|
|
Cite this paper: |
|
|
Liying SUI, Xiaocui LIU, Namin PAN, Xue LIU, Meirong GAO. Halomonas-PHB protects gnotobiotic Artemia against Vibrio and modifies Artemia gut microbiota in xenic culture conditions[J]. Journal of Oceanology and Limnology, 2023, 41(4): 1292-1299 |
|
|
|
|
|
|
|
Halomonas-PHB protects gnotobiotic Artemia against Vibrio and modifies Artemia gut microbiota in xenic culture conditions |
|
Liying SUI1,2, Xiaocui LIU1,2, Namin PAN1,2, Xue LIU1,2, Meirong GAO1,2 |
|
1 Key Laboratory of Marine Resource Chemistry and Food Technology(TUST), Ministry of Education, Tianjin University of Science and Technology, Tianjin 300457, China; 2 Asian Regional Artemia Reference Center, College of Marine and Environmental Sciences, Tianjin University of Science and Technology, Tianjin 300457, China |
|
Abstract: |
The prokaryotic cell storage compound ploy-β-hydroxybutyrate (PHB) has been considered as prebiotics that can be applied in aquaculture. In this paper, the dietary effect of a PHB-accumulating Halomonas strain (HM·PHB) identified from our previous work were studied in Artemia under gnotobiotic and xenic culture conditions, in comparison of Halomonas without PHB accumulation (HM) and microalgae Isochrysis (ISO) feeding. Under gnotobiotic condition, both HM·PHB and HM served as sole food supporting Artemia survival. Although both HM·PHB and HM feeding had no significant difference on Artemia survival percentage (P>0.05), HM·PHB significantly improved their resistance against Vibrio anguillarum challenge (P<0.05). Mass Artemia culture were further performed in xenic condition. Compared to ISO, HM·PHB feeding protected Artemia against V. anguillarum challenge (P<0.05), and HM·PHB and HM feeding resulted in increased T-AOC, pepsin, T-SOD and CAT activities (P<0.05). High throughput sequencing analysis showed that HM·PHB and HM feeding resulted in a lower Artemia gut microbial diversity (P<0.05), and modified the gut microbial community by remarkably reducing the Vibrio proportion. The outcome of the paper confirmed the beneficial effect of Halomonas-PHB in Artemia culture, which supports the use of Halomonas-PHB in the production of bio-secured live feed Artemia. |
|
Key words:
Halomonas-ploy-β-hydroxybutyrate (Halomonas-PHB)|Artemia|survival|pathogen resistance|gut microbiota
|
|
Received: 2022-04-07 Revised: |
|
|
|
|
References:
Bellisario B, Carere C, Cerfolli F et al. 2013. Infaunal macrobenthic community dynamics in a manipulated hyperhaline ecosystem: a long-term study. Aquatic Biosystems, 9(1): 20, https://doi.org/10.1186/2046-9063-9-20. Cherrington C A, Hinton M, Pearson G R et al. 1991. Shortchain organic acids at pH 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation.Journal of Applied Bacteriology, 70(2): 161-165, https://doi.org/10.1111/j.1365-2672.1991.tb04442.x. De Schryver P, Dierckens K, Thi Q Q B et al. 2011.Convergent dynamics of the juvenile European sea bass gut microbiota induced by poly-β-hydroxybutyrate.Environmental Microbiology, 13(4): 1042-1051, https://doi.org/10.1111/j.1462-2920.2010.02410.x. De Schryver P, Sinha A K, Kunwar P S et al. 2010.Poly-β-hydroxybutyrate (PHB) increases growth performance and intestinal bacterial range-weighted richness in juvenile European sea bass, Dicentrarchus labrax. Applied Microbiology and Biotechnology, 86(5): 1535-1541, https://doi.org/10.1007/s00253-009-2414-9. Defoirdt T, Sorgeloos P, Bossier P. 2011. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Current Opinion in Microbiology, 14(3):251-258, https://doi.org/10.1016/j.mib.2011.03.004. Duan Y F, Zhang J S, Dong H B et al. 2015. Oxidative stress response of the black tiger shrimp Penaeus monodon to Vibrio parahaemolyticus challenge. Fish & Shellfish Immunology, 46(2): 354-365, https://doi.org/10.1016/j.fsi.2015.06.032. Duan Y F, Zhang Y, Dong H B et al. 2017. Effect of dietary poly-β-hydroxybutyrate (PHB) on growth performance, intestinal health status and body composition of Pacific white shrimp Litopenaeus vannamei (Boone, 1931).Fish & Shellfish Immunology, 60: 520-528, https://doi.org/10.1016/j.fsi.2016.11.020. Franke A, Clemmesen C, De Schryver P et al. 2017a.Immunostimulatory effects of dietary poly-β-hydroxybutyrate in European sea bass postlarvae. Aquaculture Research, 48(12): 5707-5717, https://doi.org/10.1111/are.13393. Franke A, Roth O, De Schryver P et al. 2017b. Poly-β-hydroxybutyrate administration during early life: effects on performance, immunity and microbial community of European sea bass yolk-sac larvae. Scientific Reports, 7(1): 15022, https://doi.org/10.1038/s41598-017-14785-z. Gao M R, Du D D, Bo Z X et al. 2019. Poly-β-hydroxybutyrate (PHB)-accumulating Halomonas improves the survival, growth, robustness and modifies the gut microbial composition of Litopenaeus vannamei postlarvae.Aquaculture, 500: 607-612, https://doi.org/10.1016/j.aquaculture.2018.10.032. Gao M R, Li Y, Xie W et al. 2020. Effect of Halomonas storage poly-β-hydroxybutyrates on survival, growth and vibriosis resistance of half-smooth tongue sole Cynoglossus semilaevis juveniles. Aquaculture Research, 51(11): 4631-4637, https://doi.org/10.1111/are.14810. Giarma E, Amanetidou E, Toufexi A et al. 2017. Defense systems in developing Artemia franciscana nauplii and their modulation by probiotic bacteria offer protection against a Vibrio anguillarum challenge. Fish & Shellfish Immunology, 66: 163-172, https://doi.org/10.1016/j.fsi.2017. 05.008. Gorospe J, Nakamura K. 1996. Associated bacterial microflora in Artemia-rice bran culture. The Israeli Journal of Aquaculture, 48(2): 99-107. Gunasekara R A Y S A, Rekecki A, Cornillie P et al. 2011.Morphological characteristics of the digestive tract of gnotobiotic Artemia franciscana nauplii. Aquaculture, 321(1-2): 1-7, https://doi.org/10.1016/j.aquaculture.2011. 07.037. Halet D, Defoirdt T, van Damme P et al. 2007. Poly-β-hydroxybutyrate-accumulating bacteria protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii.FEMS Microbiology Ecology, 60(3): 363-369, https://doi.org/10.1111/j.1574-6941.2007.00305.x. Intriago P, Jones D A. 1993. Bacteria as food for Artemia.Aquaculture, 113(1-2): 115-127, https://doi.org/10.1016/0044-8486(93)90345-Y. Laranja J L Q, De Schryver P, Ludevese-Pascual G L et al. 2018. High amorphous poly-beta-hydroxybutyrate (PHB) content in a probiotic Bacillus strain displays better protective effects in Vibrio-challenged gnotobiotic Artemia. Aquaculture, 487: 15-21, https://doi.org/10.1016/j.aquaculture.2018.01.005. Lavens P, Sorgeloos P. 1996. Manual on the Production and Use of Live Food for Aquaculture. Food and Agriculture Organization of the United Nations, Rome. 295p. Makridis P, Vadstein O. 1999. Food size selectivity of Artemia franciscana at three developmental stages. Journal of Plankton Research, 21(11): 2191-2201, https://doi.org/10.1093/plankt/21.11.2191. Marques A, Thanh T H, Sorgeloos P et al. 2006a. Use of microalgae and bacteria to enhance protection of gnotobiotic Artemia against different pathogens. Aquaculture, 258(1-4): 116-126, https://doi.org/10.1016/j.aquaculture.2006.04.021. Marques A, Ollevier F, Verstraete W et al. 2006b. Gnotobiotically grown aquatic animals: opportunities to investigate host-microbe interactions. Journal of Applied Microbiology, 100(5): 903-918, https://doi.org/10.1111/j.1365-2672.2006.02961.x. Pryde S E, Duncan S H, Hold G L et al. 2002. The microbiology of butyrate formation in the human colon. FEMS Microbiology Letters, 217(2): 133-139, https://doi.org/10.1016/S0378-1097(02)01106-0. Qiao G, Lv T L, Zhang M M et al. 2020. β-hydroxybutyrate(β-HB) exerts anti-inflammatory and antioxidant effects in lipopolysaccharide (LPS) -stimulated macrophages in Liza haematocheila. Fish & Shellfish Immunology, 107:444-451, https://doi.org/10.1016/j.fsi.2020.11.005. Qiao G, Sun Q R, Zhang M M et al. 2019. Antioxidant system of soiny mullet (Liza haematocheila) is responsive to dietary poly-β-hydroxybutyrate (PHB) supplementation based on immune-related enzyme activity and de novo transcriptome analysis. Fish & Shellfish Immunology, 95: 314-327, https://doi.org/10.1016/j.fsi.2019.10.042. Quillaguamáen J, Delgado O, Mattiasson B et al. 2006. Poly(β-hydroxybutyrate) production by a moderate halophile, Halomonas boliviensis LC1. Enzyme and Microbial Technology, 38(1-2): 148-154, https://doi.org/10.1016/j.enzmictec.2005.05.013. Quiroz M, Triadó -Margarit X, Casamayor E O et al. 2015.Comparison of Artemia-bacteria associations in brines, laboratory cultures and the gut environment: a study based on Chilean hypersaline environments. Extremophiles, 19(1): 135-247, https://doi.org/10.1007/s00792-014-0694-1. Quiroz-Guzmán E, Balcázar J L, Vázquez-Juárez R et al. 2013. Proliferation, colonization, and detrimental effects of Vibrio parahaemolyticus and Vibrio harveyi during brine shrimp hatching. Aquaculture, 406-407: 85-90, https://doi.org/10.1016/j.aquaculture.2013.03.008. Sapkota A, Sapkota A R, Kucharski M et al. 2008.Aquaculture practices and potential human health risks:current knowledge and future priorities. Environment International, 34(8): 1215-1226, https://doi.org/10.1016/j.envint.2008.04.009. Sui L Y, Zhang J J, Xu G C et al. 2015. Isolation and identification of Halomonas sp. from solar saltpond and study of PHB accumulation in its cells. Marine Sciences, 39(5): 16-20. (in Chinese with English abstract) Thai T Q, Wille M, Garcia-Gonzalez L et al. 2014. Poly-ß-hydroxybutyrate content and dose of the bacterial carrier for Artemia enrichment determine the performance of giant freshwater prawn larvae. Applied Microbiology and Biotechnology, 98(11): 5205-5215, https://doi.org/10.1007/s00253-014-5536-7. Tkavc R, Ausec L, Oren A et al. 2011. Bacteria associated with Artemia spp. along the salinity gradient of the solar salterns at Eilat (Israel). FEMS Microbiology Ecology, 77(2): 310-321, https://doi.org/10.1111/j.1574-6941.2011. 01112.x. Topping D L, Clifton P M. 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews, 81(3):1031-1064, https://doi.org/10.1152/physrev.2001.81.3.1031. Touraki M, Karamanlidou G, Karavida P et al. 2012.Evaluation of the probiotics Bacillus subtilis and Lactobacillus plantarum bioencapsulated in Artemia nauplii against vibriosis in European sea bass larvae (Dicentrarchus labrax, L.). World Journal of Microbiology and Biotechnology, 28(6): 2425-2433, https://doi.org/10.1007/s11274-012-1052-z. Touraki M, Karamanlidou G, Koziotis M et al. 2013.Antibacterial effect of Lactococcus lactis subsp. lactis on Artemia franciscana nauplii and Dicentrarchus labrax larvae against the fish pathogen Vibrio anguillarum.Aquaculture International, 21(2): 481-495, https://doi.org/10.1007/s10499-012-9579-4. Turnbaugh P J, Ley R E, Mahowald M A et al. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122): 1027-1031, https://doi.org/10.1038/nature05414. Van Stappen G, Sui L Y, Nguyen V H et al. 2020. Review on integrated production of the brine shrimp Artemia in solar salt ponds. Reviews in Aquaculture, 12(2): 1054-1071, https://doi.org/10.1111/raq.12371. Yévenes, M, Quiroz M, Maruyam F et al. 2021. Vibrio sp. ArtGut-C1, a polyhydroxybutyrate producer isolated from the gut of the aquaculture live diet Artemia(Crustacea). Electronic Journal of Biotechnology, 49: 22-28, https://doi.org/10.1016/j.ejbt.2020.10.003. Yin J, Chen J C, Wu Q et al. 2015. Halophiles, coming stars for industrial biotechnology. Biotechnology Advances, 33(7): 1433-1442, https://doi.org/10.1016/j.biotechadv. 2014.10.008.
|
|
|