Sains Malaysiana 52(1)(2023): 83-93
http://doi.org/10.17576/jsm-2023-5201-07
A Talaromyces Fungal Species with Strong Antimicrobial
Activity from Deception Island, Antarctica
(Spesies Kulat Talaromyces dengan Aktiviti Antimikrob Kuat dari Pulau Deception, Antartika)
SHEAU TING
YONG1, PARIS LEONARDO LAVIN2, MARCELO ARAVENA GONZÁLEZ3 & CLEMENTE
MICHAEL VUI LING WONG1,*
1Biotechnology Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia
2Departamento de Biotecnologia, Facultad de Ciencias del Mary Recursos Biologicos, Universidad de Antofagasta,
601 Avenida Angamos, Antofagasta 1270300, Chile
3Instituto Antártico Chileno, Plaza Muñoz Gamero 1055, Punta Arenas, Chile
Diserahkan: 1 April 2022/Diterima:
11 Oktober 2022
Abstract
Deception Island is well-known for harboring highly diverse microbial communities due to its
unique volcanic environment in Antarctica. Most studies focused on bacteria,
and relatively little was known about the fungal species on this island. The
present study was aimed to determine the antimicrobial production and nutrient
utilization profiles of a soil fungus from Deception Island, designated as
Im33. Our findings showed that the strain had maximum mycelial growth and sporulation on malt-extract agar (MEA) medium, but it demonstrated the strongest
antimicrobial activity in yeast extract-malt extract broth (YMB) medium. Phylogenetic analysis of the internal
transcribed spacer 1 and 2 regions showed that it is a species belonging to the
genus Talaromyces. It
was resistant to cycloheximide concentrations up to 1,000 mg/L and exhibited broad-spectrum antimicrobial activity
against Gram-positive and Gram-negative test pathogens, as well as being able
to utilize a variety of carbon sources. This is the first report of a Talaromyces species
from Deception Island. The capability of the strain to produce broad-spectrum
antimicrobial compounds and various enzymes indicated that Antarctic fungi,
like their bacterial counterparts, have adopted various adaptation strategies
to compete and survive in the extreme environment.
Keywords: Antarctic; antimicrobial resistance;
enzymes; fungus; South Shetland Islands
Abstrak
Pulau Deception terkenal dengan kepelbagaian
komuniti mikrob kerana persekitaran gunung berapinya yang unik di Antartika.
Kebanyakan kajian tertumpu kepada bakteria dan spesies kulat di pulau ini tidak
begitu diketahui. Kajian ini bertujuan untuk menentukan profil pengeluaran
antimikrob dan penggunaan nutrien kulat tanah dari Pulau Deception, iaitu Im33.
Penemuan kami menunjukkan bahawa strain ini mempunyai pertumbuhan miselia dan
spora maksimum pada media agar-ekstrak malt (MEA), tetapi menunjukkan aktiviti
antimikrob yang paling kuat dalam media ekstrak malt ekstrak yis (YMB).
Analisis filogenetik bagi kawasan spacer 1 dan 2 yang tertranskripsi
secara dalaman menunjukkan bahawa kulat ini tergolong dalam genus Talaromyces.
Kulat ini tahan terhadap kepekatan sikloheksimida sehingga 1,000 mg/L dan
menunjukkan aktiviti antimikrob spektrum luas terhadap patogen Gram-positif dan
Gram-negatif, di samping dapat menggunakan pelbagai punca karbon. Ini
merupakan laporan pertama spesies Talaromyces dari Pulau Deception.
Keupayaan strain ini untuk menghasilkan sebatian antimikrob spektrum luas dan
pelbagai enzim menunjukkan bahawa kulat Antartika, seperti bakteria lain, telah
menggunakan pelbagai strategi penyesuaian untuk bersaing dan bertahan dalam
persekitaran yang ekstrem.
Kata kunci: Antartika; enzim; kulat; Pulau Shetland Selatan; rintang antimikrob
RUJUKAN
Ajdari, Z., Ebrahimpour,
A., Abdul Manan, M., Hamid, M., Mohamad, R. & Ariff,
A.B. 2011. Nutritional requirements for the improvement of growth and
sporulation of several strains of Monascus purpureus on solid-state cultivation. Journal of Biomedicine and Biotechnology 2011: 487329.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. 1990.
Basic local alignment search tool. Journal of Molecular Biology 215:
403-410.
Bagy, M.M.K., Abdel-Mallek,
A.Y., El-Sahanawany, A.A. & Gamal, A.M. 1997.
Studies on fungi associated with laboratory ‘golden hamster’ and antibiotic
effects of aloe sap, garlic extract and onion oil. Medical Journal of Islamic World Academy of Sciences 10: 3-12.
Balmas, V., Scherm, B., Ghignone,
S.M., Salem, A.O.M., Cacciola, S.O. & Migheli, Q. 2005. Characterisation of Phoma tracheiphila by RAPD-PCR,
microsatellite-primed PCR and ITS rDNA sequencing and development of specific
primers for in planta PCR detection. European Journal of Plant Pathology 111: 235-247.
Blanco, Y.,
Prieto-Ballesteros, O., Gómez, M.J., Moreno-Paz, M., García-Villadangos,
M., Rodríguez-Manfredi, J.A., Cruz-Gil, P., Sánchez-Román, M., Rivas, L.A.
& Parro, V. 2012. Prokaryotic communities and
operating metabolisms in the surface and the permafrost of Deception Island
(Antarctica). Environmental Microbiology 14: 2495-2510.
Cheah, Y.K., Lee,
L.H., Chieng, C.C.Y. & Wong, C.M.V.L. 2015.
Isolation, identification and screening of Actinobacteria in volcanic soil of
Deception Island (the Antarctic) for antimicrobial metabolites. Polish Polar Research 36: 67-78.
Davies, J. & Davies, D. 2010.
Origins and evolution of antibiotic resistance. Microbiology and Molecular
Biology Reviews 74(3): 417-433.
Dehoux, P., Davies, J. &
Cannon, M. 1993. Natural cycloheximide resistance in yeast: The role of
ribosomal protein L41. European Journal of Biochemistry 213: 841-848.
Dennis, P.G.,
Rushton, S.P., Newsham, K.K., Lauducina,
V.A., Ord, V.J., Daniell, T.J., O’donnell,
A.G. & Hopkins, D.W. 2012. Soil fungal community composition does not alter
along a latitudinal gradient through the maritime and sub-Antarctic. Fungal Ecology 5: 403-408.
Elíades, L.A., Cabello, M., Voget,
C., Galarza, B. & Saparrat, M. 2010. Screening
for alkaline keratinolytic activity in fungi isolated
from soils of the biosphere reserve “Pargue Costero del Sur” (Argentina). World Journal of Microbiology and Biotechnology 26: 2105-2111.
Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:
783-791.
Fujimura, K.E.
& Egger, K.N. 2012. Host plant and environment influence community assembly
of high Arctic root-associated fungal communities. Fungal Ecology 5: 409-418.
Furbino, L.E., Godinho,
V.M., Santiago, I.F., Pellizari, F.M., Alves, T.M.A.,
Zani, C.L., Junior, P.A.S., Romanha, A.J., Carvalho,
A.G.O., Gil, L.H.V.G., Rosa, C.A., Minnis, A.M. &
Rosa, L.H. 2014. Diversity patterns, ecology and biological activities of
fungal communities associated with the endemic macroalgae across the Antarctic
Peninsula. Microbial Ecology 67: 775-787.
Gesheva, V. 2012.
Biological potential of soil populations in two Shetland islands, Livingston
and Deception. The Cyprus Journal of
Sciences 10: 111-118.
Gupta, M., Manisha, K. & Grover, R. 2012.
Effect of various media types on the rate of growth of Aspergillus niger. Indian Journal of Fundamental and Applied
Life Sciences 2: 141-144.
Held, B.W., Arenz, B.E. & Blanchette, R.A.
2011. Factors influencing the deterioration of historic structures at Deception
Island, Antarctica. In Polar Settlements -
Location, Techniques and Conservation, edited by Barr, S. & Chaplin, P. Oslo: International Polar Heritage
Committee of ICOMOS. pp. 35-43.
Hocking, A.D.,
Whitelaw, M. & Harden, T.J. 1998. Penicillium radicum sp. nov. from the rhizophere of Australian wheat. Mycology Research 102: 801-806.
Ibáñez, J.M., Almendros, J., Carmona, E., Martı́nez-Arévalo, C. & Abril, M. 2003. The
recent seismo-volcanic activity at Deception Island
volcano. Deep Sea Research Part II: Topical Studies in Oceanography 50:
1611-1629.
Inoue, H.,
Decker, S.R., Taylor, L.E., Yano, S. & Sawayama,
S. 2014. Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus)
critical for hydrolysis of lignocellulosic biomass. Biotechnology for Biofuels 7: 151.
Ismail, M.A., Taligoola, H.K. & Nakamya, R.
2010. Incidence of xerophilic/xerotolerant mycobiota, fusaria and nephrotoxigenic penicillia in some cereal baby foods imported into
Uganda. Journal of Basic and Applied
Mycology Egypt 1: 23-33.
Lo
Giudice, A.L., Bruni, V. & Michaud, L. 2007. Characterization of Antarctic psychrotrophic bacteria with antibacterial activities
against terrestrial microorganisms. Journal
of Basic Microbiology 47: 496-505.
Lo
Giudice, A.L., Brilli, M., Bruni, V., Domenico, M., Fani, R. & Michaud, L. 2007. Bacterium-bacterium
inhibitory interactions among psychrotrophic bacteria
isolated from Antarctic seawater (Terra Nova Bay, Ross Sea). FEMS Microbiology Ecology 60: 383-396.
Karaiskos, I., Lagou, S., Pontikis, K., Rapti, V. & Poulakou, G. 2019. The “old” and the “new” antibiotics for
MDR Gram-negative pathogens: For whom, when and how. Frontier in Public
Health 7: 151.
Kimura,
M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
Kominek, L.A. 1975. Cycloheximide production by Streptomyces
griseus: Control mechanisms of cycloheximide biosynthesis. Antimicrobial
Agents and Chemotherapy 7(6): 856-860.
Miao, F., Yang,
R., Chen, D.D., Wang, Y., Qin, B.F., Yang, X.J. & Zhou, L. 2012. Isolation,
identification and antimicrobial activities of two secondary metabolites of Talaromyces verruculosus. Molecules 17: 14091-14098.
Nei, M. & Kumar,
S. 2000. Molecular Evolution and Phylogenetics. Oxford: Oxford University Press.
Nurbaya, Kuswinanti, T., Rosmana, A., Baharuddin,
A.R.D.S.M. & Millang, S. 2014. Growth rate and
identification of Fusarium spp. associated with Aquillaria spp. from Nunukan regency, North Kalimantan. International Journal of Current Research
and Academic Review 2:
33-40.
Pretsch, A., Nagl, M., Schwendinger, K., Kreiseder, B., Wiederstein, M., Pretsch, D., Genov, M., Hollaus, R., Zinssmeister, D., Debbab, A., Hundsberger, H., Eger, A., Proksch,
P. & Wiesner, C. 2014. Antimicrobial and anti-inflammatory activities of
endophytic fungi Talaromyces wortmannii extracts against acne-inducing bacteria. PLoS ONE 9: e97929.
Samson, R.A.,
Yilmaz, N., Houbraken, J., Spierenburg,
H., Seifert, K.A., Peterson, S.W., Varga, J. & Frisvad, J.C. 2011. Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium. Studies in Mycology 70: 159-183.
Sharma, G. &
Pandey, R.R. 2010. Influence of culture media on growth, colony character and
sporulation of fungi isolated from decaying vegetable wastes. Journal of
Yeast and Fungal Research 1: 157-164.
Shirling, E.B. & Gottlieb, D. 1966. Methods for
characterization of Streptomyces species. International Journal of
Systematic Bacteriology 16: 313-340.
Svahn, K.S., Chryssanthou, E., Olsen, B., Bohlin,
L. & Göransson, U. 2015. Penicillium nalgiovense Laxa isolated from Antarctica is a new source of the
antifungal metabolite amphotericin B. Fungal
Biology and Biotechnology 2: 1.
Tamura,
K., Stecher, G., Peterson, D., Filipski,
A. & Kumar, S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729.
Tomova, I., Stoilova-Disheva, M., Lazarkevich, I. & Vasileva-Tonkova,
E. 2015. Antimicrobial activity and resistance to heavy metals and antibiotics
of heterotrophic bacteria isolated from sediment and soil samples collected
from two Antarctic islands. Frontiers in Life Science 8: 348-357.
Tranchida, M.C., Centeno, N.D., Stenglein,
S.A. & Cabello, M.N. 2016. First record of Talaromyces udagawae in soil related to
decomposing human remains in Argentina. Revista Argentina de Microbiologia 48(1): 86-90.
Udagawa, S. 1959. Taxonomic studies of fungi on
stored rice grains. III. Penicillium group (penicillia and related genera) 2. Journal of Agricultural Science, Tokyo Nogyo Daigaku. 5: 5-21.
Waters,
D.M., Ryan, L.A.M., Murray, P.G., Arendt, E.K. & Tuohy, M.G. 2011.
Characterisation of a Talaromyces emersonii thermostable enzyme cocktail with applications in wheat dough rheology. Enzyme and Microbial Technology 49:
229-236.
White, T.J.,
Bruns, T., Lee, S.J. & Taylor, J.W. 1990. Amplification and direct
sequencing of fungal ribosomal RNA genes for phylogeetics.
In PCR Protocols: A Guide to Methods and Applications, edited by
Innis, M.A., Gelfand, D.H., Sninsky, J.J. &
White, T.J. Massachusetts: Academic Press. pp. 315-322.
Wong, C.M.V.L.,
Tam, H.K., Alias, S.A., González, M., González-Rocha, G. & Domínguez-Yévenes, M. 2011. Pseudomonas and Pedobacter isolates from King George Island inhibited
the growth of foodborne pathogens. Polish Polar Research 32(1): 3-14.
Yamazaki,
H., Ōmura, S. & Tomoda,
H. 2010. 6’-hydrox-3’-methoxy-mitorubrin, a new potentiator of antifungal
miconazole activity, produced by Penicillium radicum FKI-3765-2. Chemical and Pharmaceutical Bulletin 58: 829-832.
Yamazaki,
H., Koyama, N., Ōmura, S. & Tomoda, H. 2010. New rugulosins, anti-MRSA antibiotics,
produced by Penicillium radicum FKI-3765-2. Organic
Letters 12: 1572-1575.
Zang,
Y., Genta-Jouve, G., Escargueil,
A.E., Larsen, A.K., Guedon, L., Nay, B. & Prado,
S. 2016. Antimicrobial oligophenalenone dimers from
the soil fungus Talaromyces stipitatus. Journal of Natural Products 79(12):
2991-2996.
*Pengarang untuk surat-menyurat; email: michaelw@ums.edu.my
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