Abstract
Dissolved oxygen (DO) is one of most important factors which affect wide range physiologic features of fish, including immune responses and intestinal bacterial community. However, the underlying mechanisms remain enigmatic. To address this question, the intestinal bacterial community compositions and the immune features of Atlantic salmon (Salmo salar) grown in recirculating aquaculture systems (RAS) were characterized. Fish were reared under different DO saturation levels, e.g., 200% saturation named high group (H), 100% saturation named control group (CK), and 60% saturation named lower group (L). Large variations in the operational taxonomic units (OTUs) frequency distribution for the intestinal bacterial community of Atlantic salmon were observed. The intestinal bacterial community of all groups was dominated mainly by three phyla, e.g., Proteobacteria, Firmicutes, and Bacteroidetes. Interestingly, Acinetobacter baumannii, an opportunistic pathogen of salmon was increased significantly in L group. We further monitored the immunity features of fish under different DO levels. The results show that leucocyte number, cortisol level, the expressions of interleukin-1β (IL-1β), Toll-like receptor 4 (TLR4), and nucleotide-binding oligomerization domain like protein 2 (NOD2) were higher at significant levels in the L group than those in the other two groups. TLR4 and NOD2 are usually related with the bacterial infections; therefore, it is reasonable to believe that the stronger immune responses observed in the L group might be related with the higher abundance of A. baumannii in the intestine of Atlantic salmon. Overall, these findings demonstrated that low DO level may induce stronger immunity responses in Atlantic salmon.
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Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Bojko J, Lipp E, Ford A T, Behringer D C. 2020. Pollution can drive marine diseases. In: [eiBehringer D C, Silliman B R, Lafferty K D} eds. Marine Disease Ecology. Oxford Scholarship Online, Oxford. p.95–113, https://doi.org/10.1093/oso/9780198821632.003.0006.
Bokulich N A, Subramanian S, Faith J J et al. 2013. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10(1): 57–59, https://doi.org/10.1038/nmeth.2276.
Caporaso J G, Kuczynski J, Stombaugh J et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, https://doi.org/10.1038/nmeth.f.303.
Cecchini S, Saroglia M. 2002. Antibody response in sea bass (Dicentrarchus labrax L.) in relation to water temperature and oxygenation. Aquaculture Research, 33(8): 607–613, https://doi.org/10.1046/j.1365-2109.2002.00698.x.
Cerqueira G M, Peleg A Y. 2011. Insights into Acinetobacter baumannii pathogenicity. IUBMB Life, 63(12): 1055–1060, https://doi.org/10.1002/iub.533.
Chen H B, Boutros P C. 2011. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics, 12(1): 35, https://doi.org/10.1186/1471-2105-12-35.
Chen S F, Zhou Y Q, Chen Y R et al. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884–i890, https://doi.org/10.1093/bioinformatics/bty560.
Claireaux G, Webber D, Kerr S et al. 1995. Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating salinity and oxygenation conditions. Journal of Experimental Biology, 198(1): 61–69, https://doi.org/10.1242/jeb.198.1.61.
Conway J R, Lex A, Gehlenborg N. 2017. UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics, 33(18): 2938–2940, https://doi.org/10.1093/bioinformatics/btx364.
Cuesta A, Esteban M Á, Meseguer J. 2003. Effects of different stressor agents on gilthead seabream natural cytotoxic activity. Fish & Shellfish Immunology, 15(5): 433–441, https://doi.org/10.1016/S1050-4648(03)00022-6.
Edgar R C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5): 1792–1797, https://doi.org/10.1093/nar/gkh340.
Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998, https://doi.org/10.1038/nmeth.2604.
Edwards P, Zhang W B, Belton B et al. 2019. Misunderstandings, myths and mantras in aquaculture: its contribution to world food supplies has been systematically over reported. Marine Policy, 106: 103547, https://doi.org/10.1016/j.marpol.2019.103547.
Evans J J, Shoemaker C A, Klesius P H. 2003. Effects of sublethal dissolved oxygen stress on blood glucose and susceptibility to Streptococcus agalactiae in Nile tilapia Oreochromis niloticus. Journal of Aquatic Animal Health, 15(3): 202–208, https://doi.org/10.1577/H03-024.
Fukuda Y, Maita M, Satoh K et al. 1997. Influence of dissolved oxygen concentration on the mortality of yellowtail experimentally infected with Enterococcus seriolicida. Fish Pathology, 32(2): 129–130, https://doi.org/10.3147/jsfp.32.129.
Galindo-Villegas J, García-Moreno D, De Oliveira et al. 2012. Regulation of immunity and disease resistance by commensal microbes and chromatin modifications during zebrafish development. Proceedings of the National Academy of Sciences of the United States of America, 109(39): E2605–E2614, https://doi.org/10.1073/pnas.1209920109.
Hornik K. 2012. The comprehensive R archive network. Wiley Interdisciplinary Reviews: Computational Statistics, 4(4): 394–398, https://doi.org/10.1002/wics.1212.
Kale S D, Dikshit N, Kumar P et al. 2017. Nod2 is required for the early innate immune clearance of Acinetobacter baumannii from the lungs. Scientific Reports, 7(1): 17429, https://doi.org/10.1038/s41598-017-17653-y.
Kanther M, Sun X L, Mühlbauer M et al. 2011. Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract. Gastroenterology, 141(1): 197–207, https://doi.org/10.1053/j.gastro.2011.03.042.
Kelly C, Salinas I. 2017. Under pressure: interactions between commensal microbiota and the teleost immune system. Frontiers in Immunology, 8: 559, https://doi.org/10.3389/fimmu.2017.00559.
Knapp S, Wieland C W, Florquin S et al. 2006. Differential roles of CD14 and toll-like receptors 4and 2 in murine Acinetobacter pneumonia. American Journal of Respiratory and Critical Care Medicine, 173(1): 122–129, https://doi.org/10.1164/rccm.200505-730OC.
Kolde R, Kolde M R. 2015. Package ‘pheatmap’. R Package, 1(7): 790.
Kvamme B O, Gadan K, Finne-Fridell F et al. 2013. Modulation of innate immune responses in Atlantic salmon by chronic hypoxia-induced stress. Fish & Shellfish Immunology, 34(1): 55–65, https://doi.org/10.1016/j.fsi.2012.10.006.
Lafferty K D, Harvell C D, Conrad J M et al. 2015. Infectious diseases affect marine fisheries and aquaculture economics. Annual Review of Marine Science, 7: 471–496, https://doi.org/10.1146/annurev-marine-010814-015646.
Lu Y C, Yeh W C, Ohashi P S. 2008. LPS/TLR4 signal transduction pathway. Cytokine, 42(2): 145–151, https://doi.org/10.1016/j.cyto.2008.01.006.
Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957–2963, https://doi.org/10.1093/bioinformatics/btr507.
Meziti A, Mente E, Kormas K A. 2012. Gut bacteria associated with different diets in reared Nephrops norvegicus. Systematic and Applied Microbiology, 35(7): 473–482, https://doi.org/10.1016/j.syapm.2012.07.004.
National Research Council. 1996. Guide for the Care and Use of Laboratory Animals. Washington D C. The National Academies Press, https://doi.org/10.17226/5140.
Nutsch K M, Hsieh C S. 2012. T cell tolerance and immunity to commensal bacteria. Current Opinion in Immunology, 24(4): 385–391, https://doi.org/10.1016/j.coi.2012.04.009.
Omenetti S, Pizarro T T. 2015. The Treg/Th17 axis: a dynamic balance regulated by the gut microbiome. Frontiers in Immunology, 6: 639, https://doi.org/10.3389/fimmu.2015.00639. sai]Pires S, Parker D. 2019. Innate immune responses to Acinetobacter baumannii in the airway. Journal of Interferon & Cytokine Research, 39(8): 441–449, https://doi.org/10.1089/jir.2019.0008.
Qiu H Y, KuoLee R, Harris G et al. 2012. Role of macrophages in early host resistance to respiratory Acinetobacter baumannii infection. PLoS One, 7(6): e40019, https://doi.org/10.1371/journal.pone.0040019.
Rawls J F, Mahowald M A, Ley R E et al. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell, 127(2): 423–433, https://doi.org/10.1016/j.cell.2006.08.043.
Round J L, Mazmanian S K. 2010. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America, 107(27): 12204–12209, https://doi.org/10.1073/pnas.0909122107.
Sun G X, Liu Y, Qiu D G et al. 2016. Effects of feeding rate and frequency on growth performance, digestion and nutrients balances of Atlantic salmon (Salmo salar) in recirculating aquaculture systems (RAS). Aquaculture Research, 47(1): 176–188, https://doi.org/10.1111/are.12480.
Van Faassen H, KuoLee R, Harris G et al. 2007. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infection and Immunity, 75(12): 5597–5608, https://doi.org/10.1128/IAI.00762-07.
Wang Q, Garrity G M, Tiedje J M et al. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267, https://doi.org/10.1128/AEM.00062-07.
Wang Y F, Chi L, Liu Q H et al. 2019. Effects of stocking density on the growth and immunity of Atlantic salmon Salmo salar reared in recirculating aquaculture system (RAS). Journal of Oceanology and Limnology, 37(1): 350–360, https://doi.org/10.1007/s00343-019-7350-7.
Welker T L, Mcnulty S T, Klesius P H. 2007. Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. Journal of the World Aquaculture Society, 38(1): 12–23, https://doi.org/epdf/10.1111/j.1749-7345.2006.00069.x.
Wu C L, Lee Y L, Chang K M et al. 2003. Bronchoalveolar interleukin-1β: a marker of bacterial burden in mechanically ventilated patients with community-acquired pneumonia. Critical Care Medicine, 31(3): 812–817, https://doi.org/10.1097/01.CCM.0000054865.47068.58.
Yang H P, Hu E, Buchanan J T, Tiersch T R. 2018. A strategy for sperm cryopreservation of Atlantic salmon, Salmo salar, for remote commercial-scale high-throughput processing. Journal of the World Aquaculture Society, 49(1): 96–112, https://doi.org/epdf/10.1111/jwas.12431.
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Supported by the Shandong Province Key Research and Invention Program (No. 2017CXGC010K), the China Agriculture Research System (No. CARS-47), the National Key Research and Development Program (No. 2018YFD0901204), the National Infrastructure of Fishery Germplasm Resource (No. 2019DKA30470), the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2018SDKJ0502-2), the National Natural Science Foundation of China (Nos. 31872606, 31572657, U1701233, 31402283, 31802319), the Department of Agriculture and Rural Areas of Guangdong Province (No. KA1911101), the Natural Science Foundation of Shandong Province (No. ZR2018BC053), the Agricultural Application Technology Innovation Project of Shandong Province in 2018/2019 (No. SD2019YY011), and the Shandong Province Major Scientific and Technological Innovation Projects (No. 2019JZZY020710)
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Xu, S., Wang, Y., Gao, C. et al. Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar. J. Ocean. Limnol. 41, 364–375 (2023). https://doi.org/10.1007/s00343-021-1336-y
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DOI: https://doi.org/10.1007/s00343-021-1336-y