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Sains Malaysiana 51(8)(2022): 2339-2349
http://doi.org/10.17576/jsm-2022-5108-01
Transient or Permanent Inhabitants: Cultured Internal Microbiota of Cichlidogyrus thurstonaeand Scutogyrus longicornis (Monogenea: Ancyrocephalidae) from Oreochromis sp.
(Penghuni Sementara atau Kekal: Mikrobiota Dalaman Biakan Cichlidogyrus thurstonae dan Scutogyrus longicornis (Monogenea: Ancyrocephalidae) daripada Oreochromis sp.)
ZHI-ZHANG
ONG1, YEAK-HENG CHONG1 & WEY-LIM WONG1,2,*
1Department of Biological Science, Faculty of
Science, Universiti Tunku Abdul Rahman, Jalan Universiti,
Bandar Barat, 31900 Kampar, Perak Darul Ridzuan, Malaysia
2Centre for Agriculture and Food Research, Universiti Tunku Abdul Rahman, Jalan Universiti, Bandar Barat, 31900
Kampar, Perak Darul Ridzuan,
Malaysia
Diserahkan: 4 Ogos 2021/ Diterima: 15 Februari 2022
Abstract
Monogeneans,
a class of parasitic platyhelminthes, are usually found on the surface of fish.
When it feeds on its host, it harbours bacteria,
which can survive in its gut. Occasionally, the monogeneans may cause damages
on fish tissue while feeding and may allow secondary infection. The present
study aimed to isolate and identify culturable bacteria obtained within the gill monogeneans, Cichlidogyrus thurstonaeand Scutogyrus longicornis, and gill surface of the
tilapia fish, Oreochromis sp. based on 16S ribosomal RNA gene
sequencing. Monogeneans were isolated from the fish gill filaments and surface
disinfected using 70% ethanol before squashed aseptically on Luria Bertani (LB) agar to isolate the internal microbiota. A
total of five bacteria species, namely Burkholderia sp., Enterobacter hormaechei, Enterobacter sp., Ochrobactrum intermedium and Pantoea sp., were found within C. thurstonae, whilst a total of eight bacteria
species, namely Burkholderia contaminans, Pantoea dispersa, Sphingomonas yabuuchiae, Rhizobium pusense, O. intermedium, Acinetobacter bereziniae, Escherichia hermannii, and Staphylococcus saprophyticus,
were found within S. longicornis in which B. contaminans, P. dispersa, and S. yabuuchiaewere
also found on the surface of the tilapia fish gill filaments. Enterobacter bugandensisand Acinetobacter pittiiwere found solely on the surface of the
gill filaments. These bacteria are also found in the
environment and some of them are believed to be pathogenic to fish. We suggest that
monogeneans may serve as potential bacteria reservoirs, which facilitate the
transmission of bacteria.
Keywords: Bacteria; identification; internal microbiota; molecular; monogenean; tilapia
Abstrak
Monogenea ialah salah satu kelas parasit platyhelminthes yang sering ditemui pada permukaan badan ikan. Apabila monogenea memakan tisu hos ikan, ia memperoleh bakteria
yang dapat hidup di dalam usus monogenea. Kadangkala, monogenea boleh menyebabkan kecederaan pada tisu ikan semasa makan yang mungkin menyebabkan jangkitan
sekunder pada ikan. Kajian ini bertujuan memencilkan dan mengenal pasti bakteria yang boleh dikultur daripada monogenea, Cichlidogyrus thurstonae dan Scutogyrus
longicornis serta pada permukaan insang ikan tilapia, Oreochromis sp. berdasarkan jujukan gen 16S ribosomal RNA. Monogenea dipencilkan daripada filamen insang ikan
dan permukaan dibilas dengan 70% etanol sebelum dilenyek secara aseptik pada agar LB untuk pemencilan mikrobiota dalaman. Sebanyak lima spesies bakteria, iaitu Burkholderia sp., Enterobacter hormaechei, Enterobacter sp., Ochrobactrum intermedium dan Pantoea sp., dijumpai di dalam C. thurstonae manakala sejumlah lapan
spesies bakteria, iaitu Burkholderia contaminans, Pantoea dispersa, Sphingomonas yabuuchiae, Rhizobium pusense, O. intermedium, Acinetobacter bereziniae, Escherichia hermannii dan Staphylococcus saprophyticus dijumpai pada S. longicornis dengan B. contaminans, P. dispersadan S. yabuuchiaejuga dijumpai
pada permukaan filamen insang ikan. Walau bagaimanapun, Enterobacter bugandensisdan Acinetobacter pittiihanya dijumpai pada permukaan filamen insang
sahaja. Bakteria ini juga boleh didapati daripada persekitaran dan sebahagian daripada bakteria ini dipercayai bersifat patogen kepada ikan. Kami mendapati
monogenea berkemungkinan berfungsi sebagai perumah yang memudahkan penularan bakteria.
Kata kunci: Bakteria; mikrobiota dalaman; molekul; monogenea; pengenalpastian; tilapia
RUJUKAN
Aguilar, A., Aragort,
W., Álvarez, M.F., Leiro,
J.M. & Sanmartín, M. 2004. Hyperparasitism by Myxidium giardi 1906 (Myxozoa: Myxosporea) in Pseudodactylogyrus bini (Kikuchi, 1929) Gussev, 1965 (Monogenea: Dactylogyridae), a parasite of the European eel Anguilla anguillaL. Bulletin of the European Association of Fish Pathologists 24(6): 287-292.
Aho,
J.M., Uglem, G.L., Moore, J.P. & Larson, O.R.
1991. Bacteria associated with tegument of Clinostomum marginatum (Digenea). Journal of Parasitology 77(5): 784-786.
Al-Hisnawi,
A., Ringø, E., Davies, S.J., Waines,
P., Bradley, G. & Merrifield, D.L. 2015. First report on the autochthonous
gut microbiota of brown trout (Salmo truttaLinnaeus). Aquaculture Research 46(12):
2962-2971.
Almeida, M.V.A., Cangussú, Í.M., de Carvalho, A.L.S., Brito, I.L.P. & Costa, R.A. 2017.
Drug resistance, AmpC-β-lactamase and
extended-spectrum β-lactamase-producing Enterobacteriaceae isolated from fish and shrimp. Revista do Instituto de Medicina Tropical de
São Paulo 59: e70.
Aujoulat, F.,
Romano-Bertrand, S., Masnou, A., Marchandin,
H. & Jumas-Bilak, E. 2014. Niches, population
structure and genome reduction in Ochrobactrum intermedium: Clues to technology-driven emergence of pathogens. PLoS ONE 9(1): e83376.
Bakke, T.A., Cable, J. & Østbø, M. 2006. The ultrastructure of hypersymbionts on the monogenean Gyrodactylus salaris infecting Atlantic salmon Salmo salar. Journal of Helminthology 80(4): 377-386.
Bychowsky,
B.E. 1957. Monogenetic Trematodes, Their
Systematics and Phylogeny. English translation from the Russian (509 pp.:
1657) by Oustinoff, P.C. & Hargis Jr., W.J. 1961.
pp. xx 627. Washington D.C.: American Institute of Biological Science. Journal of the Marine Biological Association
of the United Kingdom 42(3): 707-708.
Cable, J. & Tinsley, R. 1992.
Microsporidian hyperparasites and bacteria associated
with Pseudodiplorchis americanus (Monogenea: Polystomatidae). Canadian
Journal of Zoology 70(3): 523-529.
Cone, D.K. & Odense, P.H. 1984.
Pathology of five species of Gyrodactylus Nordmann, 1832 (Monogenea). Canadian
Journal of Zoology 62(6): 1084-1088.
Cortés, A., Peachey, L., Scotti, R., Jenkins, T.P. & Cantacessi,
C. 2019. Helminth-microbiota crosstalk - A journey through the vertebrate
digestive system. Molecular and Biochemical Parasitology 233: 111222.
Cusack, R. & Cone, D.K. 1985. A
report of bacterial microcolonies on the surface of Gyrodactylus (Monogenea). Journal
of Fish Diseases 8: 125-127.
Cusack, R., Rand, T. & Cone, D.
1988. A study of bacterial microcolonies associated
with the body surface of Gyrodactylus colemanensis Mizelle & Kritsky, 1967 (Monogenea), parasitizing Salmo gairdneri Richardson. Journal of
Fish Diseases 11(3): 271-274.
Dashti,
A.A., Jadaon, M.M., Abdulsamad,
M.A. & Dashti, H.M. 2009. Heat treatment of
bacteria: A simple method of DNA extraction for molecular techniques. Kuwait
Medical Journal 41(2): 117-122.
Doughari,
H.J., Ndakidemi, P.A., Human, I.S. & Benade, S. 2011. The ecology, biology and pathogenesis of Acinetobacter spp.: An overview. Microbes and Environment 26(2): 101-112.
El-Naggar,
M. & Kearn, G. 1989. Haptor glands in the gill-parasitic, ancyrocephaline monogenean Cichlidogyrus halli typicus and the report of a possible prokaryotic
symbiont. International Journal for Parasitology 19(4): 401-408.
Fang, Y., Xie,
G.L., Lou, M.M., Li, B. & Muhammad, I. 2011. Diversity analysis of Burkholderia cepacia complex in the water bodies of West Lake, Hangzhou, China. Journal of
Microbiology 49(2): 309-314.
Garg, S.K., Kumar, S. & Tripathis, V.R. 2013. Antibiotic resistance and genetic
diversity in water-borne Enterobacteriaceae isolates from recreational and drinking water sources. International Journal
of Environmental Science and Technology 10: 789-798.
Hahn, M. & Dheilly,
N. 2018. Changes to the microbiome of the stomach and intestine of Threespine Sticklebacks associated with infection by the cestode Schistocephalus solidus. bioRxiv doi: https://doi.org/10.1101/290015.
Hall, C.M., Busch, J.D., Shippy, K., Allender, C.J., Kaestli, M., Mayo, M., Sahl,
J.W., Schupp, J.M., Colman, R.E., Keim,
P., Currie, B.J. & Wagner, D.M. 2015. Diverse Burkholderia species isolated from soils in the southern United States with no
evidence of B. pseudomallei. PLoS ONE 10: e0143254.
Hughes-Stamm,
S.R., Cribb,
T.H. & Jones, M.K. 1999.
Structure of the tegument and ectocommensal microorganisms of Gyliauchen nahaensis (Digenea: Gyliauchenidae), an
inhabitant of herbivorous fish of the Great Barrier Reef, Australia. Journal
of Parasitology 85(6): 1047-1052.
Ismail, N.I.A., Amal,
M.N.A., Shohaimi, S., Saad,
M.Z. & Abdullah, S.Z. 2016. Associations of water quality and bacteria
presence in cage cultured red hybrid tilapia, Oreochromis niloticus × O. mossambicus. Aquaculture Reports 4: 57-65.
Izvekova,
G.I. 2006. Trophic interactions in the system host (Eelpout Lota lota) -
parasite (Eubothrium rugosum) -
symbiotic microflora at hydrolysis of carbohydrate food components. Journal
of Evolutionary Biochemistry and Physiology 42(5): 595-603.
Justine, J. & Bonami, J. 1993. Virus-like particles in a monogenean (platyhelminthes) parasitic in a marine fish. International
Journal for Parasitology 23(1): 69-75.
Kearn,
G.C. 1963. Feeding in parasites: Solea solea on some monogenean skin Entobdella Soleae on and Acanthocotyle sp. Journal of the Marine Biological Association of the United
Kingdom 4: 749-766.
Kearn,
G.C. 1994. Evolutionary expansion of the Monogenea. International
Journal for Parasitology 24(8): 1227-1271.
Kearn,
G.C. 1999. The survival of monogenean (platyhelminth)
parasites on fish skin. Parasitology 119: Suppl S57-S88.
King, R.K., Flick, G.J., Pierson,
M.D., Smith, S., Boardman, G.D. & Coale, C.W.
2004. Identification of bacterial pathogens in biofilms of recirculating
aquaculture systems. Journal of Aquatic Food Product Technology 13(1):
125-133.
Korneva, J. 2008. Nanobacteria associated with mucous intestines of
freshwater fishes and tegument of their parasites (Cestoda). Acta Parasitologica 53(3): 312-314.
Korneva, Z.V. & Plotnikov,
A.O. 2012. Ultrastructure adaptations of symbiotic bacteria associated with
freshwater fish and their cestode parasites. Inland
Water Biology 5(2): 178-183.
Korneva,
Z.V. & Plotnikov, A.O. 2009. The morphology of
symbiotic nanobacteria associated with the
digestive-transport surfaces of freshwater fishes and the tegument of their cestode parasites. Inland Water Biology 2: 280-285.
Lane,
D.J. 1991. 16S/23S rRNA sequencing. In Nucleic
Acid Techniques in Bacterial Systematics, edited by Stackebrandt,
E. & Goodfellow, M. New York: John Wiley and
Sons. pp. 115-175.
Lapteva,
N.A. & Izvekova, G.I. 2004. Microflora associated
with the digestive-transport surfaces of fish and their parasitic cestodes. Russian Journal of Ecology 35: 176-180.
Lasee, B.A. & Sutherland, D.R. 1993.
Bacterial colonization of tegumental surfaces of Culaeatrema inconstans.
Journal of Fish Diseases 16: 83-85.
Leung, K.T., Chang, Y.J., Gan, Y.D., Peacock, A. & Macnaughton,
S.J. 1999. Detection of Sphingomonas spp. in soil by PCR and sphingolipid
biomarker analysis. Journal of Industrial Microbiology and Biotechnology 23(4-5): 252-260.
Li, J., Cao, J.L., Wang, X., Liu,
N., Wang, W.M. & Luo, Y. 2017. Acinetobacter pittii, an emerging new multi-drug resistant fish
pathogen isolated from diseased blunt snout bream (Megalobrama amblycephalaYih) in China. Applied
Microbiology and Biotechnology 101: 6459-6471.
Lim, S.Y., Ooi,
A.L. & Wong, W.L. 2016. Gill monogeneans of Nile tilapia (Oreochromis niloticus)
and red hybrid tilapia (Oreochromis spp.) from the wild and fish farms in Perak, Malaysia: Infection dynamics and
spatial distribution. Springerplus 5(1): 1609.
Mahboub,
H.H., Elsheshtawy, H.M., Sheraiba,
N.I., Fahmy, E.M., Masoud,
S.R., Mohamed, E.A.A., Abdelnaeim, N.S., Mohamed,
D.I., Ismail, T.A. & Ahmed, S.A.A. 2022. Dietary black cumin (Nigella
sativa) improved hemato-biochemical, oxidative
stress, gene expression, and immunological response of Nile tilapia (Oreochromis niloticus)
infected by Burkholderia cepacian. Aquaculture Reports 22: 100943.
Maravić,
A., Skočibušić, M., Šprung,
M., Šamanić, I., Puizina,
J. & Pavela-Vrančić, M. 2012.
Occurrence and antibiotic susceptibility profiles of Burkholderia cepacia complex in coastal marine
environment. International Journal of Environmental Health Research 22(6): 531-542.
Morley, N.J. 2016. Symbiotic
bacteria of helmints: What role may they play in
ecosystem under anthropogenic stress? Journal of Helminthology 90(6):
647-657.
Morris, G. 1973. The morphology of
associations between a trematode (Megalodiscus temperatus) and bacteria. Canadian Journal of
Zoology 51(12): 1313-1314.
Morris, G. & Halton,
D. 1975. The occurrence of bacteria and mycoplasma-like organisms in a
monogenean parasite, Diclidophora merlangi. International
Journal for Parasitology 5(5): 495-498.
Nemec, A., Musílek,
M., Šedo, O., De Baere, T., Maixnerová, M., van der Reijden,
T.J.K., Zdráhal, Z., Vaneechoutte,
M. & Dijkshoorn, L. 2010. Acinetobacter bereziniae sp. nov. and Acinetobacter guillouiae sp. nov., to accommodate Acinetobacter genomic species 10
and 11, respectively. International Journal of Systematic and Evolutionary
Microbiology 60: 896-903.
Nemec, A., Krizova,
L., Maixnerová, M., van der Reijden,
T.J.K., Deschaght, P., Passet,
V., Vaneechoutte, M., Brisse,
S. & Dijkshoorn, L. 2011. Genotypic and
phenotypic characterization of the Acinetobacter calcoaceticus-Acinetobacter baumannii complex with the proposal of Acinetobacter pittii sp. nov. (formerly Acinetobacter genomic species 3) and Acinetobacter nosocomialis sp. nov. (formerly Acinetobacter genomic species 13TU). Research in Microbiology 162: 393-404.
Ogawa, K. 2015. Diseases of cultured
marine fishes caused by Platyhelminthes (Monogenea, Digenea, Cestoda). Parasitology 142(1): 178-195.
Olapade,
O.A., Gao, X. & Leff, L.G. 2005. Abundance of
three bacterial populations in selected streams. Microbial Ecology 49(3): 461-467.
Pakingking,
R., Palma, P. & Usero, R. 2015. Quantitative and
qualitative analyses of the bacterial microbiota of tilapia (Oreochromis niloticus)
cultured in earthen ponds in The Philippines. World Journal of Microbiology
and Biotechnology 31(2): 265-275.
Pariselle,
A. & Euzet, L. 1995. Scutogyrus gen. n. (Monogenea, Ancyrocephalidae) for Cichlidogyrus longicornis minus Dossou, 1982, C. l. longicornis, and C. l. gravivaginusPaperna and Thurston, 1969, with description of three new species parasitic on African
Cichlids. Journal of Helminthological Society of Washington 62(2):
157-173.
Pariselle,
A. & Euzet, L. 2009. Systematic
revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31(4): 849-898.
Pati,
N.B., Doijad, S.P., Schultze,
T., Mannala, G.K., Yao, Y., Jaiswal,
S., Ryan, D., Suar, M., Gwozdzinski,
K., Bunk, B., Mraheil, M.A., Marahiel,
M.A., Hegemann, J.D., Sprӧer,
C., Goesmann, A., Falgenhauer,
L., Hain, T., Imirzalioglu, C., Mshana,
S.E., Overmann, J. & Chakraborty, T. 2018. Enterobacter bugandensis:
A novel enterobacterial species associated with
severe clinical infection. Scientific Reports 8: 5392.
Pękala-Safińska, A. 2018. Contemporary threats of
bacterial infections in freshwater fish. Journal of Veterinary Research 62: 261-267.
Plotnikov, A.O. & Korneva,
Z.V. 2008. Morphological and ultrastructural characteristics of symbiotic
bacteria colonizing the surface of the helminth Triaenophorus nodulosusand the intestine of pike Esox lucius. Inland
Water Biology 1(1): 25-31.
Poddubnaya,
L.G. & Izvekova, G.I. 2005. Detection of bacteria
associated with the tegument of caryophyllidean cestodes. Helminthologia 42(1): 9-14.
Rahman,
M.M., Izzuddin, M.H., Khan, N.S., John, A. & Naim, M.A. 2018. DNA barcoding and molecular phylogeny of
indigenous bacteria in fishes from a tropical tidal river in Malaysia. In DNA
Barcoding and Molecular Phylogeny, edited by Trivedi, S., Rehman, H., Saggu, S., Panneerselvam, C. & Ghosh, S. Switzerland: Springer.
pp. 351-366.
Selvakumar,
G., Kundu, S., Joshi, P., Nazim,
S., Gupta, A.D., Mishra, P.K. & Gupta, H.S. 2008. Characterization of a
cold-tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine
soil in the North Western Indian Himalayas. World Journal of Microbiology
and Biotechnology 24(7): 955-960.
Sepúlveda,
F.A., Kundu, S., Joshi, P., Nazim,
S., Gupta, A.D., Mishra, P.K. & Gupta, H.S. 2017. Potential role of ectoparasites (Zeuxapta seriolae and Caligus lalandei) in the transmission of pathogenic bacteria in
yellowtail kingfish Seriola lalandi,
inferred from cultivable microbiota and molecular analyses. Journal of Fish
Diseases 40(7): 979-985.
Sproston, N.G. 1946. A synopsis of the
monogenetic trematodes. Transactions of the Zoological Society of London 25: 185-600.
Sudheesh, P.S., Al-Ghabshi,
A., Al-Mazrooei, N. & Al-Habsi,
S. 2012. Comparative pathogenomics of bacteria
causing infectious diseases in fish. International Journal of Evolutionary
Biology 4: 457264.
Thakuria,
D., Schmidt, O., Finan, D., Egan, D. & Doohan, F.M. 2010. Gut wall bacteria of earthworms: A
natural selection process. Journal of the International Society for
Microbial Ecology 4: 357-366.
Urbaniak,
C., Sielaff, A.C., Frey, K.G., Allen, J.E., Singh,
N., Jaing, C., Wheeler, K. & Venkateswaran,
K. 2018. Detection of antimicrobial resistance genes associated with the
International Space Station environmental surfaces. Scientific Reports 8(1): 814.
Vanlaere,
E., Baldwin, A., Gevers, D., Henry, D., Brandt, E.D., LiPuma, J.J., Mahenthiralingam,
E., Speert, D.P., Dowson, C. & Vandamme, P. 2009. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminanssp. nov. and Burkholderia latasp. nov. International Journal of Systematic and
Evolutionary Microbiology 59: 102-111.
White, E.C., Houlden,
A., Bancroft, A.J., Hayes, K.S., Goldrick, M., Grencis, R.K. & Roberts, I.S. 2018. Manipulation of
host and parasite microbiotas: Survival strategies during chronic nematode
infection. Science Advances 4(3): eaap7399.
Whittington, I.D. 2012. Benedenia seriolae and Neobenedenia species.
In Fish Parasites: Pathobiology and Protection, edited by Woo, P.T.K.
& Buchmann, K. Wallingford: CABI. pp. 225-244.
Yamaguti, S. 1963. Systema Helminthum. IV, Monogenea and Aspidocotylea. New York: Interscience Publisher. pp. 1-699.
*Pengarang untuk surat-menyurat; email: wongwl@utar.edu.my
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