Ocular mucosal homeostasis of teleost fish provides insight into the coevolution between microbiome and mucosal immunity.
Evolution
IHNV infection
Mucosal immunity
Ocular microbiota
Rainbow trout
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
13 Jan 2024
13 Jan 2024
Historique:
received:
25
08
2023
accepted:
07
11
2023
medline:
14
1
2024
pubmed:
14
1
2024
entrez:
13
1
2024
Statut:
epublish
Résumé
The visual organ plays a crucial role in sensing environmental information. However, its mucosal surfaces are constantly exposed to selective pressures from aquatic or airborne pathogens and microbial communities. Although few studies have characterized the conjunctival-associated lymphoid tissue (CALT) in the ocular mucosa (OM) of birds and mammals, little is known regarding the evolutionary origins and functions of immune defense and microbiota homeostasis of the OM in the early vertebrates. Our study characterized the structure of the OM microbial ecosystem in rainbow trout (Oncorhynchus mykiss) and confirmed for the first time the presence of a diffuse mucosal-associated lymphoid tissue (MALT) in fish OM. Moreover, the microbial communities residing on the ocular mucosal surface contribute to shaping its immune environment. Interestingly, following IHNV infection, we observed robust immune responses, significant tissue damage, and microbial dysbiosis in the trout OM, particularly in the fornix conjunctiva (FC), which is characterized by the increase of pathobionts and a reduction of beneficial taxa in the relative abundance in OM. Critically, we identified a significant correlation between viral-induced immune responses and microbiome homeostasis in the OM, underscoring its key role in mucosal immunity and microbiota homeostasis. Our findings suggest that immune defense and microbiota homeostasis in OM occurred concurrently in early vertebrate species, shedding light on the coevolution between microbiota and mucosal immunity. Video Abstract.
Sections du résumé
BACKGROUND
BACKGROUND
The visual organ plays a crucial role in sensing environmental information. However, its mucosal surfaces are constantly exposed to selective pressures from aquatic or airborne pathogens and microbial communities. Although few studies have characterized the conjunctival-associated lymphoid tissue (CALT) in the ocular mucosa (OM) of birds and mammals, little is known regarding the evolutionary origins and functions of immune defense and microbiota homeostasis of the OM in the early vertebrates.
RESULTS
RESULTS
Our study characterized the structure of the OM microbial ecosystem in rainbow trout (Oncorhynchus mykiss) and confirmed for the first time the presence of a diffuse mucosal-associated lymphoid tissue (MALT) in fish OM. Moreover, the microbial communities residing on the ocular mucosal surface contribute to shaping its immune environment. Interestingly, following IHNV infection, we observed robust immune responses, significant tissue damage, and microbial dysbiosis in the trout OM, particularly in the fornix conjunctiva (FC), which is characterized by the increase of pathobionts and a reduction of beneficial taxa in the relative abundance in OM. Critically, we identified a significant correlation between viral-induced immune responses and microbiome homeostasis in the OM, underscoring its key role in mucosal immunity and microbiota homeostasis.
CONCLUSIONS
CONCLUSIONS
Our findings suggest that immune defense and microbiota homeostasis in OM occurred concurrently in early vertebrate species, shedding light on the coevolution between microbiota and mucosal immunity. Video Abstract.
Identifiants
pubmed: 38218870
doi: 10.1186/s40168-023-01716-6
pii: 10.1186/s40168-023-01716-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
10Subventions
Organisme : National Natural Science Foundation of China
ID : 32225050, 32073001
Informations de copyright
© 2024. The Author(s).
Références
Bergman J. Evolution fails to explain the vertebrate camera-type eye. A R J. 2022;15:277–83.
Young GC. Early evolution of the vertebrate eye—fossil evidence. Evo Edu Outreach. 2008;1:427–38.
doi: 10.1007/s12052-008-0087-y
Lamb TD, Collin SP, Pugh EN Jr. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci. 2007;8:960–76.
pubmed: 18026166
pmcid: 3143066
doi: 10.1038/nrn2283
Lamb TD, Pugh EN, Collin SP. The origin of the vertebrate eye. Evo Edu Outreach. 2008;1:415–26.
doi: 10.1007/s12052-008-0091-2
Suzuki DG, Grillner S. The stepwise development of the lamprey visual system and its evolutionary implications. Biol Rev Camb Philos Soc. 2018;93:1461–77.
pubmed: 29488315
doi: 10.1111/brv.12403
Collin SP. Scene through the eyes of an apex predator: a comparative analysis of the shark visual system. Clin Exp Optom. 2018;101:624–40.
pubmed: 30066959
doi: 10.1111/cxo.12823
Maddalena AD, Bänsch H, Heim W. Sharks of the Mediterranean: an illustrated study of all species. Jefferson: McFarland; 2015.
Mitchell MA, Tully TN. Current therapy in exotic pet practice. St. Louis, Missouri: Elsevier; 2016.
Mohun SM, Davies WIL. The evolution of amphibian photoreception. Front Ecol Evol. 2019;7:321.
doi: 10.3389/fevo.2019.00321
Guerra-Fuentes RA, Roscito JG, Nunes PM, Oliveira-Bastos PR, Antoniazzi MM, Carlos J, et al. Through the looking glass: the spectacle in gymnophthalmid lizards. Anat Rec (Hoboken). 2014;297:496–504.
pubmed: 24482378
doi: 10.1002/ar.22861
Watanabe T, Takahashi N, Minaguchi J, Mochizuki A, Hiramatsu K. Three-dimensional analysis of the nasolacrimal duct and nasal cavity and arrangement of mucosal tissue in chickens. J Poult Sci. 2020;57:303–9.
pubmed: 33132731
pmcid: 7596029
doi: 10.2141/jpsa.0190091
Tawfik HA, Abdulhafez MH, Fouad YA, Dutton JJ. Embryologic and fetal development of the human eyelid. Ophthalmic Plast Reconstr Surg. 2016;32:407–14.
pubmed: 27124372
pmcid: 5102278
doi: 10.1097/IOP.0000000000000702
Dutton JJ, Tawfik HA, Proia AD. Comprehensive textbook of eyelid disorders and diseases. Philadelphia: Wolters Kluwer; 2022.
Knop E, Knop N. Anatomy and immunology of the ocular surface. Chem Immunol Allergy. 2007;92:36–49.
pubmed: 17264481
doi: 10.1159/000099252
Edirisinghe SL, Nikapitiya C, Dananjaya SHS, Park J, Kim D, Choi D, et al. Effect of Polydeoxyribonucleotide (PDRN) Treatment on Corneal Wound Healing in Zebrafish (Danio rerio). Int J Mol Sci. 2022;23:13525.
pubmed: 36362312
pmcid: 9659220
doi: 10.3390/ijms232113525
Sridhar MS. Anatomy of cornea and ocular surface. Indian J Ophthalmol. 2018;66:190–4.
pubmed: 29380756
pmcid: 5819093
doi: 10.4103/ijo.IJO_646_17
O’Sullivan NL, Montgomery PC. Ocular mucosal immunity. Mucosal Immunol. 2015;2015:1873–97.
Liu J, Li ZJ. Resident innate immune cells in the cornea. Front Immunol. 2021;12: 620284.
pubmed: 33717118
pmcid: 7953153
doi: 10.3389/fimmu.2021.620284
Knop E, Knop N. The role of eye-associated lymphoid tissue in corneal immune protection. J Anat. 2005;206:271–85.
pubmed: 15733300
pmcid: 1571473
doi: 10.1111/j.1469-7580.2005.00394.x
van Ginkel FW, Gulley SL, Lammers A, Hoerr FJ, Gurjar R, Toro H. Conjunctiva-associated lymphoid tissue in avian mucosal immunity. Dev Comp Immunol. 2012;36:289–97.
pubmed: 21641931
doi: 10.1016/j.dci.2011.04.012
Sprouse ML, Bates NA, Felix KM, Wu HJ. Impact of gut microbiota on gut-distal autoimmunity: a focus on T cells. Immunology. 2019;15:305–18.
doi: 10.1111/imm.13037
Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3:4–14.
pubmed: 22356853
pmcid: 3337124
doi: 10.4161/gmic.19320
Willcox MD. Characterization of the normal microbiota of the ocular surface. Exp Eye Res. 2013;117:99–105.
pubmed: 23797046
doi: 10.1016/j.exer.2013.06.003
Aragona P, Baudouin C, del Castillo JMB, Messmer E, Barabino S, Merayo-Lloves J, et al. The ocular microbiome and microbiota and their effects on ocular surface pathophysiology and disorders. Surv Ophthalmol. 2021;66:907–25.
pubmed: 33819460
doi: 10.1016/j.survophthal.2021.03.010
de Paiva CS, St Leger AJ, Caspi RR. Mucosal immunology of the ocular surface. Mucosal Immunol. 2022;15:1143–57.
pubmed: 36002743
pmcid: 9400566
doi: 10.1038/s41385-022-00551-6
Zhang Y-A, Salinas I, Li J, Parra D, Bjork S, Xu Z, et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol. 2010;11:827–35.
pubmed: 20676094
pmcid: 3459821
doi: 10.1038/ni.1913
Xu Z, Parra D, Gomez D, Salinas I, Zhang YA, von Gersdorff JL, et al. Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proc Natl Acad Sci U S A. 2013;110:13097–102.
pubmed: 23884653
pmcid: 3740891
doi: 10.1073/pnas.1304319110
Xu Z, Takizawa F, Parra D, Gomez D, von Gersdorff JL, LaPatra SE, et al. Mucosal immunoglobulins at respiratory surfaces mark an ancient association that predates the emergence of tetrapods. Nat Commun. 2016;7:10728.
pubmed: 26869478
pmcid: 4754351
doi: 10.1038/ncomms10728
Kong WG, Yu YY, Dong S, Huang ZY, Ding LG, Cao JF, et al. Pharyngeal immunity in early vertebrates provides functional and evolutionary insight into mucosal homeostasis. J Immunol. 2019;203:3054–67.
pubmed: 31645417
pmcid: 6859377
doi: 10.4049/jimmunol.1900863
Hooper LV, Littman DR, Macpherson AJ. Interactions Between the Microbiota and the Immune System. Science. 2012;336:1268–73.
pubmed: 22674334
pmcid: 4420145
doi: 10.1126/science.1223490
Richardson R, Tracey-White D, Webster A, Moosajee M. The zebrafish eye-a paradigm for investigating human ocular genetics. Eye (Lond). 2017;31:68–86.
pubmed: 27612182
doi: 10.1038/eye.2016.198
Yu YY, Ding LG, Huang ZY, Xu HY, Xu Z. Commensal bacteria-immunity crosstalk shapes mucosal homeostasis in teleost fish. Rev Aquac. 2021;13:2322–43.
doi: 10.1111/raq.12570
Human Microbiome Project Consortium Structure. Function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.
doi: 10.1038/nature11234
Salinas I. The mucosal immune system of teleost fish. Biology (Basel). 2015;4:525–39.
pubmed: 26274978
Stefan KL, Kim MV, Iwasaki A. Commensal microbiota modulation of natural resistance to virus infection. Cell. 2020;183:1312–24.
pubmed: 33212011
pmcid: 7799371
doi: 10.1016/j.cell.2020.10.047
Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol. 2011;9:233–43.
pubmed: 21358670
doi: 10.1038/nrmicro2536
Lee HJ, Yoon CH, Kim HJ, Ko JH, Ryu JS, Jo DH, et al. Ocular microbiota promotes pathological angiogenesis and inflammation in sterile injury-driven corneal neovascularization. Mucosal Immunol. 2022;15:1350–62.
pubmed: 35986099
doi: 10.1038/s41385-022-00555-2
Dixon P, Paley R, Alegria-Moran R, Oidtmann B. Epidemiological characteristics of infectious hematopoietic necrosis virus (IHNV): a review. Vet Res. 2016;47:63.
pubmed: 27287024
pmcid: 4902920
doi: 10.1186/s13567-016-0341-1
Maurin C, He Z, Mentek M, Verhoeven P, Pillet S, Bourlet T, et al. Exploration of the ocular surface infection by SARS-CoV-2 and implications for corneal donation: An ex vivo study. PLoS Med. 2022;19: e1003922.
pubmed: 35231027
pmcid: 8887728
doi: 10.1371/journal.pmed.1003922
Broquet AH, Hirata Y, McAllister CS, Kagnoff MF. RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. J Immunol. 2011;186:1618–26.
pubmed: 21187438
doi: 10.4049/jimmunol.1002862
Tengroth L, Millrud CR, Kvarnhammar AM, Kumlien Georen S, Latif L, Cardell LO. Functional effects of Toll-like receptor (TLR)3, 7, 9, RIG-I and MDA-5 stimulation in nasal epithelial cells. PLoS ONE. 2014;9: e98239.
pubmed: 24886842
pmcid: 4041746
doi: 10.1371/journal.pone.0098239
Bielory L. Allergic and immunologic disorders of the eye. Part I: immunology of the eye. J Allergy Clin Immunol. 2000;106:805–816.
Cano-Suarez MT, Reinoso R, Martin MC, Calonge M, Vallelado AI, Fernandez I, et al. Epithelial component and intraepithelial lymphocytes of conjunctiva- associated lymphoid tissue in healthy children. Histol Histopathol. 2021;36:1273–83.
pubmed: 34698365
Segal KL, Lai EC, Starr CE. Management of acute conjunctivitis. Curr Ophthalmol Rep. 2014;2:116–23.
doi: 10.1007/s40135-014-0046-4
Liu Q, Xu ZY, Wang XL, Huang XM, Zheng WL, Li MJ, et al. Changes in conjunctival microbiota associated with HIV infection and antiretroviral therapy. Invest Ophth Vis Sci. 2021;62:1.
doi: 10.1167/iovs.62.12.1
Zouiouich S, Loftfield E, Huybrechts I, Viallon V, Louca P, Vogtmann E, et al. Markers of metabolic health and gut microbiome diversity: findings from two population-based cohort studies. Diabetologia. 2021;64:1749–59.
pubmed: 34110438
pmcid: 8245388
doi: 10.1007/s00125-021-05464-w
Menni C, Zhu J, Le Roy CI, Mompeo O, Young K, Rebholz CM, et al. Serum metabolites reflecting gut microbiome alpha diversity predict type 2 diabetes. Gut Microbes. 2020;11:1632–42.
pubmed: 32576065
pmcid: 7524143
doi: 10.1080/19490976.2020.1778261
Conradie TA, Jacobs K. Distribution patterns of Acidobacteriota in different fynbos soils. PLoS ONE. 2021;16: e0248913.
pubmed: 33750980
pmcid: 7984625
doi: 10.1371/journal.pone.0248913
Feng C, Jia J, Wang C, Han M, Dong C, Huo B, et al. Phytoplankton and bacterial community structure in two Chinese lakes of different trophic status. Microorganisms. 2019;7:621.
pubmed: 31783682
pmcid: 6956004
doi: 10.3390/microorganisms7120621
Varshney A, Das M, Chaudhary P, Kumari R, Yadav K. Aeromonas Salmonicida as a causative agent for postoperative endophthalmitis. Middle East Afr J Ophthalmol. 2017;24:213–5.
pubmed: 29422757
pmcid: 5793454
doi: 10.4103/meajo.MEAJO_238_17
Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int. 2017;2017:9351507.
pubmed: 29230419
pmcid: 5688358
doi: 10.1155/2017/9351507
Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33:496–503.
pubmed: 26210164
doi: 10.1016/j.tibtech.2015.06.011
Stojanov S, Berlec A, Strukelj B. The influence of probiotics on the firmicutes/bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms. 2020;8:1715.
pubmed: 33139627
pmcid: 7692443
doi: 10.3390/microorganisms8111715
McDermott AM. Antimicrobial compounds in tears. Exp Eye Res. 2013;117:53–61.
pubmed: 23880529
doi: 10.1016/j.exer.2013.07.014
Hanada S, Pirzadeh M, Carver KY, Deng JC. Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. Front Immunol. 2018;9:2640.
pubmed: 30505304
pmcid: 6250824
doi: 10.3389/fimmu.2018.02640
Ranjith K, Sharma S, Shivaji S. Microbes of the human eye: Microbiome, antimicrobial resistance and biofilm formation. Exp Eye Res. 2021;205: 108476.
pubmed: 33549582
doi: 10.1016/j.exer.2021.108476
Shivaji S, Jayasudha R, Chakravarthy SK, SaiAbhilash CR, Sai Prashanthi G, Sharma S, et al. Alterations in the conjunctival surface bacterial microbiome in bacterial keratitis patients. Exp Eye Res. 2021;203: 108418.
pubmed: 33359511
doi: 10.1016/j.exer.2020.108418
Chopra AK, Xu XJ, Ribardo D, Gonzalez M, Kuhl K, Peterson JW, et al. The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect Immun. 2000;68:2808–18.
pubmed: 10768977
pmcid: 97492
doi: 10.1128/IAI.68.5.2808-2818.2000
Zhang W, Li ZX, Yang HT, Wang GL, Liu G, Wang Y, et al. Aeromonas sobria induces proinflammatory cytokines production in mouse macrophages via activating NLRP3 inflammasome signaling pathways. Front Cell Infect. 2021;11: 691445.
doi: 10.3389/fcimb.2021.691445
Salavert M, Bretón JR, Gutiérrez I, Gobernado M. Infección ocular por Aeromonas spp.: consideraciones sobre su tratamiento e importancia de las resistencias a antimicrobianos [Ocular infection caused by Aeromonas spp.: considerations on its treatment and importance of resistance to antimicrobial agents]. Enferm Infecc Microbiol Clin. 1998;16:208–9.
pubmed: 9646574
Couturier A, Chidiac C, Truy E, Ferry T; Lyon BJI Study Group. Ethmoiditis with subperiosteal and retro-ocular abscesses due to Aeromonas sobria in a 16-year-old boy exposed to the Ardèche river. BMJ Case Rep. 2017;2017:bcr2017219505.
Han C, Huang W, Peng S. Characterization and expression analysis of the interferon regulatory factor (IRF) gene family in zig-zag eel (Mastacembelus armatus) against Aeromonas veronii infection. Dev Comp Immunol. 2023;140:104622.
pubmed: 36543267
doi: 10.1016/j.dci.2022.104622
Feng J, Guo S, Lin P. Identification of a retinoic acid-inducible gene I from Japanese eel (Anguilla japonica) and expression analysis in vivo and in vitro. Fish Shellfish Immunol. 2016;55:249–56.
pubmed: 27238428
doi: 10.1016/j.fsi.2016.05.036
Zhu YY, Xing WX, Shan SJ, Zhang SQ, Li YQ, Li T, An L, Yang GW. Characterization and immune response expression of the Rig-I-like receptor mda5 in common carp (Cyprinus carpio). J Fish Biol. 2016;88:2188–202.
pubmed: 27108774
doi: 10.1111/jfb.12981
Perin AF, Goyal S, Rosenbaum ER, Uwaydat SH. Lysinibacillus spp. Endophthalmitis: a first reported case. Ann Clin Lab Sci. 2015;45:607–608.
Morioka H, Oka K, Yamada Y, Nakane Y, Komiya H, Murase C, et al. Lysinibacillus fusiformis bacteremia: Case report and literature review. J Infect Chemother. 2022;28:315–8.
pubmed: 34865964
doi: 10.1016/j.jiac.2021.10.030
Wang J, Fan YH, Yao ZG. Isolation of a Lysinibacillus fusiformis strain with tetrodotoxin-producing ability from puffer fish Fugu obscurus and the characterization of this strain. Toxicon. 2010;56:640–3.
pubmed: 20576513
doi: 10.1016/j.toxicon.2010.05.011
Luerce TD, Gomes-Santos AC, Rocha CS, Moreira TG, Cruz DN, Lemos L, et al. Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis. Gut Pathog. 2014;6:33.
pubmed: 25110521
pmcid: 4126083
doi: 10.1186/1757-4749-6-33
Chiang MC, Chern E. Ocular surface microbiota: ophthalmic infectious disease and probiotics. Front Microbiol. 2022;13: 952473.
pubmed: 36060740
pmcid: 9437450
doi: 10.3389/fmicb.2022.952473
Petrillo F, Pignataro D, Lavano MA, Santella B, Folliero V, Zannella C, et al. Current evidence on the ocular surface microbiota and related diseases. Microorganisms. 2020;8:1033.
pubmed: 32668575
pmcid: 7409318
doi: 10.3390/microorganisms8071033
Yu Y, Huang Z, Kong W, Dong F, Zhang X, Zhai X, et al. Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses. Cell Discovery. 2022;8:31.
pubmed: 35379790
pmcid: 8979957
doi: 10.1038/s41421-022-00393-3
Garcia B, Dong F, Casadei E, Rességuier J, Ma J, Cain KD, et al. A novel organized nasopharynx-associated lymphoid tissue in teleosts that expresses molecular markers characteristic of mammalian germinal centers. J Immunol. 2022;209:2215–26.
pubmed: 36426979
doi: 10.4049/jimmunol.2200396
Liang X, Wang F, Li K, Nie X, Fang H. Effects of norfloxacin nicotinate on the early life stage of zebrafish (Danio rerio): Developmental toxicity, oxidative stress and immunotoxicity. Fish Shellfish Immunol. 2020;96:262–9.
pubmed: 31816414
doi: 10.1016/j.fsi.2019.12.008
Xu Z, Takizawa F, Casadei E, Shibasaki Y, Ding Y, Sauters TJ, et al. Specialization of mucosal immunoglobulins in pathogen control and microbiota homeostasis occurred early in vertebrate evolution. Sci Immunol. 2020;5:eaay3254.
Liu C, Zhao D, Ma W, Guo Y, Wang A, Wang Q, et al. Denitrifying sulfide removal process on high-salinity wastewaters in the presence of Halomonas sp. Appl Microbiol Biotechnol. 2016;100:1421–6.
pubmed: 26454867
doi: 10.1007/s00253-015-7039-6
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Callahan B, McMurdie P, Rosen M, Han A, Johnson A, Dada SH. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Kõljalg U, Nilsson R, Abarenkov K, Tedersoo L, Taylor A, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Towards a unified paradigm for sequence‐based identification of fungi. Mol Ecol. 2013;22:5271–5277.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:1–18.
doi: 10.1186/gb-2011-12-6-r60