Effects of dietary supplementation with a microalga (Schizochytrium sp.) on the hemato-immunological, and intestinal histological parameters and gut microbiota of Nile tilapia in net cages


Autoři: Felipe Pinheiro de Souza aff001;  Ed Christian Suzuki de Lima aff001;  Angela Maria Urrea-Rojas aff001;  Suelen Aparecida Suphoronski aff002;  César Toshio Facimoto aff002;  Jailton da Silva Bezerra Júnior aff003;  Thalita Evani Silva de Oliveira aff002;  Ulisses de Pádua Pereira aff002;  Giovana Wingeter Di Santis aff002;  Carlos Antonio Lopes de Oliveira aff003;  Nelson Mauricio Lopera-Barrero aff001
Působiště autorů: Department of Animal Science, State University of Londrina, Londrina, Parana, Brazil aff001;  Department of Preventive Veterinary Medicine, State University of Londrina, Londrina, Parana, Brazil aff002;  Department of Animal Science, State University of Maringa, Maringa, Parana, Brazil aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226977

Souhrn

Nutritional improvements in intensive aquaculture production systems is necessary for the reduction of stress, maximum utilization of nutritional components, and expression of the genetic potential of fish. The objective of this study was to evaluate the hemato-immunological, and histological parameters and gut microbiota of Nile tilapia fed with the microalga Schizochytrium sp. Males of Nile tilapia were distributed among eight net cages (6 m3), and fed for 105 days with two diets: control (CON), without Schizochytrium sp., and supplemented (SUP), with 1.2% Schizochytrium sp. in the diet. The final weight, mortality, hematocrit, total erythrocyte count (RBC), hemoglobin, hematimetric indices, white blood cell count (WBC), total protein, and serum lysozyme were measured. Alterations in intestinal morphology were evaluated. The gut microbiota was evaluated with next-generation sequencing. No significant differences (p>0.05) were found in the final weight and mortality between diets. Regarding the hematological parameters, a difference (p<0.05) was detected only in RBC, with there being lower values in the SUP, although this group also showed a tendency toward having an increased mean corpuscular hemoglobin level. There were no differences (p>0.05) in total protein and serum lysozyme concentrations or in WBCs between diets, except for lymphocytes, which presented lower values (p<0.05) in the SUP, suggesting immunomodulation by the polyunsaturated fatty acids present in the microalga. There was no difference (p>0.05) in the intestinal morphology between diets. Metagenomic data indicated greater richness (represented by the Chao index) and a higher abundance of the bacterial phylum Firmicutes in the gut microbiota of the tilapia fed with the SUP diet, demonstrating that the digestion and use of the components of the microalga could influence the microbial community. The results indicated that the microalga had modulatory effects on blood cells and the intestinal microbiota, without affecting the structure and integrity of the intestinal villi.

Klíčová slova:

Bacteria – Diet – Gastrointestinal tract – Algae – Gut bacteria – Lysozyme – Serum proteins – Fish physiology


Zdroje

1. FAO. The State of World Fisheries and Aquaculture 2018—Meeting the sustainable development goals [Internet]. Vol. 35. 2018. 176 p. ftp://ftp.fao.org/docrep/fao/011/i0250e/i0250e.pdf

2. IBGE. Pesquisa da Pecuária Municipal—PPM [Internet]. 2017 [cited 2019 May 1]. https://www.ibge.gov.br/estatisticas-novoportal/economicas/agricultura-e-pecuaria/9107-producao-da-pecuaria-municipal.html?=&t=resultados

3. Adamante WB, Nuñer APO, Barcellos LJG, Soso AB, Finco JA. Stress in Salminus brasiliensis fingerlings due to different densities and times of transportation. Arq Bras Med Vet e Zootec Med veterinária e Zootec. 2008;60(3):755–61.

4. Buck EL, Mizubuti IY, Alfieri AA, Otonel RAA, Buck LY, Souza FP, et al. Effect of propolis ethanol extract on myostatin gene expression and muscle morphometry of Nile tilapia in net cages. Genet Mol Res. 2017;16(1):1–13.

5. Levy-Pereira N, Yasui GS, Cardozo MV, Dias J, Neto, Farias THV, et al. Revista Brasileira de Zootecnia Immunostimulation and increase of intestinal lactic acid bacteria with dietary mannan-oligosaccharide in Nile tilapia juveniles. Rev Bras Zootec. 2018;47:e20170006.

6. Kubitza F. Tilápia: tecnologia e planejamento na produção comercial. 2nd ed. Jundiaí: Acqua Supre; 2011. 316 p.

7. Turco PHN, Donadelli A, Scorvo CMDF, JDS, Tarsitano MAA. Análise econômica da produção de Tilápia em tanques-rede de pequeno volume: manejo de ração com diferentes teores de proteína bruta. Informações Econômicas. 2014;44(1):5–11.

8. Quezada-Rodríguez PR, Fajer-Ávila EJ. The dietary effect of ulvan from Ulva clathrata on hematological-immunological parameters and growth of tilapia (Oreochromis niloticus). J Appl Phycol. 2017;(29):423–31.

9. Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, Beard A, et al. Algae in fish feed: Performances and fatty acid metabolism in juvenile Atlantic Salmon. PLoS One. 2015;10(4):1–17.

10. Lewis TE, Nichols PD, McMeekin TA. The biotechnological potential of thraustochytrids. Mar Biotechnol. 1999;1(6):580–7. doi: 10.1007/pl00011813 10612683

11. Sarker PK, Kapuscinski AR, Lanois AJ, Livesey ED, Bernhard KP, Coley ML. Towards sustainable aquafeeds: Complete substitution of fish oil with marine microalga Schizochytrium sp. improves growth and fatty acid deposition in juvenile Nile tilapia (Oreochromis niloticus). PLoS One. 2016;11(6):1–17.

12. Li MH, Robinson EH, Tucker CS, Manning BB, Khoo L. Effects of dried algae Schizochytrium sp., a rich source of docosahexaenoic acid, on growth, fatty acid composition, and sensory quality of channel catfish Ictalurus punctatus. Aquaculture [Internet]. 2009;292(3–4):232–6. Available from: http://dx.doi.org/10.1016/j.aquaculture.2009.04.033

13. Lyons PP, Turnbull JF, Dawson KA, Crumlish M. Effects of low-level dietary microalgae supplementation on the distal intestinal microbiome of farmed rainbow trout Oncorhynchus mykiss (Walbaum). Aquac Res. 2017;48(5):2438–52.

14. dos Santos SKA, Guilherme de Souza Moura MMP, Aline Danielle Souza Prates ALF, Azevedo RC. Microalga Schizochytrium sp. em Rações para Tilápia do Nilo. Cad Ciências Agrárias. 2015;7(1):75–9.

15. Dimitroglou A, Merrifield DL, Moate R, Davies SJ, Spring P, Sweetman J, et al. Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). J Anim Sci. 2009;87(10):3226–34. doi: 10.2527/jas.2008-1428 19617514

16. Eichmiller JJ, Hamilton MJ, Staley C, Sadowsky JM, Sorensen PW. Environment shapes the fecal microbiome of invasive carp species. Microbiome. 2016;44(4):1–13.

17. Tarnecki AM, Burgos FA, Ray CL, Arias CR. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J Appl Microbiol. 2017;123(1):2–17. doi: 10.1111/jam.13415 28176435

18. Garcia F, Schalch SHC, Onaka EM, Fonseca FS, Batista MP. Hematologia de tilápia-do-nilo alimentada com suplemento à base de algas frente a desafios de estresse agudo e crônico. Arq Bras Med Vet e Zootec. 2012;64(1):198–204.

19. Kumala FB, Wahjuningrum D, Setiawati M. Effects of dietary algae, fungi and herb on the growth and innate immunity of Nile tilapia Oreochromis niloticus challenged with Streptococcus agalactiae. AACL Bioflux. 2018;11(4):1368–77.

20. Kim CH. FOXP3 and its role in the immune system. In: Advances in Experimental Medicine and Biology. New York, NY: Springer; 2009. p. 17–29.

21. Chapkin RS, Kim W, Luptona JR., McMurraya DN. Dietary docosahexaenoic and eicosapentaenoic acid: Emerging mediators of inflammation. Prostaglandins Leukot Essent Fat Acids. 2009;81(2–3):187–91.

22. Silva DJ, de Queiroz AC. Analise de Alimentos: Métodos Químicos e Biológicos. 3rd ed. Viçosa: UFV; 2002. 235 p.

23. Blight EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol [Internet]. 1959;37(8):911–7. Available from: http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Canadian+Journal+of+Biochemistry+and+Physiology#0 13671378

24. Joseph JD., Ackman RG. Capillary column gas chromatography method for analysis of encapsulated fish oil and fish oil ethyl esters: collaborative study. J Assoc Off Anal Chem Int. 1992;75:488–506.

25. Visentainer JV. Aspectos analíticos da resposta do detector de ionizaçã o em chama para ésteres de ácidos graxos em biodiesel e alimentos. Quim Nova. 2012;35(2):274–9.

26. De Oliveira SN, Ribeiro RP, de Oliveira CAL, Lopera-Barrero NM, da SO Zardin AM, de Souza FP, et al. Multivariate analysis using morphometric and ultrasound information for selection of tilapia (Oreochromis niloticus) breeders. R Bras Zootec. 2019;48:e20170179.

27. Dawood MAO, Koshio S, El-sabagh M, Billah M, Zaineldin AI, Mamdouh M, et al. Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream, Pagrus major. Aquaculture [Internet]. 2017;470:214–22. Available from: http://dx.doi.org/10.1016/j.aquaculture.2016.12.036

28. Blaxhall PC, Daisley KW. Routine haematological methods for use with fish blood. J Fish Biol. 1973;5(6):771–81.

29. Ranzani-Paiva MJT, de Pádua SB, Tavares-Dias M, Egami MI. Métodos para análise hematológica em peixes. Maringá: Eduem; 2013. 140 p.

30. Ellis AE. Lysozyme Assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, Van Muiswinkel WB, editors. Techniques in Fish Immunology. SOS Publications: SOS Publications; 1990. p. 101–3.

31. Uran PA, Schrama JW, Rombout JHWM, Obach A, Jensen L, Koppe W, et al. Soybean meal-induced enteritis in Atlantic salmon(Salmo salar L.) at different temperatures. Aquac Nutr. 2008;14(4):324–30.

32. R Core Team. R: A language and environment for statistical computing [Internet]. R Foundation for Statistical Computing. 2017 [cited 2018 Nov 11]. https://www.r-project.org/

33. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur : Open-source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol. 2009;75(23):7537–41. doi: 10.1128/AEM.01541-09 19801464

34. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq. Appl Environ Microbiol. 2013;79(17):5112–20. doi: 10.1128/AEM.01043-13 23793624

35. Fan L, Chen J, Meng S, Song C, Qiu L, Hu G. Characterization of microbial communities in intensive GIFT tilapia (Oreochromis niloticus) pond systems during the peak period of breeding. Aquac Res. 2017;2007(48):459–72.

36. Standen BT, Peggs DL, Rawling MD, Foey A, Davies SJ, Santos GA, et al. Dietary administration of a commercial mixed-species probiotic improves growth performance and modulates the intestinal immunity of tilapia, Oreochromis niloticus. Fish Shellfish Immunol. 2016;49:427–35. doi: 10.1016/j.fsi.2015.11.037 26672904

37. Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, et al. Probiotic Pediococcus acidilactici modulates both localised intestinal- and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2013;35:1097–104. doi: 10.1016/j.fsi.2013.07.018 23871840

38. Telli GS, Ranzani-Paiva MJT, Dias D de C, Sussel FR, Ishikawa CM, Tachibana L. Dietary administration of Bacillus subtilis on hematology and non-specific immunity of Nile tilapia Oreochromis niloticus raised at different stocking densities. Fish Shellfish Immunol. 2014;39(2):305–11. doi: 10.1016/j.fsi.2014.05.025 24878743

39. Valladão GMR, Gallani SU, Pala G, Jesus RB, Kotzent S, Costa JC, et al. Practical diets with essential oils of plants activate the complement system and alter the intestinal morphology of Nile tilapia. Aquac Res. 2017;48(11):5640–9.

40. Zahran E, Risha E, AbdelHamid F, Mahgoub HA, Ibrahim T. Effects of dietary Astragalus polysaccharides (APS) on growth performance, immunological parameters, digestive enzymes, and intestinal morphology of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol [Internet]. 2014;38(1):149–57. Available from: http://dx.doi.org/10.1016/j.fsi.2014.03.002 24657260

41. Suphoronski SA, Chideroli RT, Facimoto CT, Mainardi RM, Souza FP, Lopera-Barrero NM, et al. Effects of a phytogenic, alone and associated with potassium diformate, on tilapia growth, immunity, gut microbiome and resistance against francisellosis. Sci Rep. 2019;9(6045):1–14.

42. Araujo DDM, Pezzato AC, Barros MM. Hematology of Nile tilapia fed diets with vegetable oils and stimulated by cold. Pesqui Agropecu Bras. 2011;46(3):294–302.

43. Silva BC, Martins ML, Jatobá A, Buglione CC, Vieira FN, Pereira GV, et al. Hematological and immunological responses of Nile tilapia after polyvalent vaccine administration by different routes. Pesqui Veterinária Bras. 2009;29(11):874–80.

44. Martins ML, Pilarsky F, Onaka EM, Nomura DT, F J Jr, Ribeiro K, et al. Hematologia e resposta inflamatória aguda em Oreochromis niloticus (Osteichthyes: Cichlidae) submetida aos estímulos único e consecutivo de estresse de captura. Bol do Inst Pesca. 30(1):71–80.

45. Tavares-dias BM, Ono EA, Pilarski F, Moraes FR. Can thrombocytes participate in the removal of cellular debris in the blood circulation of teleost fish? A cytochemical study and ultrastructural analysis. J Appl Ichthyol. 2007;23:709–12.

46. Yeganeh S, Adel M. Effects of dietary algae (Sargassum ilicifolium) as immunomodulator and growth promoter of juvenile great sturgeon (Huso huso Linnaeus, 1758). J Appl Phycol. 2018;1–10.

47. Marino F, Di Caro G, Gugliandolo C, Spanò A, Faggio C, Genovese G, et al. Preliminary Study on the In vitro and In vivo Effects of Asparagopsis taxiformis Bioactive Phycoderivates on Teleosts. Front Physiol. 2016;7:1–11.

48. Wan AHL, Soler-vila A, Keeffe DO, Casburn P, Fitzgerald R, Johnson MP. The inclusion of Palmaria palmata macroalgae in Atlantic salmon (Salmo salar) diets: effects on growth, haematology, immunity and liver function. J Appl Phycol [Internet]. 2016;28:3091–100. Available from: http://dx.doi.org/10.1007/s10811-016-0821-8

49. Han SC, Koo DH, Kang NJ, Yoon WJ, Kang GJ, Kang HK, et al. Docosahexaenoic acid alleviates atopic dermatitis by generating tregs and IL-10/TGF-β-modified macrophages via a TGF-β-dependent mechanism. J Invest Dermatol [Internet]. 2015;135(6):1556–64. Available from: http://dx.doi.org/10.1038/jid.2014.488 25405323

50. Kohl KD, Amaya J, Passement CA, Dearing MD, Mccue MD. Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts. Microbiol Ecol. 2014;90:883–94.

51. Zhang M, Sun Y, Liu Y, Qiao F, Chen L, Liu W, et al. Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture [Internet]. 2016;454:72–80. Available from: http://dx.doi.org/10.1016/j.aquaculture.2015.12.014

52. Desai AR, Links MG, Collins SA, Mansfield GS, Drew MD, Van Kessel AG, et al. Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture. 2012;350–353:134–42.

53. Panigrahi A, Kiron V, Kobayashi T, Puangkaew J, Satoh S, Sugita H. Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet Immunol Immunopathol. 2004;102(4):379–88. doi: 10.1016/j.vetimm.2004.08.006 15541791

54. Reveco FE, Øverland M, Romarheim OH, Mydland LT. Intestinal bacterial community structure differs between healthy and inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture [Internet]. 2014;420–421:262–9. Available from: http://dx.doi.org/10.1016/j.aquaculture.2013.11.007

55. Bledsoe JW, Peterson BC, Swanson KS, Small BC. Ontogenetic characterization of the intestinal microbiota of channel catfish through 16S rRNA gene sequencing reveals insights on temporal shifts and the influence of environmental microbes. PLoS One. 2016;11(11):1–22.

56. Finegold SM, Vaisanen ML, Molitoris DR, Tomzynski TJ, Song Y, Liu C, et al. Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. Syst Appl Microbiol. 2003;26(2):177–81. doi: 10.1078/072320203322346010 12866843

57. Tsuchiya C, Sakata T, Sugita H. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol. 2008;46(1):43–8. doi: 10.1111/j.1472-765X.2007.02258.x 17944860

58. Gerritsen J, Hornung B, Renckens B, Van Hijum SAFT, Martins VAP, Rijkers GT, et al. Genomic and functional analysis of Romboutsia ilealis CRIB T reveals adaptation to the small intestine. PeerJ. 2017;5:1–28.

59. Gerritsen J, Fuentes S, Grievink W, van Niftrik L, Tindall BJ, Timmerman HM, et al. Characterization of Romboutsia ilealis gen. nov., sp. nov., isolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinib. Int J Syst Evol Microbiol. 2014;64(PART 5):1600–16.

60. Wang Y, Song J, Zhai Y, Zhang C, Gerritsen J, Wang H, et al. Romboutsia sedimentorum sp. nov., isolated from an alkaline-saline lake sediment and emended description of the genus Romboutsia. Int J Syst Evol Microbiol. 2015;65(2015):1193–8.

61. Chamberlain AHL, Moss ST. The thraustochytrids: a protist group with mixed affinities. BioSystems. 1988;21(3–4):341–9. doi: 10.1016/0303-2647(88)90031-7 3395686

62. Darley WM, Porter D, Fuller MS. Cell wall composition and synthesis via Golgi-directed scale formation in the marine eucaryote, Schizochytrium aggregatum, with a note on Thraustochytrium sp. Arch Mikrobiol. 1973;90(2):89–106. doi: 10.1007/bf00414512 4350550

63. Etyemez M, Balcázar JL. Bacterial community structure in the intestinal ecosystem of rainbow trout (Oncorhynchus mykiss) as revealed by pyrosequencing-based analysis of 16S rRNA genes. Res Vet Sci [Internet]. 2015;100:8–11. Available from: http://dx.doi.org/10.1016/j.rvsc.2015.03.026 25843896

64. Gram L, Melchiorsen J, Spanggaard B, Huber I, Al GET, Icrobiol APPLENM. AH2, a Possible Probiotic Treatment of Fish. Appl Env Microbiol. 1999;65(3):969–73.

65. Baldo L, Riera JL, Tooming-Klunderud A, Albà MM, Salzburger W. Gut Microbiota Dynamics during Dietary Shift in Eastern African Cichlid Fishes. PLoS One. 2015;1–23.

66. Tan CK, Natrah I, Suyub IB, Edward MJ, Kaman N, Samsudin AA. Comparative study of gut microbiota in wild and captive Malaysian Mahseer (Tor tambroides). Microbiologyopen. 2019;8(e734):1–12.

67. Carda‐Diéguez M, Mira A, Fouz B. Pyrosequencing survey of intestinal microbiota diversity in cultured sea bass (Dicentrarchus labrax) fed functional diets. FEMS Microbiol Ecol. 2014;87(2014):451–459.

68. Zheng X, Yang R, Hu J, Lin S, Gu Z, Ma Z. The gut microbiota community and antioxidant enzymes activity of barramundi reared at seawater and freshwater. Fish Shellfish Immunol [Internet]. 2019;89:127–31. Available from: https://doi.org/10.1016/j.fsi.2019.03.054 30930278

69. Bravo-Tello K, Ehrenfeld N, Solı CJ, Hedrera M, Pizarro-guajardo M, Paredes-sabja D. Effect of microalgae on intestinal inflammation triggered by soybean meal and bacterial infection in zebrafish. PLoS One. 2017;12(11):1–13.


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