Salinity significantly affects intestinal microbiota and gene expression in striped catfish juveniles

Gene expression; Intestinal microbiota; Osmoregulation; Salinity; Striped catfish; Ion exchange; Pattern recognition; Proteins; Water; Exposed to; Fish species; Fresh Water; Freshwater fishes; Genes expression; Microbiotas; Phylogenetic diversity; Fish; bacterial RNA; chaperonin 60; fresh water; heat shock protein 70; heat shock protein 90; pattern recognition receptor; RNA 16S; salt water; fish; gene expression; ion exchange; juvenile; microorganism; osmoregulation; pollution exposure; salinity; Akkermansia; Article; bacterial gene; Bacteroidetes; catfish; controlled study; DNA extraction; environmental exposure; Firmicutes; gene control; immune response; intestine flora; metabolism; microbial diversity; nonhuman; operational taxonomic unit; osmotic stress; phylogeny; Proteobacteria; Verrucomicrobia; Vibrio; animal; physiology; Ireland; Shannon; Animals; Catfishes; Gastrointestinal Microbiome; Gene Expression; Phylogeny

Abstract :

[en] Abstract: In the present study, juvenile striped catfish (Pangasianodon hypophthalmus), a freshwater fish species, have been chronically exposed to a salinity gradient from freshwater to 20 psu (practical salinity unit) and were sampled at the beginning (D20) and the end (D34) of exposure. The results revealed that the intestinal microbial profile of striped catfish reared in freshwater conditions were dominated by the phyla Bacteroidetes, Firmicutes, Proteobacteria, and Verrucomicrobia. Alpha diversity measures (observed OTUs (operational taxonomic units), Shannon and Faith’s PD (phylogenetic diversity)) showed a decreasing pattern as the salinities increased, except for the phylogenetic diversity at D34, which was showing an opposite trend. Furthermore, the beta diversity between groups was significantly different. Vibrio and Akkermansia genera were affected differentially with increasing salinity, the former being increased while the latter was decreased. The genus Sulfurospirillium was found predominantly in fish submitted to salinity treatments. Regarding the host response, the fish intestine likely contributed to osmoregulation by modifying the expression of osmoregulatory genes such as nka1a, nka1b, slc12a1, slc12a2, cftr, and aqp1, especially in fish exposed to 15 and 20 psu. The expression of heat shock proteins (hsp) hsp60, hsp70, and hsp90 was significantly increased in fish reared in 15 and 20 psu. On the other hand, the expression of pattern recognition receptors (PRRs) were inhibited in fish exposed to 20 psu at D20. In conclusion, the fish intestinal microbiota was significantly disrupted in salinities higher than 10 psu and these effects were proportional to the exposure time. In addition, the modifications of intestinal gene expression related to ion exchange and stressful responses may help the fish to adapt hyperosmotic environment. Key points: • It is the first study to provide detailed information on the gut microbiota of fish using the amplicon sequencing method. • Salinity environment significantly modified the intestinal microbiota of striped catfish. • Intestinal responses may help the fish adapt to hyperosmotic environment. © 2022, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Disciplines :

Animal production & animal husbandry

Author, co-author :

Hieu, D.Q.; Research Unit in Environmental and Evolutionary Biology, Institute of Life Earth & Environment (ILEE), University of Namur, Namur, Belgium

Hang, B.T.B.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

Lokesh, J.; Université de Pau Et Des Pays de L’Adour, Saint-Pee-sur-Nivelle, NuMéA, INRAE, E2S UPPA, France

Garigliany, Mutien-Marie ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie générale et autopsies

Huong, D.T.T.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

Yen, D.T.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

Liem, P.T.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

Tam, B.M.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

Hai, D.M.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam, Department of Animal Production, Faculty of Veterinary Medicine, University of Liège, Liege, Belgium

Son, V.N.; College of Aquaculture and Fisheries, Can Tho University, Can Tho City, Viet Nam

More authors (3 more)

Language :

English

Title :

Salinity significantly affects intestinal microbiota and gene expression in striped catfish juveniles

Publication date :

2022

Journal title :

Applied Microbiology and Biotechnology

ISSN :

0175-7598

eISSN :

1432-0614

Publisher :

Springer Science and Business Media Deutschland GmbH

Volume :

106

Issue :

Pages :

3245 - 3264

Peer reviewed :

Peer Reviewed verified by ORBi

Funding text :

The research was supported by the Académie de Recherche et d’Enseignement Supérieur (ARES) and the General Directorate and Development for Cooperation (DGD) in Belgium.

Available on ORBi :

since 11 May 2023

Statistics

Number of views

100 (2 by ULiège)

Number of downloads

153 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abdel-Moein KA, Saeed H, Samir A (2015) Novel detection of Helicobacter pylori in fish: a possible public health concern. Acta Trop 152:141–144. 10.1016/j.actatropica.2015.09.005 DOI: 10.1016/j.actatropica.2015.09.005
Aoki M, Kaneko T, Katoh F, Hasegawa S, Tsutsui N, Aida K (2003) Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. J Exp Biol 206:3495–3505. 10.1242/jeb.00579 DOI: 10.1242/jeb.00579
Asnicar F, Weingart G, Tickle TL, Huttenhower C, Segata N (2015) Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3:e1029 DOI: 10.7717/peerj.1029
Baldo L, Riera JL, Salzburger W, Barluenga M (2019) Phylogeography and ecological niche shape the cichlid fish gut microbiota in Central American and African Lakes. Front Microbiol 10:2372 DOI: 10.3389/fmicb.2019.02372
Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal Alkaline Phosphatase Detoxifies Lipopolysaccharide and Prevents Inflammation in Zebrafish in Response to the Gut Microbiota. Cell Host Microbe 2:371–382. 10.1016/j.chom.2007.10.010 DOI: 10.1016/j.chom.2007.10.010
Bledsoe JW, Peterson BC, Swanson KS, Small BC (2016) 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 11:e0166379–e0166379. 10.1371/journal.pone.0166379 DOI: 10.1371/journal.pone.0166379
Chang X, Wang X, Feng J, Su X, Liang J, Li H, Zhang J (2020) Impact of chronic exposure to trichlorfon on intestinal barrier, oxidative stress, inflammatory response and intestinal microbiome in common carp (Cyprinus carpio L.). Environ Pollut 259:113846. 10.1016/j.envpol.2019.113846 DOI: 10.1016/j.envpol.2019.113846
Chen Y-H, Lu C-W, Shyu Y-T, Lin S-S (2017) Revealing the saline adaptation strategies of the halophilic bacterium Halomonas beimenensis through high-throughput omics and transposon mutagenesis approaches. Sci Rep 7:13037. 10.1038/s41598-017-13450-9 DOI: 10.1038/s41598-017-13450-9
De Wachter B, Scholliers A, Blust R (1998) Semiquantitative immunoblot detection of 70 kDa stress proteins in the carp Cyprinus carpio. Bull Environ Contam Toxicol 60:37–44. 10.1007/s001289900588 DOI: 10.1007/s001289900588
Deane EE, Woo NYS (2004) Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). Am J Physiol Integr Comp Physiol 287:R1054–R1063 DOI: 10.1152/ajpregu.00347.2004
Deane EE, Kelly SP, Luk JCY, Woo NYS (2002) Chronic salinity adaptation modulates hepatic heat shock protein and insulin-like growth factor I expression in black sea bream. Mar Biotechnol 4:193–205
Deane E, Luk J, Woo NYS (2011) Aquaporin 1a expression in gill, intestine, and kidney of the euryhaline silver sea bream. Front Physiol 2:39 DOI: 10.3389/fphys.2011.00039
Dehler CE, Secombes CJ, Martin SAM (2017) Seawater transfer alters the intestinal microbiota profiles of Atlantic salmon (Salmo salar L.). Sci Rep 7:13877. 10.1038/s41598-017-13249-8 DOI: 10.1038/s41598-017-13249-8
Dehler CE, Secombes CJ, Martin SAM (2017) Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L.). Aquaculture 467:149–157. 10.1016/j.aquaculture.2016.07.017 DOI: 10.1016/j.aquaculture.2016.07.017
Demirci M, Tokman HB, Uysal HK, Demiryas S, Karakullukcu A, Saribas S, Cokugras H, Kocazeybek BS (2019) Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergol Immunopathol (madr) 47:365–371. 10.1016/j.aller.2018.12.009 DOI: 10.1016/j.aller.2018.12.009
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. 10.1038/s41587-020-0548-6 DOI: 10.1038/s41587-020-0548-6
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. 10.1038/nmeth.2604 DOI: 10.1038/nmeth.2604
Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci 110:9066 LP – 9071. 10.1073/pnas.1219451110 DOI: 10.1073/pnas.1219451110
Fabret C, Feher VA, Hoch JA (1999) Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181:1975–1983. 10.1128/JB.181.7.1975-1983.1999 DOI: 10.1128/JB.181.7.1975-1983.1999
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. 10.1016/0006-3207(92)91201-3 DOI: 10.1016/0006-3207(92)91201-3
FAO (2020) GLOBEFISH Highlights January 2020 issue, with Jan. – Sep. 2019 Statistics – A quarterly update on world seafood markets. Globefish Highlights no. 1–2020. Rome. 10.4060/ca7968en
Fasano A, Shea-Donohue T (2005) Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2:416–422. 10.1038/ncpgasthep0259 DOI: 10.1038/ncpgasthep0259
Gallique M, Bouteiller M, Merieau A (2017) The type VI secretion system: a dynamic system for bacterial communication? Front Microbiol 8:1454 DOI: 10.3389/fmicb.2017.01454
Gancz H, Jones KR, Merrell DS (2008) Sodium chloride affects Helicobacter pylori growth and gene expression. J Bacteriol 190:4100–4105. 10.1128/JB.01728-07 DOI: 10.1128/JB.01728-07
Gioacchini G, Rossi G, Carnevali O (2017) Host-probiotic interaction: new insight into the role of the endocannabinoid system by in vivo and ex vivo approaches. Sci Rep 7:1261. 10.1038/s41598-017-01322-1 DOI: 10.1038/s41598-017-01322-1
Givens CE, Bowers JC, DePaola A, Hollibaugh JT, Jones JL (2014) Occurrence and distribution of Vibrio vulnificus and Vibrio parahaemolyticus – potential roles for fish, oyster, sediment and water. Lett Appl Microbiol 58:503–510. 10.1111/lam.12226 DOI: 10.1111/lam.12226
Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154. 10.1111/j.1574-695X.2007.00343.x DOI: 10.1111/j.1574-695X.2007.00343.x
Gómez-Gallego C, Pohl S, Salminen S, De Vos WM, Kneifel W (2016) Akkermansia muciniphila: a novel functional microbe with probiotic properties. Benef Microbes 7:571–584 DOI: 10.3920/BM2016.0009
Gregório SF, Carvalho ESM, Encarnação S, Wilson JM, Power DM, Canário AVM, Fuentes J (2013) Adaptation to different salinities exposes functional specialization in the intestine of the sea bream (Sparus aurata L.). J Exp Biol 216:470–479. 10.1242/jeb.073742 DOI: 10.1242/jeb.073742
Grosell M (2006) Intestinal anion exchange in marine fish osmoregulation. J Exp Biol 209:2813–2827. 10.1242/jeb.02345 DOI: 10.1242/jeb.02345
Grosell M (2010) The role of the gastrointestinal tract in salt and water balance. In: Grosell M (ed) Fish physiology. Elsevier, pp 135–164
Hall M, Beiko RG (2018) 16S rRNA gene analysis with QIIME2. In: Beiko RG, Hsiao W, Parkinson J (eds) Microbiome analysis. Springer New York, pp 113–129. 10.1007/978-1-4939-8728-3_8
Herlemann DPR, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. 10.1038/ismej.2011.41 DOI: 10.1038/ismej.2011.41
Hightower LE (1991) Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66:191–197 DOI: 10.1016/0092-8674(91)90611-2
Hörmannsperger G, Haller D (2010) Molecular crosstalk of probiotic bacteria with the intestinal immune system: clinical relevance in the context of inflammatory bowel disease. Int J Med Microbiol 300:63–73. 10.1016/j.ijmm.2009.08.006 DOI: 10.1016/j.ijmm.2009.08.006
Humphreys C (2020) Intestinal Permeability. In: Pizzorno JE, Murray MT (eds) Textbook of Natural Medicine, 5th edn. Churchill Livingstone, St. Louis (MO), pp 166–177 DOI: 10.1016/B978-0-323-43044-9.00019-4
Jahid IK, Mizan MFR, Ha AJ, Ha S-D (2015) Effect of salinity and incubation time of planktonic cells on biofilm formation, motility, exoprotease production, and quorum sensing of Aeromonas hydrophila. Food Microbiol 49:142–151. 10.1016/j.fm.2015.01.016 DOI: 10.1016/j.fm.2015.01.016
Karlsen C, Paulsen SM, Tunsjø HS, Krinner S, Sørum H, Haugen P, Willassen N-P (2008) Motility and flagellin gene expression in the fish pathogen Vibrio salmonicida: Effects of salinity and temperature. Microb Pathog 45:258–264. 10.1016/j.micpath.2008.06.002 DOI: 10.1016/j.micpath.2008.06.002
Kazakov AE, Rodionov DA, Alm E, Arkin AP, Dubchak I, Gelfand MS (2009) Comparative genomics of regulation of fatty acid and branched-chain amino acid utilization in proteobacteria. J Bacteriol 191:52–64. 10.1128/JB.01175-08 DOI: 10.1128/JB.01175-08
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1. 10.1093/nar/gks808 DOI: 10.1093/nar/gks808
Kruse S, Goris T, Westermann M, Adrian L, Diekert G (2018) Hydrogen production by Sulfurospirillum species enables syntrophic interactions of Epsilonproteobacteria. Nat Commun 9:4872. 10.1038/s41467-018-07342-3 DOI: 10.1038/s41467-018-07342-3
Langenheder S, Kisand V, Wikner J, Tranvik LJ (2003) Salinity as a structuring factor for the composition and performance of bacterioplankton degrading riverine DOC. FEMS Microbiol Ecol 45:189–202. 10.1016/S0168-6496(03)00149-1 DOI: 10.1016/S0168-6496(03)00149-1
Larsen MH, Blackburn N, Larsen JL, Olsen JE (2004) Influences of temperature, salinity and starvation on the motility and chemotactic response of Vibrio anguillarum. Microbiology 150:1283–1290. 10.1099/mic.0.26379-0 DOI: 10.1099/mic.0.26379-0
Larsen PF, Nielsen EE, Koed A, Thomsen DS, Olsvik PA, Loeschcke V (2008) Interpopulation differences in expression of candidate genes for salinity tolerance in winter migrating anadromous brown trout (Salmo trutta L.). BMC Genet 9:1–9 DOI: 10.1186/1471-2156-9-12
Laverty G, Skadhauge E (2012) Adaptation of teleosts to very high salinity. Comp Biochem Physiol Part A Mol Integr Physiol 163:1–6. 10.1016/j.cbpa.2012.05.203 DOI: 10.1016/j.cbpa.2012.05.203
Le D, Nguyen P, Nguyen D, Dierckens K, Boon N, Lacoere T, Kerckhof F-M, De Vrieze J, Vadstein O, Bossier P (2020) Gut microbiota of migrating wild rabbit fish (Siganus guttatus) larvae have low spatial and temporal variability. Microb Ecol 79:539–551. 10.1007/s00248-019-01436-1 DOI: 10.1007/s00248-019-01436-1
Li J, Dai Z, Jana D, Callaway DJE, Bu Z (2005) Ezrin controls the macromolecular complexes formed between an adapter protein Na+/H+ exchanger regulatory factor and the cystic fibrosis transmembrane conductance regulator*. J Biol Chem 280:37634–37643. 10.1074/jbc.M502305200 DOI: 10.1074/jbc.M502305200
Li Z, Lui EY, Wilson JM, Ip YK, Lin Q, Lam TJ, Lam SH (2014) Expression of key ion transporters in the gill and esophageal-gastrointestinal tract of euryhaline Mozambique tilapia Oreochromis mossambicus acclimated to fresh water, seawater and hypersaline water. PLoS One 9:e87591 DOI: 10.1371/journal.pone.0087591
Lin YM, Chen CN, Lee TH (2003) The expression of gill Na, K-ATPase in milkfish, Chanos chanos, acclimated to seawater, brackish water and fresh water. Comp Biochem Physiol Part A Mol Integr Physiol 135:489–497 DOI: 10.1016/S1095-6433(03)00136-3
Lind U, Alm Rosenblad M, Wrange A-L, Sundell KS, Jonsson PR, André C, Havenhand J, Blomberg A (2013) Molecular characterization of the α-subunit of Na+/K+ ATPase from the euryhaline barnacle Balanus improvisus reveals multiple genes and differential expression of alternative splice variants. PLoS ONE 8:e77069–e77069. 10.1371/journal.pone.0077069 DOI: 10.1371/journal.pone.0077069
Liu C, Sun D, Zhu J, Liu W (2019) Two-Component Signal Transduction Systems: A Major Strategy for Connecting Input Stimuli to Biofilm Formation. Front Microbiol 9:3279 DOI: 10.3389/fmicb.2018.03279
Lokesh J, Kiron V, Sipkema D, Fernandes JMO, Moum T (2019) Succession of embryonic and the intestinal bacterial communities of Atlantic salmon (Salmo salar) reveals stage-specific microbial signatures. Microbiologyopen 8:e00672. 10.1002/mbo3.672 DOI: 10.1002/mbo3.672
Louca S, Doebeli M (2018) Efficient comparative phylogenetics on large trees. Bioinformatics 34:1053–1055 DOI: 10.1093/bioinformatics/btx701
Madsen SS, Bujak J, Tipsmark CK (2014) Aquaporin expression in the Japanese medaka (Oryzias latipes) in freshwater and seawater: challenging the paradigm of intestinal water transport? J Exp Biol 217:3108–3121. 10.1242/jeb.105098 DOI: 10.1242/jeb.105098
Malakpour Kolbadinezhad S, Coimbra J, Wilson JM (2018) Osmoregulation in the Plotosidae catfish: Role of the salt secreting dendritic organ. Front Physiol 9:761 DOI: 10.3389/fphys.2018.00761
Marshall WS, Grosell M (2005) Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Clairborne JB (eds) The physiology of fishes. CRC Press, Boca Raton, pp 177–230
Marshall WS, Singer TD (2002) Cystic fibrosis transmembrane conductance regulator in teleost fish. Biochim Biophys Acta - Biomembr 1566:16–27. 10.1016/S0005-2736(02)00584-9 DOI: 10.1016/S0005-2736(02)00584-9
Martin SAM, Dehler CE, Król E (2016) Transcriptomic responses in the fish intestine. Dev Comp Immunol 64:103–117. 10.1016/j.dci.2016.03.014 DOI: 10.1016/j.dci.2016.03.014
Martinez A-S, Cutler CP, Wilson GD, Phillips C, Hazon N, Cramb G (2005) Regulation of expression of two aquaporin homologs in the intestine of the European eel: effects of seawater acclimation and cortisol treatment. Am J Physiol Integr Comp Physiol 288:R1733–R1743. 10.1152/ajpregu.00747.2004 DOI: 10.1152/ajpregu.00747.2004
Masip L, Veeravalli K, Georgiou G (2006) The many faces of glutathione in bacteria. Antioxid Redox Signal 8:753–762. 10.1089/ars.2006.8.753 DOI: 10.1089/ars.2006.8.753
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217 DOI: 10.1371/journal.pone.0061217
Mishra P, Samanta M, Mohanty S, Maiti NK (2010) Characterization of Vibrio species isolated from freshwater fishes by ribotyping. Indian J Microbiol 50:101–103. 10.1007/s12088-010-0010-4 DOI: 10.1007/s12088-010-0010-4
Mitchell JG, Kogure K (2006) Bacterial motility: links to the environment and a driving force for microbial physics. FEMS Microbiol Ecol 55:3–16 DOI: 10.1111/j.1574-6941.2005.00003.x
Mundy PC, Jeffries KM, Fangue NA, Connon RE (2020) Differential regulation of select osmoregulatory genes and Na+/K+-ATPase paralogs may contribute to population differences in salinity tolerance in a semi-anadromous fish. Comp Biochem Physiol Part A Mol Integr Physiol 240:110584. 10.1016/j.cbpa.2019.110584 DOI: 10.1016/j.cbpa.2019.110584
Nguyen PTH, Do HTT, Mather PB, Hurwood DA (2014) Experimental assessment of the effects of sublethal salinities on growth performance and stress in cultured tra catfish (Pangasianodon hypophthalmus). Fish Physiol Biochem 40:1839–1848. 10.1007/s10695-014-9972-1 DOI: 10.1007/s10695-014-9972-1
Pan F, Zarate JM, Tremblay GC, Bradley TM (2000) Cloning and characterization of salmon hsp90 cDNA: Upregulation by thermal and hyperosmotic stress. J Exp Zool 287:199–212. 10.1002/1097-010X(20000801)287:3%3c199::AID-JEZ2%3e3.0.CO;2-3 DOI: 10.1002/1097-010X(20000801)287:3<199::AID-JEZ2>3.0.CO;2-3
Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz JL (2010) Host–microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355 DOI: 10.1038/mi.2010.12
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. 10.1093/nar/29.9.e45 DOI: 10.1093/nar/29.9.e45
Picchietti S, Fausto AM, Randelli E, Carnevali O, Taddei AR, Buonocore F, Scapigliati G, Abelli L (2009) Early treatment with Lactobacillus delbrueckii strain induces an increase in intestinal T-cells and granulocytes and modulates immune-related genes of larval Dicentrarchus labrax (L.). Fish Shellfish Immunol 26:368–376. 10.1016/j.fsi.2008.10.008 DOI: 10.1016/j.fsi.2008.10.008
Randa MA, Polz MF, Lim E (2004) Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70:5469–5476. 10.1128/AEM.70.9.5469-5476.2004 DOI: 10.1128/AEM.70.9.5469-5476.2004
Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci U S A 101:4596–4601. 10.1073/pnas.0400706101 DOI: 10.1073/pnas.0400706101
Ray AK, Ringø E (2014) The gastrointestinal tract of fish. In: Merrifield D, Ringø E (eds) Aquaculture nutrition: gut health, probiotics and prebiotics. Wiley-Blackwell Publishing, Oxford, UK, pp 1–13
Ringø E, Olsen RE, Mayhew TM, Myklebust R (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227:395–415. 10.1016/j.aquaculture.2003.05.001 DOI: 10.1016/j.aquaculture.2003.05.001
Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801. 10.1111/j.1365-2761.2010.01183.x DOI: 10.1111/j.1365-2761.2010.01183.x
Ronkin D, Seroussi E, Nitzan T, Doron-Faigenboim A, Cnaani A (2015) Intestinal transcriptome analysis revealed differential salinity adaptation between two tilapiine species. Comp Biochem Physiol Part D Genomics Proteomics 13:35–43. 10.1016/j.cbd.2015.01.003 DOI: 10.1016/j.cbd.2015.01.003
Ross DE, Marshall CW, May HD, Norman RS (2016) Comparative genomic analysis of Sulfurospirillum cavolei MES reconstructed from the metagenome of an electrosynthetic microbiome. PLoS ONE 11:e0151214–e0151214. 10.1371/journal.pone.0151214 DOI: 10.1371/journal.pone.0151214
Salyers AA (1984) Bacteroides of the human lower intestinal tract. Annu Rev Microbiol 38:293–313. 10.1146/annurev.mi.38.100184.001453 DOI: 10.1146/annurev.mi.38.100184.001453
Schmidt VT, Smith KF, Melvin DW, Amaral-Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol Ecol 24:2537–2550. 10.1111/mec.13177 DOI: 10.1111/mec.13177
Schmitz M, Douxfils J, Mandiki SNM, Morana C, Baekelandt S, Kestemont P (2016) Chronic hyperosmotic stress interferes with immune homeostasis in striped catfish (Pangasianodon hypophthalmus, S.) and leads to excessive inflammatory response during bacterial infection. Fish Shellfish Immunol 55:550–558. 10.1016/j.fsi.2016.06.031 DOI: 10.1016/j.fsi.2016.06.031
Schmitz M, Mandiki SNM, Douxfils J, Ziv T, Admon A, Kestemont P (2016) Synergic stress in striped catfish (Pangasianodon hypophthalmus, S.) exposed to chronic salinity and bacterial infection: Effects on kidney protein expression profile. J Proteomics 142:91–101. 10.1016/j.jprot.2016.04.046 DOI: 10.1016/j.jprot.2016.04.046
Schmitz M, Baekelandt S, Bequet S, Kestemont P (2017) Chronic hyperosmotic stress inhibits renal Toll-Like Receptors expression in striped catfish (Pangasianodon hypophthalmus, Sauvage) exposed or not to bacterial infection. Dev Comp Immunol 73:139–143. 10.1016/j.dci.2017.03.020 DOI: 10.1016/j.dci.2017.03.020
Schmitz M, Baekelandt S, Tran Thi LK, Mandiki SNM, Douxfils J, Nguyen TQ, Do Thi Thanh H, Kestemont P (2017) Osmoregulatory and immunological status of the pond-raised striped catfish (Pangasianodon hypophthalmus S.) as affected by seasonal runoff and salinity changes in the Mekong Delta. Vietnam Fish Physiol Biochem 43:39–49. 10.1007/s10695-016-0266-7 DOI: 10.1007/s10695-016-0266-7
Schmitz M, Ziv T, Admon A, Baekelandt S, Mandiki SNM, L’Hoir M, Kestemont P (2017) Salinity stress, enhancing basal and induced immune responses in striped catfish Pangasianodon hypophthalmus (Sauvage). J Proteomics 167:12–24. 10.1016/j.jprot.2017.08.005 DOI: 10.1016/j.jprot.2017.08.005
Scott GR, Baker DW, Schulte PM, Wood CM (2008) Physiological and molecular mechanisms of osmoregulatory plasticity in killifish after seawater transfer. J Exp Biol 211:2450–2459. 10.1242/jeb.017947 DOI: 10.1242/jeb.017947
Seck EH, Senghor B, Merhej V, Bachar D, Cadoret F, Robert C, Azhar EI, Yasir M, Bibi F, Jiman-Fatani AA, Konate DS, Musso D, Doumbo O, Sokhna C, Levasseur A, Lagier JC, Khelaifia S, Million M, Raoult D (2019) Salt in stools is associated with obesity, gut halophilic microbiota and Akkermansia muciniphila depletion in humans. Int J Obes 43:862–871. 10.1038/s41366-018-0201-3 DOI: 10.1038/s41366-018-0201-3
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60 DOI: 10.1186/gb-2011-12-6-r60
Sutriana A, Hashim R, Akter MN, Nor SAM (2018) Galactooligosaccharide and a combination of yeast and β-glucan supplements enhance growth and improve intestinal condition in striped catfish Pangasianodon hypophthalmus fed soybean meal diets. Fish Sci 84:523–533. 10.1007/s12562-018-1195-4 DOI: 10.1007/s12562-018-1195-4
Takei Y (2021) The digestive tract as an essential organ for water acquisition in marine teleosts: lessons from euryhaline eels. Zool Lett 7:10. 10.1186/s40851-021-00175-x DOI: 10.1186/s40851-021-00175-x
Takei Y, Hwang P-P (2016) Homeostatic responses to osmotic stress. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish Physiology. Elsevier, pp 207–249
Team RC (2013) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org/
Teschler JK, Cheng AT, Yildiz FH (2017) The two-component signal transduction system VxrAB positively regulates Vibrio cholerae biofilm formation. J Bacteriol 199:e00139-e217 DOI: 10.1128/JB.00139-17
Tine M, Bonhomme F, McKenzie DJ, Durand J-D (2010) Differential expression of the heat shock protein Hsp70 in natural populations of the tilapia, Sarotherodon melanotheron, acclimatised to a range of environmental salinities. BMC Ecol 10:11. 10.1186/1472-6785-10-11 DOI: 10.1186/1472-6785-10-11
Tlaskalova-Hogenova H, Tuckova L, Mestecky J, Kolinska J, Rossmann P, Stepankova R, Kozakova H, Hudcovic T, Hrncir T, Frolova L, Kverka M (2005) Interaction of mucosal microbiota with the innate immune system. Scand J Immunol 62:106–113. 10.1111/j.1365-3083.2005.01618.x DOI: 10.1111/j.1365-3083.2005.01618.x
Tyagi I, Tyagi K, Bhutiani R, Chandra K, Kumar V (2021) Bacterial diversity assessment of world’s largest sewage-fed fish farms with special reference to water quality: a Ramsar site. Environ Sci Pollut Res 28:42372–42386. 10.1007/s11356-021-13756-2 DOI: 10.1007/s11356-021-13756-2
Usher ML, Talbot C, Eddy FB (1990) Effects of transfer to seawater on digestion and gut function in Atlantic salmon smolts (Salmo salar L.). Aquaculture 90:85–96. 10.1016/0044-8486(90)90285-U DOI: 10.1016/0044-8486(90)90285-U
Wexler HM (2007) Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621. 10.1128/CMR.00008-07 DOI: 10.1128/CMR.00008-07
Whittamore JM (2012) Osmoregulation and epithelial water transport: lessons from the intestine of marine teleost fish. J Comp Physiol B 182:1–39. 10.1007/s00360-011-0601-3 DOI: 10.1007/s00360-011-0601-3
Winklhofer KF, Tatzelt J, Haass C (2008) The two faces of protein misfolding: gain- and loss-of-function in neurodegenerative diseases. EMBO J 27:336–349. 10.1038/sj.emboj.7601930 DOI: 10.1038/sj.emboj.7601930
Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21:3100–3102. 10.1111/j.1365-294X.2012.05646.x DOI: 10.1111/j.1365-294X.2012.05646.x
Wu J, Shi Y-H, Zhang X-H, Li C-H, Li M-Y, Chen J (2015) Molecular characterization of an IL-1β gene from the large yellow croaker (Larimichthys crocea) and its effect on fish defense against Vibrio alginolyticus infection. Dong wu xue yan jiu = Zool Res 36:133–141
Xu T, Wu Y, Lin Z, Bertram R, Götz F, Zhang Y, Qu D (2017) Identification of genes controlled by the essential YycFG two-component system reveals a role for biofilm modulation in Staphylococcus epidermidis. Front Microbiol 8:724 DOI: 10.3389/fmicb.2017.00724
Xu Y, Wang N, Tan H-Y, Li S, Zhang C, Feng Y (2020) Function of Akkermansia muciniphila in obesity: interactions with lipid metabolism, immune response and gut systems. Front Microbiol 11:219 DOI: 10.3389/fmicb.2020.00219
Yang W-K, Hseu J-R, Tang C-H, Chung M-J, Wu S-M, Lee T-H (2009) Na+/K+-ATPase expression in gills of the euryhaline sailfin molly, Poecilia latipinna, is altered in response to salinity challenge. J Exp Mar Bio Ecol 375:41–50 DOI: 10.1016/j.jembe.2009.05.004
Yang W-K, Hsu A-D, Kang C-K, Lai IP, Liao P-S, Lee T-H (2018) Intestinal FXYD12 and sodium-potassium ATPase: A comparative study on two euryhaline medakas in response to salinity changes. PLoS One 13:e0201252 DOI: 10.1371/journal.pone.0201252
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. 10.1186/1471-2105-13-134 DOI: 10.1186/1471-2105-13-134
Zhang M, Sun Y, Liu Y, Qiao F, Chen L, Liu W-T, Du Z, Li E (2016) Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture 454:72–80. 10.1016/j.aquaculture.2015.12.014 DOI: 10.1016/j.aquaculture.2015.12.014
Zhang T, Li Q, Cheng L, Buch H, Zhang F (2019) Akkermansia muciniphila is a promising probiotic. Microb Biotechnol 12:1109–1125. 10.1111/1751-7915.13410 DOI: 10.1111/1751-7915.13410
Zhao R, Symonds JE, Walker SP, Steiner K, Carter CG, Bowman JP, Nowak BF (2020) Salinity and fish age affect the gut microbiota of farmed Chinook salmon (Oncorhynchus tshawytscha). Aquaculture 528:735539. 10.1016/j.aquaculture.2020.735539 DOI: 10.1016/j.aquaculture.2020.735539