Skip to main content

Advertisement

Log in

Changes on the intestinal bacterial community of white shrimp Penaeus vannamei fed with green seaweeds

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

In recent years, development of sustainable and ecological food production has gained worldwide interest. It seems clear that this phenomenon is causing changes in aquaculture-focused research, with the development of new integration systems. However, it is still necessary to understand different aspects involved in integrated systems, including co-culture systems such as shrimp and seaweed. This study evaluated the effect of green seaweeds as food source on white shrimp Penaeus vannamei intestinal bacterial communities. Shrimp were evaluated after a 4-week experimental trial under different diet treatments: fed with only pellet (P), only Ulva clathrata (UC), U. clathrata + pellet (UCP), only Ulva lactuca (UL), and U. lactuca + pellet (ULP). In terms of growth and survival, no significant differences (P > 0.05) were found between ULP and UCP treatments compared with the control (P). Analysis of the bacterial biota of shrimp intestine revealed significant differences on community composition in ULP, UL, and UC compared with the control (P) (P < 0.05). We found that Proteobacteria is the most abundant phylum in all treatments, followed by Bacteroidetes for UC, UCP, and UL and Actinobacteria for P and ULP treatments. Shrimp fed only with seaweed U. lactuca (UL, ULP) had a significantly higher abundance of Rubritalea, Lysinibacillus, Acinetobacter, and Blastopirellula, and for U. clathrata treatments (UC, UCP), it was Litoreibacter. Relative abundance of Vibrio was higher in the control (P), showing a decrease in UC and UL treatments. Our findings provide a better understanding of integrated aquaculture systems, specifically those utilizing seaweed as natural feed source.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci 101:15718–15723

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bonder MJ, Abeln S, Zaura E, Brandt BW (2012) Comparing clustering and pre-processing in taxonomy analysis. Bioinformatics 28:2891–2897

    Article  CAS  PubMed  Google Scholar 

  • Brito LO, Arantes R, Magnotti C, Derner R, Pchara F, Olivera A, Vinatea L (2014) Water quality and growth of Pacific white shrimp Litopenaeus vannamei (Boone) in co-culture with green seaweed Ulva lactuca (Linnaeus) in intensive system. Aquac Int 22:497–508

    Article  CAS  Google Scholar 

  • Cardona C, Weisenhorn P, Henry C, Gilbert JA (2016) Network-based metabolic analysis and microbial community modeling. Curr Opin Microbiol 31:124–131

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhang CK, Cheng Y, Zhang S, Zhao H (2013) A comparison of methods for clustering 16S rRNA sequences into OTUs. PLoS One 8:e70837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole JR, Wang Q, Fish J, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642

    Article  CAS  PubMed  Google Scholar 

  • Cornejo-Granados F, Lopez-Zavala AA, Gallardo-Becerra L, Mendoza-Vargas A, Sánchez F, Vichido R, Brieba LG, Viana MT, Sotelo-Mundo R, Ochoa-Leyva A (2017) Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Sci Rep 7:11783

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Couteau C, Coiffard L (2016) Seaweed application in cosmetics. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Elsevier, Amsterdam, pp 423–441.

  • Cruz-Suárez LE, León A, Peña-Rodríguez A, Rodríguez-Peña G, Moll B, Ricque-Marie D (2010) Shrimp/Ulva co-culture: a sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 301:64–68

    Article  Google Scholar 

  • Daniel H, Gholami AM, Berry D, Desmarchelier C, Hahne H, Loh G, Mondot S, Lepage P, Rothballer M, Walker A, Böhm C, Wenning M, Wagner M, Blaut M, Schmitt-Kopplin P, Kuster B, Haller D, Clavel T (2014) High-fat diet alters gut microbiota physiology in mice. ISME J 8:295–308

    Article  CAS  PubMed  Google Scholar 

  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin S, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563

    Article  CAS  PubMed  Google Scholar 

  • Ebeling ME (1968) The dumas method for nitrogen in feeds. JAOC 51:766–770

  • Elizondo-González R, Quiroz-Guzmán E, Escobedo-Fregoso C, Magallón-Servín P, Peña-Rodríguez A (2018) Use of seaweed Ulva lactuca for water bioremediation and as feed additive for white shrimp Litopenaeus vannamei. PeerJ 6:e4459

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations) (2017) Fishery and aquaculture statistics. Global Aquaculture Production 1950–2015 (FishStatJ). Updated 2017. FAO Fisheries and Aquaculture Department. FAO, Rome. Accessed Apr 18, 2017 at http://www.fao.org/fishery/statistics/global-aquaculture-production/query/es

  • FAO (2018) The global status of seaweed production, trade and utilization. Food and Agriculture Organization of the United Nations, Rome

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152

  • Gamboa-Delgado J, Peña-Rodríguez A, Ricque-Marie D, Cruz-Suárez LE (2011) Assessment of nutrient allocation and metabolic turnover rate in Pacific white shrimp Litopenaeus vannamei co-fed live macroalgae Ulva clathrata and inert feed: dual stable isotope analysis. J Shellfish Res 30:969–979

    Article  Google Scholar 

  • Ge H, Ni Q, Li J, Chen Z, Zhao F (2019) Integration of white shrimp (Litopenaeus vannamei) and green seaweed (Ulva prolifera) in minimum-water exchange aquaculture system. J Appl Phycol 31:1425–1432

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

    Article  CAS  PubMed  Google Scholar 

  • Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Li X, Wang L, Shao Z (2016) Changes in the intestinal bacterial community during the growth of white shrimp, Litopenaeus vannamei. Aquac Res 47:1737–1746

    Article  Google Scholar 

  • Kandhasamy M, Arunachalam KD (2008) Evaluation of in vitro antibacterial property of seaweeds of southeast coast of India. Afr J Biotechnol 7:1958–1961

    Article  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the Proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: volume 5: Proteobacteria: Alpha and Beta subclasses. Springer, New York, pp 3–37

  • Khoi LV, Fotedar R (2011) Integration of western king prawn (Penaeus latisulcatus Kishinouye, 1896) and green seaweed (Ulva lactuca Linnaeus, 1753) in a closed recirculating aquaculture system. Aquaculture 322:201–209

    Article  Google Scholar 

  • Kim JM, Choi MY, Kim JW, Lee SA, Ahn JH, Song J, Kim SH, Weon HY (2017) Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera). J Microbiol 55:21–30

    Article  CAS  PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar M, Gupta V, Kumari P, Reddy CRK, Jha B (2011) Assessment of nutrient composition and antioxidant potential of Caulerpaceae seaweeds. J Food Compos Anal 24:270–278

    Article  CAS  Google Scholar 

  • Lahaye M, Gómez-Pinchetti JL, Jimenez del Rio M, Garcia-Reina G (1995) Natural decoloration, composition and increase in dietary fibre content of an edible marine algae, Ulva rigida (Chlorophyta), grown under different nitrogen conditions. J Sci Food Agric 68:99–104

    Article  CAS  Google Scholar 

  • Laramore S, Baptiste R, Wills PS, Hanisak MD (2018) Utilization of IMTA-produced Ulva lactuca to supplement or partially replace pelleted diets in shrimp (Litopenaeus vannamei) reared in a clear water production system. J Appl Phycol 30:3603–3610

    Article  CAS  Google Scholar 

  • Li P, Burr GS, Gatlin DM, Hume ME, Patnaik S, Castille FL, Lawrence AL (2007) Dietary supplementation of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of Pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. J Nutr 137:2763–2768

    Article  CAS  PubMed  Google Scholar 

  • Liu CH, Cheng W, Hsu JP, Chen JC (2004) Vibrio alginolyticus infection in the white shrimp Litopenaeus vannamei confirmed by polymerase chain reaction and 16S rDNA sequencing. Dis Aquat Org 61:169–174

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Fonseca PC, Carneiro MA, Moreira WS (2006) Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour Technol 18:2402–2406

    Article  CAS  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391

    Article  Google Scholar 

  • Niu J, Xie SW, Fang HH, Xie JJ, Guo TY, Zhang YM, Liu ZL, Liao SY, He JY, Tian LX, Liu YJ (2018) Dietary values of macroalgae Porphyra haitanensis in Litopenaeus vannamei under normal rearing and WSSV challenge conditions: effect on growth, immune response and intestinal microbiota. Fish Shellfish Immunol 81:135–149

    Article  CAS  PubMed  Google Scholar 

  • Omont A, Quiroz-Guzman E, Tovar-Ramirez D, Peña-Rodríguez A (2019) Effect of diets supplemented with different seaweed extracts on growth performance and digestive enzyme activities of juvenile white shrimp Litopenaeus vannamei. J Appl Phycol 31:1433–1442

    Article  CAS  Google Scholar 

  • Pallaoro MF, Vieira N, Hayashi L (2016) Ulva lactuca (Chlorophyta Ulvales) as co-feed for Pacific white shrimp. J Appl Phycol 503:3659–3665

    Article  CAS  Google Scholar 

  • Peña-Rodríguez A, Mawhinney TP, Ricque-Marie D, Cruz-Suárez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata (Roth) C. Agardh. Food Chem 129:491–498

    Article  PubMed  CAS  Google Scholar 

  • Peña-Rodríguez A, Elizondo-Gonzalez R, Nieto-Lopez MG, Ricque-Marie D, Cruz-Suarez LE (2017a) Practical diets for the sustainable production of brown shrimp, Farfantepenaeus californiensis, juveniles in presence of the green macroalga Ulva clathrata as natural food. J Appl Phycol 29:413–421

    Article  CAS  Google Scholar 

  • Peña-Rodríguez A, Magallon-Barajas FJ, Cruz-Suárez LE, Elizondo-González R, Moll B (2017b) Effects of stocking density on the performance of brown shrimp Farfantepenaeus californiensis co-cultured with the green seaweed Ulva clathrata. Aquac Res 48:2803–2811

    Article  CAS  Google Scholar 

  • Qiao F, Liu YK, Sun YH, Wang XD, Chen K, Li TY, Li EC, Zhang ML (2017) Influence of different dietary carbohydrate sources on the growth and intestinal microbiota of Litopenaeus vannamei at low salinity. Aquac Nutr 23:444–452

    Article  CAS  Google Scholar 

  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH : a versatile open source tool for metagenomics. PeerJ 4:e2584

    Article  PubMed  PubMed Central  Google Scholar 

  • Santizo RB, Serrano AE Jr, Corre VL (2014) Proximate composition and dry matter digestibility of Ulva lactuca in the black tiger shrimp Penaeus monodon. Anim Biol Anim Husb 6:75–83

    Google Scholar 

  • Selvin J, Manilal A, Sujith S, Seghal Kiran G, Premnath Lipton A (2011) Efficacy of marine green alga Ulva fasciata extract on the management of shrimp bacterial diseases. Lat Am J Aquat Res 39:197–204

    Article  Google Scholar 

  • Sivakumar K, Kannappan S, Dineshkumar M, Patil PK (2014) Evaluation of marine macro alga, Ulva fasciata against bio-luminescent causing Vibrio harveyi during Penaeus monodon larviculture. Afr J Microbiol Res 8:803–813

    Article  CAS  Google Scholar 

  • Sung HH, Li HC, Tsai FM, Ting YY, Chao WL (1999) Changes in the composition of Vibrio communities in pond water during tiger shrimp (Penaeus monodon) cultivation and in the hepatopancreas of healthy and diseased shrimp. J Exp Mar Biol Ecol 236:261–271

    Article  Google Scholar 

  • Sung HH, Hsu SF, Chen CK, Ting YY, Chao WL (2001) Relationships between disease outbreak in cultured tiger shrimp (Penaeus monodon) and the composition of Vibrio communities in pond water and shrimp hepatopancreas during cultivation. Aquaculture 192:101–110

    Article  Google Scholar 

  • Swapna B, Venkatrayulu C, Swathi AV (2015) Effect of probiotic bacteria Bacillus licheniformis and Lactobacillus rhamnosus on growth of the Pacific white shrimp Litopenaeus vannamei (Boone, 1931). Eur J Exp Biol 5:31–36

    CAS  Google Scholar 

  • Syad AN, Shunmugiah KP, Kasi PD (2013) Seaweeds as nutritional supplements: analysis of nutritional profile, physicochemical properties and proximate composition of G. acerosa and S. wightii. Biomed Prev Nutr 3:139–144

    Article  Google Scholar 

  • Thuy TTT, Ly BM, Van TTT, Quang NV, Tu HC, Zheng Y, Seguin-Devaux C, Mi B, Ai U (2015) Anti-HIV activity of fucoidans from three brown seaweed species. Carbohydr Polym 115:122–128

    Article  CAS  PubMed  Google Scholar 

  • Troell M, Joyce A, Chopin T, Neori A, Buschmann AH, Fang JG (2009) Ecological engineering in aquaculture—potential for integrated multi-trophic aquaculture (IMTA) in marine offshore systems. Aquaculture 297:1–9

    Article  Google Scholar 

  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    Article  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Sun Y, Chen K, Yu N, Zhou Z, Chen L, Du Z, Li E (2014) Characterization of the intestinal microbiota in Pacific white shrimp, Litopenaeus vannamei, fed diets with different lipid sources. Aquaculture 434:449–455

    Article  CAS  Google Scholar 

  • Zokaeifar H, Balcázar JL, Saad CR, Kamarudin MS, Sijam K, Arshad A, Nejat N (2012) Effects of Bacillus subtilis on the growth performance, digestive enzymes, immune gene expression and disease resistance of white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 33:683–689

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to Gran Mahr laboratory, especially Samuel Echeverria and Omar Camorlinga for kindly donating the shrimp juveniles; Armando León from Algal Tech SAPI de CV for providing U. clathrata seaweed; Sandra de la Paz-Reyes from Laboratory of Aquaculture Nutrition, Pablo Monsalvo-Spencer, and Gabriel Robles Villegas from the laboratory for acclimatization and maintenance of aquatic organisms; and Gabriela Mendoza-Carrión from Genomics and Bioinformatics Laboratory at CIBNOR for all the facilities and technical support during the experiment development. This work was performed within the framework of a UBO/CIBNOR agreement to receive Master’s degree candidates from UBO to complete their MS thesis project.

Data availability statement

Data available from corresponding author on request.

Funding

This work was supported by a grant to Maxence Gemin by the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19) and co-funded by a grant from the French government under the program “Investissements d’Avenir”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alberto Peña-Rodríguez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Online Resources 1

Box plot of richness and bacterial diversity by individual replicates. Observed OTUs, Chao1, Shannon and InvSimpson indices were estimated for treatments with only pellet (P), only U. clathrata (UC), U. clathrata + pellet (UCP), only U. lactuca (UL) and U. lactuca + pellet (ULP) (PNG 70 kb)

Online Resources 2

Relative read abundance of different bacterial phyla by individual replicate for each treatment (only pellet (P), only U. clathrata (UC), U. clathrata + pellet (UCP), only U. lactuca (UL) and U. lactuca + pellet (ULP) (PNG 81 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elizondo-González, R., Quiroz-Guzmán, E., Howe, A. et al. Changes on the intestinal bacterial community of white shrimp Penaeus vannamei fed with green seaweeds. J Appl Phycol 32, 2061–2070 (2020). https://doi.org/10.1007/s10811-020-02072-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02072-w

Keywords

Navigation