All Issue

2025 Vol.55, Issue 1 Preview Page

Review Article

Exploring the Bioactive Properties and Potential Probionts in the Fish Mucosa
Francis Harry Shone Villaruel Leonora1
,
Christopher Marlowe Arandela Caipang1*
1Division of Biological Sciences, College of Arts and Sciences, University of the Philippines Visayas, Miagao, Iloilo 5023, Philippines
*cacaipang@up.edu.ph
31 March 2025. pp. 26-41
PDF XML Citation
Abstract

Aquaculture systems face significant economic losses and mass mortality events due to disease outbreaks arising from environmental stressors and pathogenic infections. The fish mucosal immune system plays a crucial role in maintaining host homeostasis and serves as the primary defense barrier against exogenous pathogens. The mucosal interface, characterized by its dynamic interplay with the external environment, harbors a diverse repertoire of bioactive molecules and commensal microbiota that contribute immensely to host immunity. Early studies on mucosal extracts demonstrated broad-spectrum antimicrobial activity against various bacterial and fungal pathogens, including those relevant to both fish and human health. Subsequent studies have explored additional bioactivities, including antibiofilm, antiparasitic, and anticancer properties. Furthermore, novel biomolecules responsible for these bioactivities have been identified within the mucosa, presenting potential applications in the development of new antimicrobials with innovative modes of action against drug-resistant pathogens. Additionally, emerging studies on mucosal probionts have identified promising candidates for aquaculture applications, following in vitro and in vivo characterization. Given the dynamic and crucial relationship between the mucosa and fish health, further research into this critical interface is essential.

Keywords
Aquaculture
Bioactivity
Fish health
Mucus
Probionts
References
1

Mancuso M, Rappazzo AC, Genovese M, El Hady M, Ghonimy A, Ismail M, et al. In vitro selection of bacteria and isolation of probionts from farmed Sparus aurata with potential for use as probiotics. Int J Anim Biol. 2015;1(4):93-98.

2

El-Saadony MT, Alagawany M, Patra AK, Kar I, Tiwari R, Dawood MAO, et al. The functionality of probiotics in aquaculture: an overview. Fish Shellfish Immunol. 2021;117:36-52.

10.1016/j.fsi.2021.07.00734274422
3

Dash S, Das SK, Samal J, Thatoi HN. Epidermal mucus, a major determinant in fish health: a review. Iran J Vet Res. 2018;19(2):72-81.

4

Rizzo C, Gugliandolo C, Giudice AL. Exploring Mediterranean and Arctic environments as a novel source of bacteria producing antibacterial compounds to be applied in aquaculture. Appl Sci. 2020;10(11):4006.

10.3390/app10114006
5

Santajit S, Indrawattana N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. Biomed Res Int. 2016;2475067.

10.1155/2016/247506727274985PMC4871955
6

Venkateswaran P, Vasudevan S, David H, Shaktivel A, Shanmugam K, Neelakantan P, et al. Revisiting ESKAPE pathogens: virulence, resistance, and combating strategies focusing on quorum sensing. Front Cell Infect Microbiol. 2023;13:1159798.

10.3389/fcimb.2023.115979837457962PMC10339816
7

Lazado CC, Caipang CM. Mucosal immunity and probiotics in fish. Fish Shellfish Immunol. 2014;39(1):78-89.

10.1016/j.fsi.2014.04.01524795079
8

Bunnoy A, Na-Nakorn U, Kayansamruaj P, Srisapoome P. Acinetobacter strain KUO11TH, a unique organism related to Acinetobacter pittii and isolated from the skin mucus of healthy bighead catfish and its efficacy against several fish pathogens. Microorganisms. 2073;7(11):549.

10.3390/microorganisms711054931717696PMC6920915
9

Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR. Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance; a review. Front Microbiol. 2019;10:539.

10.3389/fmicb.2019.0053930988669PMC6452778
10

Leonora FHSV, Boonyarat VDS, Pugoy JJ, Chiong AES, Polido MA IV, Caipang CMA. Bacteriophages in the fish mucosa: updates on their biology, interactions, and applications. Biologia. 2024;79(6):1861-1873.

10.1007/s11756-024-01646-0
11

Bragadeeswaran S, Thangaraj S. Hemolytic and antibacterial studies on skin mucus of eel fish, Anguilla anguilla Linnaeus, 1758. Asian J Biol Sci. 2011;4(3):272-276.

10.3923/ajbs.2011.272.276
12

Brinchmann MF. Immune relevant molecules identified in the skin mucus of fish using -omics technologies. Mol Biosyst. 2016;12(7):2056-2063.

10.1039/C5MB00890E27173837
13

Ivanova L, Rangel-Huerta OD, Tartor H, Gjessing MC, Dahle MK, Uhlig S. Fish skin and gill mucus: a source of metabolites for non-invasive health monitoring and research. Metabolites. 2022;12(1):28.

10.3390/metabo1201002835050150PMC8781917
14

Hedmon O, Jacqueline A, Koffi KT, Drago KC, Engeu OP. Fish mucus: a neglected reservoir for antimicrobial peptides. Asian J Pharm Res Dev. 2018;6(4):6-11

10.22270/ajprd.v6i4.389
15

Giacomello E, Marchini D, Rasotto MB. A male sexually dimorphic trait provides antimicrobials to eggs in blenny fish. Biol Lett. 2006;2(3):330-333.

10.1098/rsbl.2006.049217148395PMC1686180
16

Esteban MA. An overview of the immunological defenses in fish skin. ISRN Immunology. 2012;853470.

10.5402/2012/853470
17

Gomez D, Sunyer JO, Salinas I. The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol. 2013;35(6):1729-1739.

10.1016/j.fsi.2013.09.03224099804PMC3963484
18

Tiralongo F, Messina G, Lombardo BM, Longhitano L, Voltt GL, Tibullo D. Skin mucus of marine fish as a source for the development of antimicrobial agents. Front Mar Sci. 2020;7:541853.

10.3389/fmars.2020.541853
19

Larsen A, Tao Z, Bullard SA, Arias CR. Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiol Ecol. 2013;85(3):483-494.

10.1111/1574-6941.1213623607777
20

Carda-Dieguez M, Ghai R, Rodriguez-Valera F, Amaro C. Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution. Microbiome. 2017;5(1):162.

10.1186/s40168-017-0376-129268781PMC5740887
21

Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024-1033.

10.1111/cmi.1230824798552PMC4143175
22

Clinton M, Wyness AJ, Martin SAM, Brierly AS, Ferrier DEK. Sampling the fish gill microbiome: a comparison of tissue biopsies and swabs. BMC Microbiol. 2021;21(1):313.

10.1186/s12866-021-02374-034758745PMC8579561
23

Lowrey L, Woodhams DC, Tacchi L, Salinas I. Topographical mapping of the rainbow trout (Oncorhynchus mykiss) microbiome reveals a diverse bacterial community with antifungal properties in the skin. Appl Environ Microbiol. 2015;81(19):6915-6925.

10.1128/AEM.01826-1526209676PMC4561705
24

Yu YY, Ding LG, Huang ZY, Xu HY. Xu Z. Commensal-bacteria-immunity crosstalk shapes mucosal homeostasis in teleost fish. Rev Aquac. 2021;13(4):2322-2343.

10.1111/raq.12570
25

Santoso HB, Suhartono E, Yunita R, Biyatmoko D. Epidermal mucus as a potential biological matrix for fish health analysis. Egypt J Aquat Biol Fish. 2020;24(6):361-382.

10.21608/ejabf.2020.114402
26

Fernandez-Alacid L, Sanahuja I, Ordonez-Grande B, Sanchez-Nuño S, Viscor G, Gisbert E, et al. Skin mucus metabolites in response to physiological challenges: A valuable non-invasive method to study teleost marine species. Sci Total Environ. 2018;644:1323-1335.

10.1016/j.scitotenv.2018.07.08330743845
27

Azaldin NA, Azmi L, Jamali MAM, Ismail INA. Antimicrobial activity of eel mucus: a review. Malaysian J Sci Health Technol. 2023;9(2):164-173.

10.33102/mjosht.v9i2.363
28

Subramanian S, Ross NW, MacKinnon SL. Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comp Biochem Physiol B Biochem Mol Biol. 2008;150(1):85-92.

10.1016/j.cbpb.2008.01.01118342561
29

Del Rosario M, De la Torre H, Reyes D, Noboa A, Salazar L, Marcillo E, et al. Presence of antimicrobial activity in the mucus of chame fish (Dormitator latifrons). J Pure Appl Microbiol. 2012;6(4):1615-1622.

30

Dhanaraj M, Haniffa MA, Arun Singh SV, Muthu Ramakrishnan C, Manikaandaraja D, James Milton M. Antibacterial activity of skin and intestinal mucus of five different freshwater fish species Viz., Channa striatus, C. micropeltes, C. marulius, C. punctatus, and C. gachua. Malaysian J Sci. 2009;28(3):257-262.

10.22452/mjs.vol28no3.3
31

Kuppulakshmi C, Prakash M, Gunasekaran G, Manimegalai G, Sarojini S. Antibacterial properties of fish mucus from Channa punctatus and Cirrhinus mrigala. Eur Rev Med Pharmacol Sci. 2008;12(3):149-153.

32

Wei OY, Xavier R, Marimuthu K. Screening of antibacterial activity of mucus extract of snakehead fish, Channa striatus (Bloch). Eur Rev Med Pharmacol Sci. 2010;14(8):675-681.

33

Hussain A, Sachan SG. Evaluation of the antimicrobial efficacy of epidermal mucus extract from air-breathing fish (Channa punctatus) and identification of the peptides serving as immune components. Int J Pept Res Ther. 2024;30:4.

10.1007/s10989-023-10581-8
34

Lirio GAC, De Leon JAA, Villafuerte AG. Antimicrobial activity of epidermal mucus from top aquaculture fish species against medically-important pathogens. Walailak J Sci Tech. 2018;16(5):329-340.

10.48048/wjst.2019.6287
35

Pethkar MR, Lookhande MV. Antifungal activity of skin mucus of three cultivable fish species (Catla catla, Cirrhinus mrigala and Anguilla anguilla). Int J Zool Stud. 2017;2(6):1-3.

36

Ikram MNNK, Ridzwan BH. A preliminary screening of antifungal activities from skin mucus extract of Malaysian local swamp eel (Monopterus albus). Int Res J Pharm Pharmacol. 2013;3(1):1-8.

37

Hilles AR, Mahmood S, Hashim R. Evaluation of the antibacterial activity of skin mucus from Asian swamp eel (Monopterus albus). Indian J Geo Mar Sci. 2019;48(12):1855-1859.

38

Ali S, Shah SAUR, Rauf M, Hassan M, Ullah W, Dawar FU. Bactericidal role of epidermal mucus of freshwater fish treated with Aeromonas hydrophila. J Fish Dis. 2023;46(11):1225-1237.

10.1111/jfd.1384137501533
39

Balasubramanian S, Rani BP, Prakash AA, Prakash M, Senthilraja P, Gunasekaran G. Antimicrobial properties of skin mucus from four freshwater cultivable fishes (Catla catla, Hypophthalmichthys molitrix, Labeo rohita and Ctenopharyngodon idella). African J Microbiol Res. 2012;6(24):5110-5120.

40

Sajorne RE, Mabuhay-Omar JA. Antimicrobial property of the epidermal mucus of tilapia Oreochromis spp. Palawan Sci. 2020;12:43-60.

10.69721/TPS.J.2020.12.1.03
41

Hilles AR, Mahmood S, Waly MI, Kaderi MA, Ahmed QU, Azmi SNH, et al. The therapeutic potential of skin mucus from Asian swamp eel (Monopterus albus): In vivo evaluation and histological evidence. J King Saud Univ Sci. 2022;34(4):102011.

10.1016/j.jksus.2022.102011
42

Patel M, Ashraf MS, Siddiqui AJ, Ashraf SA, Sachidanandan M, Snoussi M, et al. Profiling and role of bioactive molecules from Puntius sophore (freshwater/brackish fish) skin mucus with its potent antibacterial, antiadhesion, and antibiofilm activities. Biomolecules. 2020;10(6):920.

10.3390/biom1006092032560562PMC7355610
43

Leng W, Wu X, Xiong Z, Shi T, Sun Q, Yuan L, et al. Study on antibacterial properties of mucus extract of snakehead (Channa argus) against Escherichia coli and its application in chilled fish fillets preservation. LWT. 2022;167(2):113840.

10.1016/j.lwt.2022.113840
44

Wang H, Tang W, Zhang R, Ding S. Analysis of enzyme activity, antibacterial activity, antiparasitic activity and physico-chemical stability of skin mucus derived from Amphiprion clarkii. Fish Shellfish Immunol. 2019;86:653-661.

10.1016/j.fsi.2018.11.06630502467
45

Vennila R, Kumar KR, Kanchana S, Arumugam M, Vijayalakshmi S, Balasubramaniam T. Preliminary investigation on antimicrobial and proteolytic property of the epidermal mucus secretion of marine stingrays. Asian Pac J Trop Biomed. 2011;1(2):S239-243.

10.1016/S2221-1691(11)60162-7
46

Fuochi V, Li Volti G, Camiolo G, Tiralongo F, Giallongo C, Distefano A, et al. Antimicrobial and anti-proliferative effects of skin mucus derived from Dasyatis pastinaca (Linnaeus, 1758). Mar Drugs. 2017;15(11):342.

10.3390/md1511034229104260PMC5706032
47

Stevens JL, Jackson RL, Olson JB. Bacteria associated with lionfish (Pterois volitans/miles complex) enhibit antibacterial activity against known fish pathogens. Mar Ecol Prog Ser. 2016;558:167-180.

10.3354/meps11789
48

Go HJ, Kim CH, Park JB, Kim TY, Lee TK, Oh HY, et al. Biochemical and molecular identification of a novel hepcidin type 2-like antimicrobial peptide in the skin mucus of the pufferfish (Takifugu pardalis). Fish Shellfish Immunol. 2019;93:683-693.

10.1016/j.fsi.2019.08.01731408729
49

Ebran N, Julien S, Orange N, Auperin B, Molle G. Isolation and characterization of novel glycoproteins from fish epidermal mucus: correlation between their pore-forming properties and their antibacterial activities. Biochim Biophys Acta. 2000;1467(2):271-280.

10.1016/S0005-2736(00)00225-X11030587
50

Subramanian S, Ross NW, MacKinnon SL. Myxinidin, a novel antimicrobial peptide from the epidermal mucus of hagfish, Myxine glutinosa L. Mar Biotechnol. 2009;11(6):748-757.

10.1007/s10126-009-9189-y19330556
51

Valero Y, Cortes J, Mercado L. NK-lysin from skin-secreted mucus of Atlantic salmon and its potential role in bacteriostatic activity. Fish Shellfish Immunol. 2019;87:410-413.

10.1016/j.fsi.2019.01.03430703553
52

Liang Y, Guan R, Huang W, Xu T. Isolation and identification of a novel inducible antibacterial peptide from the skin mucus of Japanese eel, Anguilla japonica. Protein J. 2011;30(6):413-421.

10.1007/s10930-011-9346-921796440
53

Abdel-Shafi S, Osman A, Al-Mohammadi AR, Enan G, Kamal N, Sitohy M. Biochemical, biological characteristics and antibacterial activity of glycoprotein extracted from the epidermal mucus of African catfish (Clarias gariepinus). Int J Biol Macromol. 2019;138:773-780.

10.1016/j.ijbiomac.2019.07.15031351952
54

Li T, Liu Q, Wang D, Li J. Characterization and antimicrobial mechanism of CF-14, a new antimicrobial peptide from the epidermal mucus of catfish. Fish Shellfish Immunol. 2019;92:881-888.

10.1016/j.fsi.2019.07.01531291603
55

Najm AAK, Azfaralariff A, Dyari HRE, Othman BA, Shahid M, Khalili N, et al. Anti-breast cancer synthetic pepitdes derived from the Anabaas testudineus skin mucus fractions. Sci Rep. 2021;11(1):23182.

10.1038/s41598-021-02007-634848729PMC8632885
56

Law D, Abdulkareem Najm A, Chong JX, K'ng JZY, Amran M, Ching HL, et al. In silico identification and in vitro assessment of a potential anti-breast cancer activity of antimicrobial peptide retrieved from the ATMP1 Anabas testudineus fish peptide. Peer J. 2023;11:e15651.

10.7717/peerj.1565137483971PMC10362845
57

Diaz-Puertas R, Adamek M, Mallavia R, Falco A. Fish skin mucus extracts: an underexplored source of antimicrobial agents. Mar Drugs. 2023;21(6):350.

10.3390/md2106035037367675PMC10303038
58

Chiarello M, Villager S, Bouvier C, Bettarel Y, Bouvier T. High diversity of skin-associated bacterial communities of marine fishes is promoted by their high variability among body parts, individuals and species. FEMS Microbiol Ecol. 2015;91(7):fiv061.

10.1093/femsec/fiv06126048284
59

Tarnecki AM, Burgos FA, Ray CL, Arias CR. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J Appl Microbiol. 2017;123(1):2-17.

10.1111/jam.1341528176435
60

Minniti G, Hagen LH, Porcellato D, Jorgensen SM, Pope PB, Vaaje-Kolstad G. The skin-mucus microbial community of farmed Atlantic salmon (Salmo salar). Front Microbiol. 2017;8:2043.

10.3389/fmicb.2017.0204329104567PMC5655796
61

Nayak SK. Probiotics and immunity: a fish perspective. Fish Shellfish Immunol. 2010;29(1):2-14.

10.1016/j.fsi.2010.02.01720219683
62

Tapia-Paniagua ST, Ceballos-Francisco D, Belebona MC, Esteban MA, Moriñigo MA. Mucus glycosylation, immunity and bacterial microbiota associated to the skin of experimentally ulcered gilthead seabream (Sparus aurata). Fish Shellfish Immunol. 2018;75:381-390.

10.1016/j.fsi.2018.02.00629421587
63

Zhao Q, Maynard CL. Mucus, commensals, and the immune system. Gut Microbes. 2022;14(1):2041342.

10.1080/19490976.2022.204134235239459PMC8903774
64

Paone P, Cani PD. Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut. 2020;69(12):2232-2243.

10.1136/gutjnl-2020-32226032917747PMC7677487
65

Slack E, Balmer ML, Fritz JH, Hapfelmeier S. Functional flexibility of intestinal IgA-broadening the fine line. Front Immunol. 2012;3:100.

10.3389/fimmu.2012.0010022563329PMC3342566
66

Yang Y, Palm NW. Immunoglobulin A and the microbiome. Curr Opin Microbiol. 2020;56:89-96.

10.1016/j.mib.2020.08.00332889295
67

Vine NG, Leukes WD, Kaiser H, Daya S, Baxter J, Hecht T. Competition for attachment of aquaculture candidate probiotic and pathogenic bacteria on fish intestinal mucus. J Fish Dis. 2004;27(6):319-326.

10.1111/j.1365-2761.2004.00542.x15189372
68

Chabrillon M, Arijo S, Diaz-Rosales P, Balebona MC, Moriñigo MA. Interference of Listonella anguillarum with potential probiotic microorganisms isolated from farmed gilthead seabream (Sparus aurata, L.). Aquac Res. 2006;37(1):78-86.

10.1111/j.1365-2109.2005.01400.x
69

Grześkowiak L, Collado MC, Vesterlund S, Mazurkiewicz J, Salminen S. Adhesion abilities of commensal fish bacteria by use of mucus model system: quantitative analysis. Aquaculture. 2011;318(1-2):33-36.

10.1016/j.aquaculture.2011.04.037
70

Lazado CC, Caipang CM, Brinchmann MF, Kiron V. In vitro adherence of two candidate probiotics from Atlantic cod and their interference with the adhesion of two pathogenic bacteria. Vet Microbiol. 2011;148(2-4):252-259.

10.1016/j.vetmic.2010.08.02420884135
71

Thelma J, Asha Devi NK. Evaluation of probiotics from mucus associated epibiotic bacteria on marine fishes. J Mar Biol Oceanogr. 2016;5(3).

72

Ritchie KB, Schwarz M, Mueller J, Lapacek VA, Merselis D, Walsh CJ, et al. Survey of antibiotic-producing bacteria associated with the epidermal mucus layers of rays and skates. Front Microbiol. 2017;8:1050.

10.3389/fmicb.2017.0105028725216PMC5496964
73

Medina M, Sotil G, Flores V, Fernandez C, Sandoval N. In vitro assessment of some proviotic properties and inhibitory activity against Yersinia ruckeri of bacteria isolated from rainbow trout Oncorhynchus mykiss (Walbaum). Aquaculture Reports. 2020;18:100447.

10.1016/j.aqrep.2020.100447
74

Bhatnagar A, Rathi P. Isolation and characterization of autochthonous probiotics from skin mucus and their in vivo validation with dietary probiotic bacteria on growth performance and immunity of Labeo calbasu. Fish Physiol Biochem. 2023;49(2):191-208.

10.1007/s10695-022-01168-z36622624
75

Das A, Nakhro K, Chowdhury S, Kamilya D. Effects of potential probiotic Bacillus amyloliquifaciens FPTB16 on systemic and cutaneous mucosal immune responses and disease resistance of catla (Catla catla). Fish Shellfish Immunol. 2013;35(5):1547-1553.

10.1016/j.fsi.2013.08.02224012512
76

Geraylou Z, Vanhove MPM, Souffreau C, Rurangwa E, Buyse J, Ollevier F. In vitro selection and characterization of putative probiotics isolated from the gut of Acipenser baerii (Brandt, 1869). Aquaculture Res. 2014;45(2):341-352.

10.1111/j.1365-2109.2012.03232.x
77

Midhun SJ, Neethu S, Vysakh A, Sunil MA, Radhakrishnan EK, Jyothis M. Antibacterial activity of autochthonous bacteria isolated from Anabas testudineus (Bloch, 1792) and its in vitro probiotic characterization. Microb Pathog. 2017;113:312-320.

10.1016/j.micpath.2017.10.05829102685
78

Melo-Bolivar JF, Ruiz Pardo RY, Junca H, Sidjabat HE, Cano-Lozano JA, Villamil Diaz LM. Competitive exclusion bacterial culture derived from the gut microbiome of Nile tilapia (Oreochromis niloticus) as a resource to efficiently recover probiotic strains: taxonomic, genomic, and functional proof of concept. Microorganisms. 2022;10(7):1376.

10.3390/microorganisms1007137635889095PMC9321352
79

Reverter M, Sasal P, Tapissier-Bontemps N, Lecchini D, Suzuki M. Characterisation of gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems. FEMS Microbiol Ecol. 2017;93(6).

10.1093/femsec/fix05128431143
80

Birlanga VB, McCormack G, Ijaz UZ, MacCarthy E, Smith C, Collins G. Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon. Sci Rep. 2022;12(1):16719.

10.1038/s41598-022-17008-236202859PMC9537138
Information
  • Publisher :The Korean Society for Microbiology and The Korean Society of Virology
  • Publisher(Ko) :대한미생물학회‧대한바이러스학회
  • Journal Title :JOURNAL OF BACTERIOLOGY AND VIROLOGY
  • Volume : 55
  • No :1
  • Pages :26-41
  • Received Date : 2024-11-09
  • Revised Date : 2024-12-26
  • Accepted Date : 2025-01-21
  • DOI :https://doi.org/10.4167/jbv.2025.55.1.026
Journal Informaiton JOURNAL OF BACTERIOLOGY AND VIROLOGY JOURNAL OF BACTERIOLOGY AND VIROLOGY
  • NRF
  • 임플란트학회 전용 배너
  • KOFST
  • crossref crossmark
  • crossref cited-by
  • crossref funder-registry
  • crosscheck
  • orcid
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close