Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon <italic style="font-style: italic">Salmo salar</italic>

Shihong XU; Yanfeng WANG; Caixia GAO; Sarath BABU V; Jun LI; Qinghua LIU; Zhizhong XIAO; Yingxuan XU; Chunyan ZHAO; Li LIN; Liang CHI

doi:10.1007/s00343-021-1336-y

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Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar

Aquaculture and Fisheries | Updated：2023-04-27

- Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar
- Journal of Oceanology and Limnology Vol. 41, Issue 1, Pages: 364-375(2023)
- Affiliations：
  
  1.Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China
  2.College of Veterinary Medicine, Qingdao Agricultural University, Qingdao 266109, China
  3.Laboratory Animal and Comparative Medicine Team, State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences(CAAS), Harbin 150069, China
  4.CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  5.Guangdong Provincial Water Environment and Aquatic Products Security Engineering Technology Research Center, Guangzhou Key Laboratory of Aquatic Animal Diseases and Waterfowl Breeding, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
  6.University College London, London WC1 E 6BT, United Kingdom
  7.School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China
  8.Guangdong Provincial Water Environment and Aquatic Products Security Engineering Technology Research Center, Guangzhou Key Laboratory of Aquatic Animal Diseases and Waterfowl Breeding, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
- Author bio：
  
  Li LIN, E-mail: linli@zhku.edu.cn
  Liang CHI, E-mail: lchi@qau.edu.cn
- Funds：
- DOI：10.1007/s00343-021-1336-y
  CLC：
- Received：31 October 2021，
  
  Accepted：11 November 2021，
  
  Online First：08 December 2021，
  
  Published：2023-01
- Accepted：
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Shihong XU, Yanfeng WANG, Caixia GAO, et al. Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar[J]. Journal of Oceanology and Limnology, 2023, 41(1): 364-375.
DOI：

Shihong XU, Yanfeng WANG, Caixia GAO, et al. Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar[J]. Journal of Oceanology and Limnology, 2023, 41(1): 364-375. DOI： 10.1007/s00343-021-1336-y.

摘要

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-1

(IL-1

)

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

baumannii

in the intestine of Atlantic salmon. Overall

these findings demonstrated that low DO level may induce stronger immunity responses in Atlantic salmon.

关键词

Keywords

references

Bojko J, Lipp E, Ford A T, Behringer D C. 2020. Pollution can drive marine diseases. In : Behringer 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 https://doi.org/10.1093/oso/9780198821632.003.0006 .

N A Bokulich , S Subramanian , J J Faith , 等 . Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing . Nature Methods , 2013 . 10 ( 1 ): 57 - 59 . DOI: 10.1038/nmeth.2276 http://doi.org/10.1038/nmeth.2276 .

J G Caporaso , J Kuczynski , J Stombaugh , 等 . QIIME allows analysis of high-throughput community sequencing data . Nature Methods , 2010 . 7 ( 5 ): 335 - 336 . DOI: 10.1038/nmeth.f.303 http://doi.org/10.1038/nmeth.f.303 .

S Cecchini , M Saroglia . Antibody response in sea bass ( Dicentrarchus labrax L. ) in relation to water temperature and oxygenation . Aquaculture Research , 2002 . 33 ( 8 ): 607 - 613 . DOI: 10.1046/j.1365-2109.2002.00698.x http://doi.org/10.1046/j.1365-2109.2002.00698.x .

G M Cerqueira , A Y Peleg . Insights into Acinetobacter baumannii pathogenicity . IUBMB Life , 2011 . 63 ( 12 ): 1055 - 1060 . DOI: 10.1002/iub.533 http://doi.org/10.1002/iub.533 .

H B Chen , P C Boutros . VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R . BMC Bioinformatics , 2011 . 12 ( 1 ): 35 DOI: 10.1186/1471-2105-12-35 http://doi.org/10.1186/1471-2105-12-35 .

S F Chen , Y Q Zhou , Y R Chen , 等 . Fastp: an ultra-fast all-in-one FASTQ preprocessor . Bioinformatics , 2018 . 34 ( 17 ): i884 - i890 . DOI: 10.1093/bioinformatics/bty560 http://doi.org/10.1093/bioinformatics/bty560 .

G Claireaux , D Webber , S Kerr , 等 . Physiology and behaviour of free-swimming Atlantic cod ( Gadus morhua ) facing fluctuating salinity and oxygenation conditions . Journal of Experimental Biology , 1995 . 198 ( 1 ): 61 - 69 . DOI: 10.1242/jeb.198.1.61 http://doi.org/10.1242/jeb.198.1.61 .

J R Conway , A Lex , N Gehlenborg . UpSetR: an R package for the visualization of intersecting sets and their properties . Bioinformatics , 2017 . 33 ( 18 ): 2938 - 2940 . DOI: 10.1093/bioinformatics/btx364 http://doi.org/10.1093/bioinformatics/btx364 .

A Cuesta , M á Esteban , J Meseguer . Effects of different stressor agents on gilthead seabream natural cytotoxic activity . Fish & Shellfish Immunology , 2003 . 15 ( 5 ): 433 - 441 . DOI: 10.1016/S1050-4648(03)00022-6 http://doi.org/10.1016/S1050-4648(03)00022-6 .

R C Edgar . MUSCLE: multiple sequence alignment with high accuracy and high throughput . Nucleic Acids Research , 2004 . 32 ( 5 ): 1792 - 1797 . DOI: 10.1093/nar/gkh340 http://doi.org/10.1093/nar/gkh340 .

R C Edgar . UPARSE: highly accurate OTU sequences from microbial amplicon reads . Nature Methods , 2013 . 10 ( 10 ): 996 - 998 . DOI: 10.1038/nmeth.2604 http://doi.org/10.1038/nmeth.2604 .

P Edwards , W B Zhang , B Belton , 等 . Misunderstandings, myths and mantras in aquaculture: its contribution to world food supplies has been systematically over reported . Marine Policy , 2019 . 106 103547 DOI: 10.1016/j.marpol.2019.103547 http://doi.org/10.1016/j.marpol.2019.103547 .

J J Evans , C A Shoemaker , P H Klesius . Effects of sublethal dissolved oxygen stress on blood glucose and susceptibility to Streptococcus agalactiae in Nile tilapia Oreochromis niloticus . Journal of Aquatic Animal Health , 2003 . 15 ( 3 ): 202 - 208 . DOI: 10.1577/H03-024 http://doi.org/10.1577/H03-024 .

Y Fukuda , M Maita , K Satoh , 等 . Influence of dissolved oxygen concentration on the mortality of yellowtail experimentally infected with Enterococcus seriolicida . Fish Pathology , 1997 . 32 ( 2 ): 129 - 130 . DOI: 10.3147/jsfp.32.129 http://doi.org/10.3147/jsfp.32.129 .

J Galindo-Villegas , D García-Moreno , Oliveira De , 等 . 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 , 2012 . 109 ( 39 ): E2605 - E2614 . DOI: 10.1073/pnas.1209920109 http://doi.org/10.1073/pnas.1209920109 .

K Hornik . The comprehensive R archive network . Wiley Interdisciplinary Reviews: Computational Statistics , 2012 . 4 ( 4 ): 394 - 398 . DOI: 10.1002/wics.1212 http://doi.org/10.1002/wics.1212 .

S D Kale , N Dikshit , P Kumar , 等 . Nod2 is required for the early innate immune clearance of Acinetobacter baumannii from the lungs . Scientific Reports , 2017 . 7 ( 1 ): 17429 DOI: 10.1038/s41598-017-17653-y http://doi.org/10.1038/s41598-017-17653-y .

M Kanther , X L Sun , M Mühlbauer , 等 . Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract . Gastroenterology , 2011 . 141 ( 1 ): 197 - 207 . DOI: 10.1053/j.gastro.2011.03.042 http://doi.org/10.1053/j.gastro.2011.03.042 .

C Kelly , I Salinas . Under pressure: interactions between commensal microbiota and the teleost immune system . Frontiers in Immunology , 2017 . 8 559 DOI: 10.3389/fimmu.2017.00559 http://doi.org/10.3389/fimmu.2017.00559 .

S Knapp , C W Wieland , S Florquin , 等 . Differential roles of CD14 and toll-like receptors 4and 2 in murine Acinetobacter pneumonia . American Journal of Respiratory and Critical Care Medicine , 2006 . 173 ( 1 ): 122 - 129 . DOI: 10.1164/rccm.200505-730OC http://doi.org/10.1164/rccm.200505-730OC .

R Kolde , M R Kolde . Package 'pheatmap' . R Package , 2015 . 1 ( 7 ): 790 .

B O Kvamme , K Gadan , F Finne-Fridell , 等 . Modulation of innate immune responses in Atlantic salmon by chronic hypoxia-induced stress . Fish & Shellfish Immunology , 2013 . 34 ( 1 ): 55 - 65 . DOI: 10.1016/j.fsi.2012.10.006 http://doi.org/10.1016/j.fsi.2012.10.006 .

K D Lafferty , C D Harvell , J M Conrad , 等 . Infectious diseases affect marine fisheries and aquaculture economics . Annual Review of Marine Science , 2015 . 7 471 - 496 . DOI: 10.1146/annurev-marine-010814-015646 http://doi.org/10.1146/annurev-marine-010814-015646 .

Y C Lu , W C Yeh , P S Ohashi . LPS/TLR4 signal transduction pathway . Cytokine , 2008 . 42 ( 2 ): 145 - 151 . DOI: 10.1016/j.cyto.2008.01.006 http://doi.org/10.1016/j.cyto.2008.01.006 .

T Magoč , S L Salzberg . FLASH: fast length adjustment of short reads to improve genome assemblies . Bioinformatics , 2011 . 27 ( 21 ): 2957 - 2963 . DOI: 10.1093/bioinformatics/btr507 http://doi.org/10.1093/bioinformatics/btr507 .

A Meziti , E Mente , K A Kormas . Gut bacteria associated with different diets in reared Nephrops norvegicus . Systematic and Applied Microbiology , 2012 . 35 ( 7 ): 473 - 482 . DOI: 10.1016/j.syapm.2012.07.004 http://doi.org/10.1016/j.syapm.2012.07.004 .

National Research Council . Guide for the Care and Use of Laboratory Animals , : Washington D C The National Academies Press , 1996 . DOI: 10.17226/5140 http://doi.org/10.17226/5140 .

K M Nutsch , C S Hsieh . T cell tolerance and immunity to commensal bacteria . Current Opinion in Immunology , 2012 . 24 ( 4 ): 385 - 391 . DOI: 10.1016/j.coi.2012.04.009 http://doi.org/10.1016/j.coi.2012.04.009 .

S Omenetti , T T Pizarro . The Treg/Th17 axis: a dynamic balance regulated by the gut microbiome . Frontiers in Immunology , 2015 . 6 639 DOI: 10.3389/fimmu.2015.00639 http://doi.org/10.3389/fimmu.2015.00639 .

S Pires , D Parker . Innate immune responses to Acinetobacter baumannii in the airway . Journal of Interferon & Cytokine Research , 2019 . 39 ( 8 ): 441 - 449 . DOI: 10.1089/jir.2019.0008 http://doi.org/10.1089/jir.2019.0008 .

H Y Qiu , R KuoLee , G Harris , 等 . Role of macrophages in early host resistance to respiratory Acinetobacter baumannii infection . PLoS One , 2012 . 7 ( 6 ): e40019 DOI: 10.1371/journal.pone.0040019 http://doi.org/10.1371/journal.pone.0040019 .

J F Rawls , M A Mahowald , R E Ley , 等 . Reciprocal gut microbiota transplants from zebrafish and mice to germfree recipients reveal host habitat selection . Cell , 2006 . 127 ( 2 ): 423 - 433 . DOI: 10.1016/j.cell.2006.08.043 http://doi.org/10.1016/j.cell.2006.08.043 .

J L Round , S K Mazmanian . 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 , 2010 . 107 ( 27 ): 12204 - 12209 . DOI: 10.1073/pnas.0909122107 http://doi.org/10.1073/pnas.0909122107 .

G X Sun , Y Liu , D G Qiu , 等 . 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 , 2016 . 47 ( 1 ): 176 - 188 . DOI: 10.1111/are.12480 http://doi.org/10.1111/are.12480 .

H Van Faassen , R KuoLee , G Harris , 等 . Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice . Infection and Immunity , 2007 . 75 ( 12 ): 5597 - 5608 . DOI: 10.1128/IAI.00762-07 http://doi.org/10.1128/IAI.00762-07 .

Q Wang , G M Garrity , J M Tiedje , 等 . Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy . Applied and Environmental Microbiology , 2007 . 73 ( 16 ): 5261 - 5267 . DOI: 10.1128/AEM.00062-07 http://doi.org/10.1128/AEM.00062-07 .

Y F Wang , L Chi , Q H Liu , 等 . 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 , 2019 . 37 ( 1 ): 350 - 360 . DOI: 10.1007/s00343-019-7350-7 http://doi.org/10.1007/s00343-019-7350-7 .

T L Welker , S T Mcnulty , P H Klesius . Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus , to enteric septicemia . Journal of the World Aquaculture Society , 2007 . 38 ( 1 ): 12 - 23 . DOI: 10.1111/j.1749-7345.2006.00069.x http://doi.org/10.1111/j.1749-7345.2006.00069.x .

C L Wu , Y L Lee , K M Chang , 等 . Bronchoalveolar interleukin-1β: a marker of bacterial burden in mechanically ventilated patients with community-acquired pneumonia . Critical Care Medicine , 2003 . 31 ( 3 ): 812 - 817 . DOI: 10.1097/01.CCM.0000054865.47068.58 http://doi.org/10.1097/01.CCM.0000054865.47068.58 .

H P Yang , E Hu , J T Buchanan , T R Tiersch . A strategy for sperm cryopreservation of Atlantic salmon, Salmo salar , for remote commercial-scale high-throughput processing . Journal of the World Aquaculture Society , 2018 . 49 ( 1 ): 96 - 112 . DOI: 10.1111/jwas.12431 http://doi.org/10.1111/jwas.12431 .

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⁰

Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar

DOI：10.1007/s00343-021-1336-y

摘要

Abstract

关键词

Keywords

references