.

    Sequencing. The 5 most dominant bands in the DGGE gel from the 3 treatments were sequenced. Plugs from these 5 bands were removed using sterile 200-µL pipette tips, incubated in 10 mmol/L Tris, 1 mmol/L EDTA, pH 7.5 buffer, and then amplified using a blunt end polymerase with the same primers as used for DGGE analysis except primer 3 did not have the 40-bp GC clamp. The blunt end products were then used in a Zero Blunt TOPO PCR cloning kit for Sequencing (Invitrogen) according to the methods provided in the kit. Three clones were sequenced and then analyzed using nBLAST at the National Center for Biotechnology Information to identify the genus and/or species.

    Sampling and immune characteristic assays. Shrimp fed 0, 0.1, and 0.8% scFOS were chosen for immune characteristic analyses. At the end of wk 6, 8 shrimp from 8 tanks in each of the 3 treatments were randomly obtained and bled to measure total hemocyte count (THC) and hemocyte respiratory burst. Hemolymph (~200 µL) was withdrawn from the ventral sinus of each shrimp into a 1-mL sterile syringe (25 gauge) containing 0.5 mL of anticoagulant solution (30 mmol/L trisodium citrate, 0.34 mol/L sodium chloride, 10 mmol/L EDTA, pH 7.55, 780 mOsm/kg osmolality) as described by Liu et al. (25). The hemolymph amount was precisely measured by weighing the syringes prior to and after bleeding. Fifty microliters of hemolymph-anticoagulant mixture was mixed with 50 µL of trypan blue and placed in a hemacytometer for counting. Hemocyte respiratory burst was analyzed as described by Liu et al. (25). Briefly, hemolymph from individual shrimp was centrifuged in 0.01% poly-L-lysine-coated microtubes. The hemocytes were incubated with 0.1% zymosan for 30 min and 0.2% nitroblue tetrazolyum for 2 h. Cells were then fixed by methanol, nitroblue tetrazolyum diformazan precipitate was dissolved in 120 µL 2 mol/L KOH and 140µL dimethyl sulfoxide, and transferred to a 96-well plate for absorbance determination at 620 nm. An additional 8 shrimp from each of 8 tanks from the 3 treatments were bled for phenoloxidase determination by following the procedure described by Hernández-López et al. (26).

    Statistical analysis. All the data were subjected to Levene's test of equality of error variances and 1-way ANOVA followed by Student-Newman-Kuels test, using SPSS based on a randomized complete block design. Survival data were arc sin transformed prior to ANOVA because of lack of constant variance. In addition, linear regression analysis was performed using SPSS with all the response characteristics measured to determine whether any performance was responsive to incremental concentrations of scFOS in the diet. Treatment effects were considered significant if P ≤ 0.05. Replicate tanks served as the experimental unit in all analyses. Values in the text are presented as means ± SEM.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Water quality. Water total ammonia nitrogen was 0.22 ± 0.07 mg/L, nitrite nitrogen was 0.20 ± 0.09 mg/L, nitrate nitrogen was 0.28 ± 0.12 mg/L, and pH was 7.94 ± 0.04. Water temperature was 30.3 ± 0.5°C, salinity was 37.8 ± 1.0 parts per thousand, and DO was 5.5 ± 0.1 mg/L. These water quality conditions would suggest the shrimp were maintained under optimal conditions for the duration of the feeding trial.

    Growth performance and feed utilization. Because of the high quality of animals, experimental diets, and environmental conditions, shrimp fed all experimental diets demonstrated a high growth rate (1.54 ± 0.06 g/wk) and survival (93–98%). The shrimp reached ~16.8 g after the 6-wk feeding period from an initial size of 7.5 g. Dietary supplementation of FOS did not affect the weight gain or survival (~96%) of shrimp during the feeding trial. Feed efficiency ranged from 0.56 to 0.64 g gain/g feed, indicating that feed intake and utilization by shrimp in this study were excellent. Adding scFOS to diets did not affect feed efficiency. These data indicate that there were no negative effects of up to 0.8% dietary scFOS on shrimp growth performance.

    Intestinal microbiota analyses. The dendrogram analysis (Fig. 1) showed that the shrimp were clustered into 2 groups. The intestinal tract microbial community from shrimp fed the basal diet was unique compared to that from shrimp fed the scFOS diets (SC = 74.9%). The intestinal tract microbial community from shrimp fed the scFOS diets was very similar (SC = 92.3%), but the communities were not identical (SC < 95%). The DNA sequences obtained from the intestinal tract of shrimp in this study revealed that most of the bacteria were either uncultured or unidentified to the genus and species level (Table 2). Most of the bacteria were related to those associated with marine sediments and biofilms or similar to intestinal microbes found in humans and rats.


Figure 1
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  		FIGURE 1  Dendrogram of the GI tract microbial community of shrimp fed the basal diet (lane 1), the diet containing 0.1% scFOS (lane 2), and the diet containing 0.8% scFOS (lane 3). The community from shrimp fed the basal diet (B1–5) was different from that of shrimp fed the scFOS diets (F1, 3, 4, 6, and 7) (SC = 74.9%). The GI tract microbial community from shrimp fed the scFOS diets was very similar (SC = 92.3%), but the communities were not identical (SC < 95%). Arrows indicate bands that were sequenced and identified in Table 2.

 

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  		TABLE 2 Identified bacterial species from the DNA sequencing

 
    Immune responses. THC, hemocyte phenoloxidase activity, and hemocyte respiratory burst were determined for shrimp fed 0, 0.1, and 0.8% scFOS to evaluate potential influences on immunity. All 3 characteristics showed relatively large variation among individual shrimp. THC was increased by supplementation of incremental concentrations of dietary scFOS (0–0.8%) based on linear regression analysis, although scFOS supplementation accounted for only 16.8% of the variation (adjust R2 = 0.168; P = 0.03) (Fig. 2A). Hemocyte phenoloxidase tended to be greater in shrimp fed both levels of scFOS than in controls (P = 0.1) (Fig. 2B) and dietary scFOS supplementation enhanced (P < 0.05) the hemocyte respiratory burst (Fig. 2C). Supplementation with ScFOS accounted for 22.2% of the variation in hemocyte respiratory burst of individual shrimp in this study (adjusted R2 = 0.222; P = 0.013).


Figure 2
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  		FIGURE 2  THC (A), hemocyte phenoloxidase (B), and hemocyte respiratory burst (C) of shrimp fed 0, 0.1, or 0.8% for 6 wk. Bars are means ± SEM, n = 8. Means without a common letter differ (P < 0.05).

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Prebiotics such as scFOS have been recognized for being involved in digestion, absorption, and metabolism of various nutrients in terrestrial organisms (12,16,27). Dietary supplementation of FOS recently has been shown to enhance growth rate of aquatic animals such as soft-shell turtle (17) and turbot larvae (18). A recent report showed that scFOS supplementation at concentrations from 0.04 to 0.16% of diet improved specific growth rate and the feed conversion ratio of Pacific white shrimp cultured in a recirculating system, although survival was low (42–61%) for all treatments (19). In this study, weight gain and survival were not significantly enhanced by scFOS supplementation. However, because excellent growth and survival were obtained with the shrimp, diets, and culture conditions used in this study, a greater growth rate was probably not possible. Also, because benefits of scFOS supplementation are presumably conferred through intestinal microbial changes and the microbial populations in the culture environment may dramatically impact microbial populations, the effects of scFOS supplementation on growth performance might need re-evaluation under various culture conditions, especially in eutrophic waters. The scFOS-fed shrimp had a distinct intestinal tract microbial population compared to shrimp fed the basal diet. The DGGE profile of shrimp in this study was relatively simple compared to ruminal microbial populations in cows (28) and sheep (29) and to cecal microbial populations in chickens (23,30). The microbial populations from the shrimp GI tract in this study are similar in complexity to the microbial populations of fishes. Romero and Navarrete (31) reported that larval Coho salmon (Onchorhynchus kisutch) had simple DGGE profiles consisting of 4 bands, with Pseudomonas spp. and Aeromonas spp. being the dominant species detected. The uptake of a potential probiotic organism for haddock (Melanogrammus aeglefinus) larva was confirmed using DGGE (32). The DGGE profiles of the haddock larva also were relatively simple with 5 dominant bands present, although all bands were not present at each time point examined (32).

The majority of bacterial sequences isolated from the DGGE bands of shrimp intestinal samples in this study could not be identified to the species level, because they are not in the National Center for Biotechnology Information Blast database. Most were related to marine sediment bacteria, marine biofilm bacteria, or GI bacteria found in mammals. It is not surprising to find sediment bacteria or biofilm bacteria in the intestinal tract of shrimp, because they are bottom feeders and will ingest food along with other benthic particles. These results are similar to those of a previous study with a different marine shrimp in which it was determined to contain marine sediment bacteria, rumen bacteria, and bacteria from squid (33). The presence of bacteria found in marine biofilms indicates these bacteria may be used as a source of nutrients or other biochemicals. Two of the bands intensified by the addition of scFOS were found to be Alkalibacillus spp. and Micrococcus spp. or an unidentified seawater bacterium. Both Alkalibacillus spp. and Micrococcus spp. are gram-positive aerobic microbes that can tolerate saline environments (34,35). The other genus identified was Aquabacterium, which include gram-negative microaerophiles that use oxygen and nitrate as electron acceptors (36) and Roseobacter spp., which are photosynthetic {alpha}-Proteobacteria that inhabit the marine environment (37). Whether any of these genera are beneficial to shrimp is unknown. Recently, Vibrio parahaemolyticus, Aeromonas hydrophila, Lactobacillus sp., and Streptococcus faecalis were isolated from the GI tract of Pacific white shrimp fed graded levels of scFOS using selective agars, but none of the bacterial species responded to increased dietary scFOS in a consistent manner (19).

The changes in the microbial community noted in this study may have benefited the shrimp, possibly by increasing nonspecific immune responses and by increasing the concentrations and/or production of volatile fatty acids in the GI tract. Both of these benefits have been demonstrated in chickens (38) and swine (39). Butyrate has been shown to downregulate the expression of invasion genes in Salmonella sp. (40), indicating a possible mechanism of increased disease resistance, although volatile fatty acid production was not examined in this study.

Several publications have reported that dietary supplementation of probiotics and prebiotics can enhance resistance of animals to infectious diseases (7). Pathogen inhibition is usually considered to be achieved by competition for territory in the GI tract, reduction in pH, and release of natural antibiotics from beneficial microbial populations (15). Enhanced resistance also might be attributable to the beneficial influence of GI microbes on host innate and adaptive immunity (41). For example, Perdigon et al. (42) showed that lactic acid bacteria-containing yogurt could inhibit the growth of intestinal carcinoma through increased activity of Immunoglobulin A, T cells, and macrophages in mice. In recent years, dietary probiotics also were substantiated to enhance the innate (9,43) and adaptive immunity (44) of various aquatic animals. Although the GI tract microbiota of crustaceans such as shrimp and prawns have been studied for over 2 decades (45,46), the interactive influences of the microbial populations and shrimp health as well as potential influences of diets are generally poorly understood. Rengpipat et al. (8–10) demonstrated that dietary supplementation of probiotics such as Bacillus sp. can enhance growth, immunity, and disease resistance of black tiger shrimp (Penaeus monodon). However, potential influences of prebiotics on shrimp immunity have not been investigated.

This study is the first, to our knowledge, to show that prebiotics such as scFOS can alter GI microbial composition as well as enhance THC and hemocyte respiratory burst, 2 major shrimp immunity characteristics (47–49); however, it remains untested as to whether the upregulated immunity can enhance resistance to various pathogens such as Vibrio sp. or White Spot Syndrome Virus that pose severe threats to the global shrimp culture industry (2,48). Additional research is being conducted to establish correlations between identified GI microbial species and upregulated immune responses of shrimp as well as to identify mechanism(s) of immunomodulation by prebiotic substrate-microbe-immune system interactions in shrimp. Such studies hold considerable potential for the development of novel probiotics and synbiotics. Because microbial diversity in various aquacultural environments might impact GI microbiota of shrimp and efficiency of prebiotics and probiotics, further evaluation of the potential use of these supplements for shrimp health and growth management in typical commercial settings is warranted.


   FOOTNOTES
 
1 Supported by the USDA, U.S. Shrimp Farming Program, USDA/CSREES grant no. 2002-38808-01345, Project R-9005, Shrimp Mariculture Research Project, Texas Agricultural Experimental Station, Texas A&M University System, and GTC Nutrition, Golden, CO. Back

2 Author disclosures: P. Li, G. S. Burr, D. M. Gatlin III, M. E. Hume, S. Patnaik, F. L. Castille, and A. L. Lawrence, no conflicts of interest. Back

7 These authors contributed equally to this article. Back

8 Abbreviations used: DGGE, denaturing gradient gel electrophoresis; DO, dissolved oxygen; FOS, fructooligosaccharide; GI, gastrointestinal; scFOS, short-chain fructooligosaccharide; SC, similarity coefficient; THC, total hemocyte count. Back

Manuscript received 14 August 2007. Initial review completed 27 August 2007. Revision accepted 13 September 2007.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

1. Leung PS, Engle C. Shrimp culture: economics, market, and trade. Ames (IA): Blackwell Publishing; 2006.

2. Lightner DV. Biosecurity in shrimp farming: pathogen exclusion through use of SPF stock and routine surveillance. J World Aquacult Soc. 2005;36:229–48.

3. Gatesoupe FJ. The use of probiotics in aquaculture. Aquaculture. 1999;180:147–65.

4. Irianto A, Austin B. Probiotics in aquaculture. J Fish Dis. 2002;25:633–42.

5. Burr GS, Gatlin DM III, Ricke S. Microbial ecology of the gastrointestinal tract and the potential application of probiotics and prebiotics in finfish aquaculture. J World Aquacult Soc. 2005;36:425–36.

6. Farzanfar A. The use of probiotics in shrimp aquaculture. FEMS Immunol Med Microbiol. 2006;48:149–58.[Medline]

7. Gatlin DM III. Nutrition and fish health. In: Halver JE, Hardy RW, editors. Fish nutrition. 3rd ed. San Diego: Academic Press; 2002. p. 671–702.

8. Rengpipat S, Phianphak W, Piyatiratitivorakul S, Menasveta P. Effects of a probiotic bacterium in black tiger shrimp Penaeus monodon survival and growth. Aquaculture. 1998;167:301–13.

9. Rengpipat S, Rukpratanporn S, Piyatiratitivorakul S, Menasveta P. Immunity enhancement in black tiger shrimp (Penaeus monodon) by a probiont bacterium (Bacillus S11). Aquaculture. 2000;191:271–88.

10. Rengpipat S, Tunyamum A, Fast AW, Piyatiratitivorakul S, Menasveta P. Enhanced growth and resistance to vibrio challenge in pond-reared black tiger shrimp Penaeus monodon by a Bacillus probiotic. Dis Aquat Organ. 2003;55:169–73.[Medline]

11. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401–12.[Abstract/Free Full Text]

12. Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Wolf BW, Chow J, Garleb KA, Williams JA, Fahey JC. Fructooligosaccharide and Lactobacillus acidophilus modify bowel function and protein catabolites excreted by healthy humans. J Nutr. 2002;132:3042–50.[Abstract/Free Full Text]

13. Teitelbaum JE, Walker WA. Nutritional impact of pre-and probiotics as protective gastrointestinal organisms. Annu Rev Nutr. 2002;22:107–38.[Medline]

14. Sghir A, Chow JM, Mackie RI. Continuous culture selection of bifidobacteria and lactobacilli from human fecal samples using fructooligosaccharide as selective substrate. J Appl Microbiol. 1998;85:769–77.[Medline]

15. Manning TS, Gibson GR. Prebiotics. Best Pract Res Clin Gastroenterol. 2004;18:287–98.[Medline]

16. Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Healy H, Dawson KA, Merchen NR, Fahey JC. Supplemental fructooligosaccharides and mannonoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. J Nutr. 2002;132:980–9.[Abstract/Free Full Text]

17. Ji G, Liu Z, Leng X. Effects of dietary beta-glucan and fructooligosaccharides on the growth and activities of superoxide dismutase and lysozyme of Trionyx sinensis. J Shanghai Fish Univ. 2004;13:36–40.

18. Mahious AS, Gatesoupe FJ, Hervi M, Metailler R, Ollevier F. Effects of dietary inulin and oligosaccharides as prebiotics for weaning turbot Psetta maxima (Linneuas, C. 1758). Aquac Int. 2006;14:219–29.

19. Zhou Z, Ding Z, Huiyuan LV. Effects of dietary short-chain fructooligosaccharides on intestinal microflora, survival and growth performance of juvenile white shrimp Litopenaeus vannamei. J World Aquacult Soc. 2007;38:296–301.

20. Davis DA, Lawrence AL, Gatlin DM III. Response of Penaeus vannamei to dietary calcium, phosphorus and calcium:phosphorus ratio. J World Aquacult Soc. 1993;24:504–15.

21. D' Abramo LRD, Conklin DE, Akiyama DM. Crustacean nutrition. Baton Rouge (LA): World Aquaculture Society; 1997.

22. Gong H, Lawrence AL, Jiang D, Castille FL, Gatlin DM III. Lipid nutrition of juvenile Litopenaeus vannamei: I. Dietary cholesterol and de-oiled soy lecithin requirements and their interaction. Aquaculture. 2000;190:305–24.

23. Hume ME, Kubena LF, Edrington TS, Donskey CJ, Moore RW, Ricke SC, Nisbet DJ. Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. Poult Sci. 2003;82:1100–7.[Abstract/Free Full Text]

24. Muyzer G, De Waal EC, Litterlinden AG. Profiling of complex microbial population by denature gradient gel electrophoresis analysis of polymerase-chain reaction amplified genes coding for 16S RNA. Appl Environ Microbiol. 1993;59:695–700.[Abstract/Free Full Text]

25. Liu CH, Yeh ST, Cheng SY, Chen JC. The immune response of the white shrimp Litopenaeus vannamei and its susceptibility to Vibrio infection in relation with the molt cycle. Fish Shellfish Immunol. 2004;16:151–61.[Medline]

26. Hernández-López J, Gollas-Galván T, Vargas-Albores F. Activation of the prophenoloxidase system of the brown shrimp (Penaeus californiensis Holmes). Comp Biochem Physiol. 1996;113C:61–6.

27. Steer TE, Johnson IT, Gee JM, Gibson GR. Metabolism of the soyabean isoflavone glycoside genistin in vitro by the human gut bacteria and the effect of prebiotics. Br J Nutr. 2003;90:635–42.[Medline]

28. Karnati SK, Sylvester JT, Noftsger SM, Yu Z, St-Pierre NR, Firkins JL. Assessment of ruminal bacterial populations and protozoal generation time in cows fed different methionine sources. J Dairy Sci. 2007;90:798–809.[Abstract/Free Full Text]

29. Edwards JE, McEwan NR, McKain N, Walker N, Wallace RJ. Influence of flavomycin on ruminal fermentation and microbial populations in sheep. Microbiology. 2005;151:717–25.[Abstract/Free Full Text]

30. Johansen CH, Bjerrum L, Finster K, Pedersen K. Effects of Campylobacter jejuni infection on the development of the intestinal microflora of broiler chickens. Poult Sci. 2006;85:579–87.[Abstract/Free Full Text]

31. Romero J, Navarrete P. 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of Coho salmon (Onchorynchus kisutch). Microb Ecol. 2006;51:422–30.[Medline]

32. Plante S, Pernet F, Haché R, Ritchie R, Ji B, McIntosh D. Ontogenetic variations in lipid class and fatty acid composition of haddock larvae Melanogrammus aeglefinus in relation to changes in diet and microbial environment. Aquaculture. 2007;263:107–21.

33. Lau WWY, Jumars PA, Armburst EV. Genetic diversity of attached bacteria in the hindgut of the deposit-feeding shrimp Neotrypaea (formerly Callianassa) californiensis (Decapoda: Thalassinidae). Microb Ecol. 2002;43:455–66.[Medline]

34. Jeon CO, Lim JM, Lee JM, Xu LH, Jiang CL, Kim CJ. Reclassification of Bacillus haloalkaliphilus Pritzw 1996 as Alkalibacillus haloalkalipilus gen. nov., comb. Nov. and the description of Alkalibacillus salilacus sp. nov, a novel halophilic bacterium isolated from a salt lake in China. Int J Syst Evol Microbiol. 2005;55:1891–6.[Abstract/Free Full Text]

35. Joshi AA, Kanekar PP, Kelkar AS, Shouche YS, Vani AA, Borgave SB, Sarnaik SS. Cultivable bacterial diversity of alkaline Lonar Lake, India. Microb Ecol. 2007;10.1007/s00248–007–9264–8.

36. Kalmbach S, Manz W, Wecke J, Szewzyk U. Aquabacterium gen. nov.,with description of Aquabacterium citratiphilum sp. nov., Aquabacterium parvum sp. nov. and Aquabacterium commune sp. nov., three in situ dominant bacterial species from the Berlin drinking water system. Int J Syst Bacteriol. 1999;49:769–77.[Abstract/Free Full Text]

37. Wagner-Döbler I, Biebl H. Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol. 2006;60:255–80.[Medline]

38. Bailey J, Blankenship L, Cox N. Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poult Sci. 1991;70:2433–8.[Medline]

39. Smiricky-Tjardes M, Grieshop C, Flickinger E, Bauer L, Fahey G. Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility, ileal and fecal bacterial concentrations, and ileal fermentative characteristics of growing pigs. J Anim Sci. 2003;81:2535–45.[Abstract/Free Full Text]

40. Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L, Pasmans F, Haesebrouck F, Ducatelle R. The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathol. 2006;35:182–8.[Medline]

41. Erickson KL, Hubbard NE. Probiotic immunomodulation in health and diseases. J Nutr. 2000;130:S403–9.

42. Perdigon G, Alvarez S, Rachid M, Agüero G, Gobbato N. Immune system stimulation by probiotics. J Dairy Sci. 1995;78:1597–606.[Abstract]

43. Kim D, Austin B. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol. 2006;21:513–24.[Medline]

44. Picchietti S, Mazzini M, Taddei AR, Renna R, Fausto AM, Mulero V, Carnevali O, Cresci A, Abelli L. Effects of administration of probiotic strains on GALT of larval gilthead seabream: immunohistochemical and ultrastructural studies. Fish Shellfish Immunol. 2006;22:57–67.[Medline]

45. Dempsey AC, Kitting CL. Characteristic of bacteria isolated from penaeid shrimp. Crustaceana (Leiden). 1987;52:90–3.

46. Harris JM. The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol. 1993;25:195–231.

47. Chen G, Huang J, Song X. General situation of the immunological capacity of shrimp. J Fisheries China. 2004;28:209–15.

48. Söderhäil K, Cerenius L. Crustacean immunity. Annu Rev Fish Dis. 1992;1:3–23.

49. Smith VJ, Brown JH, Hauton C. Immunostimulation in crustaceans: does it really protect against infection. Fish Shellfish Immunol. 2003;15:71–90.[Medline]




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