SciELO - Scientific Electronic Library Online

 
vol.25 issue2LIPID VESICLES: APPLICATIONS, PRINCIPAL COMPONENTS AND METHODS USED IN THEIR FORMULATIONS. A REVIEWDIURNAL FEEDING BEHAVIOUR OF CRAB-EATING RACCOON UPON A PARADOXAL FROG, WITH A REVIEW OF ITS DIET author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Acta Biológica Colombiana

Print version ISSN 0120-548X

Acta biol.Colomb. vol.25 no.2 Bogotá May/Aug. 2020

https://doi.org/10.15446/abc.v25n2.76405 

Nota Breve

ANTIFUNGAL ACTIVITY SCREENING OF ANTARCTIC ACTINOBACTERIA AGAINST PHYTOPATHOGENIC FUNGI

Evaluación de la actividad antifúngica de actinobacterias antárticas contra hongos fitopatógenos

Andrés SANTOS1  2   

Kattia NÚÑEZ-MONTERO1  2  3   

Claudio LAMILLA1  2 

Mónica PAVEZ1  2 

Damián QUEZADA-SOLÍS1 

Leticia BARRIENTOS1  2  * 

1 Laboratorio de Biología Molecular Aplicada, Centro de Excelencia en Medicina Traslacional, Universidad de La Frontera, Avenida Alemania 0458, 4810296 Temuco, Chile

2 Núcleo Científico y Tecnológico en Biorecursos (BIOREN), Universidad de La Frontera, Avenida Francisco Salazar 01145, 481123 Temuco, Chile

3 Centro de Investigación en Biotecnología, Escuela de Biología, Instituto Tecnológico de Costa Rica, 30101 Cartago, Costa Rica.


ABSTRACT

The extreme weather conditions in the Antarctic have exerted selective pressures favoring differential features in bacteria to survive this untapped environment (i.e., antibiotic molecules). Notably, higher chances of antibiotic discovery from extremophiles have been proposed recently. Although new organic and environmentally friendly sources for helping in the control of plant pathogenic fungi are necessary, the information about anti-phytopathogenic applications of extremophile microorganisms from untapped environments is limited. In this study, we determined the antifungal effect of actinobacterial strains isolated from Antarctic soils and sediments. Co-culture inhibition assays and Minimum Inhibitory Concentration (MIC) determination revealed that all Antarctic strains (x28) can inhibit the growth of at least one phytopathogenic fungi including Fusarium oxysporum, Rhizoctonia solani, Botrytis sp. and Phytophthora infestans. Additionally, new novel antagonistic relationships are reported. Our work establishes a precedent on Antarctic actinobacteria strains with the capacity to produce antifungal compounds, and its potential for developing new fungicides or biocontrol agents solving current agriculture problems.

Keywords: Antagonism; Antarctic bacteria; antifungal; extremophile; plant pathogen

RESUMEN

Las condiciones climáticas extremas en la Antártica han ejercido presiones selectivas en las bacterias, de forma que éstas poseen características diferenciales (ej. moléculas antibióticas) que les permiten sobrevivir a este entorno poco explorado. Recientemente se ha propuesto que pueden existir mayores posibilidades para el descubrimiento de antibióticos a partir de extremófilos. A pesar de que son necesarias nuevas fuentes orgánicas y amigables con el medio ambiente para controlar los hongos patógenos en plantas, la información sobre las aplicaciones anti-fitopatogénicas de microorganismos extremófilos, de ambientes poco explorados, es limitada. En este estudio, se determinó el efecto antifúngico de actinobacterias aisladas de suelos y sedimentos antárticos. Mediante ensayos de inhibición en co-cultivo y determinación de la concentración mínima inhibitoria (CIM) se reveló que todas las cepas antárticas (x28) tienen la capacidad de inhibir el crecimiento de al menos un hongo fitopatógeno, incluyendo Fusarium oxysporum, Rhizoctonia solani, Botrytis sp. y Phytophthora infestans. Adicionalmente, se reportan nuevas relaciones antagónicas. Nuestro trabajo establece un precedente sobre cepas de actinobacterias antárticas con capacidad para la producción de compuestos antifúngicos y su potencial para el desarrollo de nuevos fungicidas o agentes de control biológico con el fin de resolver problemas actuales de la agricultura.

Palabras clave: Antagonismo; antifúngico; bacteria antártica; extremófilos; patógeno de plantas

Antarctica is an isolated ice-bound continent; only 0.34 % of its area is ice-free with terrestrial ecosystems such as exposed nunataks and cliffs (Convey et al., 2009). Biodiversity is simple compared with other regions of the Earth, due to the severe climatic conditions and the scarcity of suitable habitats. Higher taxonomic groups are not represented in this environment; however in terms of biomass and diversity, microorganisms dominate both (Convey et al., 2009). The Actinobacteria phylum has been reported as one of the more abundant microbial groups in different Antarctic regions (Cary et al., 2010; Pearce et al., 2012). This phylum is recognized as a producer of a wide variety of secondary metabolites with different activities including herbicides, antifungals, antitumor or immunosuppressant compounds, and anthelmintic agents (Manivasagan et al., 2014).

Bacteria inhabiting Antarctica have adopted peculiar survival strategies to achieve competitive advantages (Núñez-Montero and Barrientos, 2018). Particularly, antagonistic activity may contribute to the adaptation of Antarctic bacteria to permanently low temperatures by reducing the presence of competitive microorganisms (Lo Giudice et al., 2007). Therefore, we hypothesized that our collection of Antarctic psychrophilic Actinobacteria might represent an unexplored source of antifungal compounds for the biocontrol of phytopathogenic fungi, helping to cover an essential need in agriculture.

Plant-fungal pathogens cause most of the diseases occurring in agricultural and horticultural industries, leading to annual economic losses that exceed 200 billion US dollars (Shuping and Eloff, 2017). Fungi species such as Phytophthora infestans, Fusarium oxysporum, Botrytis sp., and Rhizoctonia solani are probably some of the most essential plant pathogens currently described. P. infestans is a foliar pathogen and causes severe losses to potato and tomato crops worldwide, while some pathogenic strains of F. oxysporum are responsible for wilt in various plant species (Son et al., 2008). Botrytis sp. is the causal agent of gray mold disease in a broad range of dicotyledonous plants, with a large impact on wine grapes (Plesken et al., 2015). Finally, R. solani is known as the cause of rice sheath blight, black scurf on potatoes, bare patch on cereals, and root on soybean, among many other diseases (Wibberg et al., 2016).

It is extremely important to find new organic and environmentally friendly sources to help control plant pathogenic fungi, considering that the indiscriminate and excessive use of fungicides owing to reduced efficacy of this products has led to environmental pollution and high residual toxicity (Son et al., 2008). This study aimed to determine the antifungal effect of actinobacteria strains isolated from the Antarctic against phytopathogenic fungi of agricultural interest.

A total of 28 Antarctic Actinobacteria strains previously isolated from soil, marine sediment and seawater were used (Lamilla et al., 2017) to evaluate the antagonistic effect against four phytopathogenic fungi: Fusarium oxysporum, Rhizoctonia solani, Botrytis sp., and Phytophthora infestans, kindly facilitated by the INIA-Chile collection (National Institute for Agricultural Research, Chile). To this aim, an in vitro antagonism assay by dual culture method was used to select the strains with potential for biocontrol, as previously described in similar works (Quecine et al., 2008; Costa et al., 2013; Law et al., 2017). Briefly, fungi inocula were cultivated in potato dextrose agar (PDA, Difco), except for P. infestans performed in V8 agar (CaCO3 3 g/L, agar 20 g/L, 16 % commercial V8 Campbell's juice) or OA (Oatmeal Agar: oatmeal 60 g/L, agar 15 g/L, pH 7.2).

Actinobacteria inoculum was grown in M1 broth (peptone 2.0 g/L, yeast extract 4.0 g/L, starch 10.0 g/L; agar 18.0 g/L, pH 7.0) at 150 rpm, 15 °C for five days. Bacterial suspensions equivalent to 0.5 McFarland were prepared for each Actinobacteria strain and cultivated in half of PDA, M1 or OA plates, which were incubated at 15 °C for eight days. Agar discs from each fungus were placed in the middle of the remaining agar plate (approximately 2 cm from the actinobacteria culture). The co-cultures were incubated at 20 °C, and inhibitory zones were evaluated after 48 h. Supernatants from active actinobacterial strains (30 ml from M1 cultures) were used to determine the Minimum Inhibitory Concentration (MIC) at 75, 50, 25, 12.5, 6.25, 3.3 and 1.56 % for each supernatant following the Clinical and Laboratory Standards Institute (Weinstein et al., 2012) recommended protocol in microdilution plate. Negative controls were performed using media without bacteria. All experiments were performed in triplicate.

Our results showed a high rate of antifungal activity among our Antarctic actinobacteria isolates (Table 1, Fig.1). All the strains showed antifungal activity for at least one of the fungi studied, most of them belonging to genus Arthrobacter (53 %), Streptomyces (17 %) and Rhodococcus (3.5 %). These genera are recognized for its capacity to produce antibiotic molecules: Streptomyces is a genus characterized by the ability to produce secondary metabolites, representing 70-80 % of the antibiotics produced by Actinobacteria (Jackson et al., 2018; Núñez-Montero et al., 2019); antifungal tetrapeptides and antimycobacterial molecules have been characterized from Rhodococcus sp. (Chiba et al., 1999; Iwatsuki et al., 2007); and Arthrobacter is a common genus ofActinobacteria present in soil, capable ofproducing antibiotics such as arthrobacillin type A, B and C (Wietz et al., 2010). Results showed that particularly strain Se18.01 (Arthrobacter polychromogenes) was capable of inhibiting the growth of all tested fungi; therefore, these bacteria could be secreting one or multiple bioactive metabolites with activity against phytopathogenic fungi, which have a pronounced and broad antifungal effect.

Table 1 Antagonistic effect and MIC determination of 28 actinobacteria strains isolated from Antarctic against four phytopathogenic fungi. 

*Area with human presence

a Based on (Lamilla et al., 2017)

+: inhibition of mycelial growth of the fungus is observed

-: No inhibition of mycelial growth of the fungus is observed

NG: No suitable growth of the actinobacteria strain or fungi in the media tested

PDA: Potato Dextrose Agar M1: M1 Agar

OA: Oatmeal Agar

MIC: Minimal Inhibitory Concentration

Figure 1 Different actinobacteria Antarctic strains inhibiting the growth of phytopathogenic fungi on agar plate antagonism assay. 

MIC determination showed that 13 of the strains (48 %) were able to inhibit the growth of F. oxysporum; these strains corresponded to Streptomyces sp. (So1) and Arthrobacter sp. (So2c and Dwa41.01), which inhibited at low concentrations (1.56 %; 3.13 %; and 6.25 %, respectively). Coincidently, other reports have shown the antifungal activity of Streptomyces sp. and Arthrobacter sp. against Fusarium sp. (Legrand et al., 2017; Rashad et al., 2017), however, there are no reports of cold-adapted members of these genera with activity against F. oxysporum.

On the other hand, Rhodococcus sp. (So6b) showed the lowest MIC (25 %) against Botrytis sp. among other 16 active strains with MIC values between 50 % and 75 %. To the best of our knowledge, this is the first report addressing the antifungal activity of an Antarctic Rhodococcus strain against Botrytis sp. Other authors have reported the antimicrobial activity from a marine Rhodococcus strain (Yellamanda et al., 2016), highlighting the potential of this genus for exploration of biological activities, and particularly, antifungal compounds. Similarly, four Arthrobacter strains (Arthrobacter oxydans Se5.02, Arthrobacter polychromogenes Se18.01 , Arthrobacter phenanthrenivorans Se32.02, Arthrobacter psychrolactophilus So5b) were able to inhibit the growth of Rhizoctonia solani at the lowest concentration tested (1.56 %), antagonistic relationships that have not been reported to date. Additionally, Phytophthora infestans was inhibited by eight out of 28 strains (26 %) with a lowest MIC of 25 % for Arthrobacter polychromogenes (Se18.01), Arthrobacter phenanthrenivorans (Se28.01), Streptomyces sp.(So13.3), and Rhodococcus sp. (Sod9), being the first description of antagonistic activity of these strains against P. infestans. The new antifungal potential activities described here suggest that Antarctic -and other extreme environments- could provide a new source for the discovery of active molecules due to the differential evolutionary attributes of its microbial life.

Antagonism on agar plates also showed that most of the actinobacteria strains change their activity dependently of the culture media composition. As previously reported, this could be explained because different culture conditions will activate distinct biosynthetic pathways for secondary metabolites production, since actinobacteria can have multiple silent biosynthetic gene clusters, which can be expressed under specific conditions (Rosen and Seyedsayamdost, 2017). Therefore, the nutritional differences between the tested culture media (M1, PDA or OA) allowed or suppressed the production of the antifungal bioactive metabolites. Consequently, in a further analysis it should be possible to design an optimized culture condition increasing the efficiency of Antarctic actinobacteria activity and production of antifungal compounds.

Antibiotic molecules by psychrophiles and psychrotolerant organisms has been poorly studied in comparison with mesophilic organisms (O'Brien et al., 2004); particularly, actinobacteria have been proposed as unexplored microorganisms for biocontrol in vegetable crops, nonetheless anti-phytopathogenic activity derived from Antarctic actinobacteria have been previously reported only for some bacterial plant pathogens (i.e. Xhanthomonas sp. and Erwinia sp.) (Núñez-Montero and Barrientos, 2018). Some other works have described anti-phytopathogenic fungi effects and biocontrol potential from Antarctic yeast strains (Vero et al., 2013; Sangorrín et al., 2014) and fungus (Fenice and Gooday, 2006), and cold-adapted chitinolytic microorganisms have been described as an attractive source for potential biocontrol of phytopathogens in cold environments and the biocontrol of microbial spoilage of refrigerated food (Park et al., 2009; Ramli et al., 2011). Our work provides valuable data on Antarctic actinobacteria strains with the capacity to produce antifungal compounds against phytopathogenic fungi and has a real potential to become a fungicide or antifungal source for biocontrol in multiple crops. Also, we should note the importance of performing the chemical analyzes to determine the novelty of the metabolites being produced by these Antarctic strains and field trials for the promising actinobacterial strains will be undertaken to validate their possible role as biocontrol agents. It is noteworthy that cold-adapted actinobacteria might represent an interest biocontrol source, protecting crops with higher efficiency even at low temperatures during winter and in temperate climate zones.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge Grant INACH RT_14-12 from Instituto Antártico Chileno, Grant DI19-0079 from Universidad de La Frontera, Chilean National Commission for Scientific and Technological Research (CONICYT-PFCHA/Doctorado Nacional/2017-21170263 to K.N-M and CONICYT-PFCHA/Doctorado Nacional/2017-21171392 to A.S), and to the Network for Extreme Environments Research (NXR 17-0003). Attribution to https://www.freepik.es/fotos-vectores-gratis/ made by brgfx www.freepik.es for vectors used in the graphical abstract.

REFERENCES

Cary SC, McDonald IR, Barrett JE, Cowan DA. On the rocks: The microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol. 2010;8:129-38. Doi: https://doi.org/10.1038/nrmicro2281.Links ]

Chiba H, Agematu H, Kaneto R, Terasawa T, Sakai K, Dobashi K, Yoshioka T. Rhodopeptins ( Mer-N1033 ), Novel Cyclic Tetrapeptides with Antifungal. Activity from Rhodococcus sp. wit J Antibiot . 1999;52(8):695-699. [ Links ]

Convey P, Stevens MI, Hodgson DA, Smellie JL, Hillenbrand CD, Barnes DKA, et al. Exploring biological constraints on the glacial history of Antarctica. Quat Sci Rev. 2009;28(27-28):3035-3048. Doi: https://doi.org/10.1016/j.quascirev.2009.08.015Links ]

Costa FG, Zucchi TD, de Melo IS. Biological control of phytopathogenic fungi by endophytic actinomycetes isolated from maize (Zea mays L.). Brazilian Arch Biol Technol. 2013;56(6):948-955. Doi: https://doi.org/10.1590/S1516-89132013000600009Links ]

Fenice M, Gooday GW. Mycoparasitic actions against fungi and oomycetes by a strain (CCFEE 5003) of the fungus Lecanicillium muscarium isolated in Continental Antarctica. Ann Microbiol. 2006;56:1-6. Doi: https://doi.org/10.1007/BF03174961Links ]

Lo Giudice A, Bruni V, Michaud L. Characterization of Antarctic psychrotrophic bacteria with antibacterial activities against terrestrial microorganisms. J Basic Microbiol. 2007;47(6):496-505. Doi: https://doi.org/10.1002/jobm.200700227Links ]

Iwatsuki M, Uchida R, Takakusagi Y, Matsumoto A, Jiang CL, Takahashi Y, et al. Lariatins, novel anti-mycobacterial peptides with a lasso structure, produced by Rhodococcus jostii K01-B0171. J Antibiot. 2007;60:367-363. Doi: https://doi.org/10.1038/ja.2007.48Links ]

Jackson SA, Crossman L, Almeida EL, Margassery LM, Kennedy J, Dobson ADW. Diverse and abundant secondary metabolism biosynthetic gene clusters in the genomes of marine sponge derived Streptomyces spp. Isolates. Mar Drugs. 2018;16(2):67. Doi: https://doi.org/10.3390/md16020067Links ]

Lamilla C, Pavez M, Santos A, Hermosilla A, Llanquinao V, Barrientos L. Bioprospecting for extracellular enzymes from culturable Actinobacteria from the South Shetland Islands, Antarctica. Polar Biol. 2017;40(3):719-726. Doi: https://doi.org/10.1007/s00300-016-1977-zLinks ]

Law JWF, Ser HL, Khan TM, Chuah LH, Pusparajah P, Chan KG, et al. The potential of Streptomyces as Biocontrol Agents against the Rice Blast Fungus, Magnaporthe oryzae (Pyricularia oryzae). Front Microbiol. 2017;8. Doi: https://doi.org/10.3389/fmicb.2017.00003Links ]

Legrand F, Picot A, Cobo-Díaz JF, Chen W, Le Floch G. Challenges facing the biological control strategies for the management of Fusarium Head Blight of cereals caused by F. graminearum. Biol Control. 2017;113:26-38. Doi: https://doi.org/10.1016/j.biocontrol.2017.06.011Links ]

Manivasagan P, Kang KH, Sivakumar K, Li-Chan ECY, Oh HM, Kim SK. Marine actinobacteria: An important source of bioactive natural products. Environ Toxicol Pharmacol. 2014;38(1):172-188. Doi: https://doi.org/10.1016/j.etap.2014.05.014Links ]

Núñez-Montero K, Barrientos L. Advances in antarctic research for antimicrobial discovery: A Comprehensive narrative review of bacteria from antarctic environments as potential sources of novel antibiotic compounds against human pathogens and microorganisms of industrial importance. Antibiotics. 2018;7(4):90. Doi: https://doi.org/10.3390/antibiotics7040090Links ]

Núñez-Montero K, Lamilla C, Abanto M, Maruyama F, Jorquera MA, Santos A, Martinez-Urtaza J, Barrientos L. Antarctic Streptomyces fildesensis So13.3 strain as a promising source for antimicrobials discovery. Sci Rep. 2019;9:7488. Doi: https://doi.org/10.1038/s41598-019-43960-7Links ]

O'Brien A, Sharp R, Russell NJ, Roller S. Antarctic bacteria inhibit growth of food-borne microorganisms at low temperatures. FEMS Microbiol Ecol. 2004;48(2):157-167. Doi: https://doi.org/10.1016/j.femsec.2004.01.001Links ]

Park HJ, Kim D, Kim IH, Lee CE, Kim IC, Kim JY, et al. Characteristics of cold-adaptive endochitinase from Antarctic bacterium Sanguibacter antarcticus KOPRI 21702. Enzyme Microb Technol. 2009;45(5):391-396. Doi: https://doi.org/10.1016/j.enzmictec.2009.07.002Links ]

Pearce DA, Newsham KK, Thorne MAS, Calvo-Bado L, Krsek M, Laskaris P, et al. Metagenomic Analysis of a Southern Maritime Antarctic Soil. Front Microbiol. 2012;3:403. Doi: https://doi.org/10.3389/fmicb.2012.00403Links ]

Plesken C, Weber RWS, Rupp S, Leroch M, Hahn M. Botrytis pseudocinerea is a significant pathogen of several crop plants but susceptible to displacement by fungicide-resistant B. cinerea strains. Appl Environ Microbiol. 2015;81:7048-7056. Doi: https://doi.org/10.1128/AEM.01719-15Links ]

Quecine MC, Araujo WL, Marcon J, Gai CS, Azevedo JL, Pizzirani-Kleiner AA. Chitinolytic activity of endophytic Streptomyces and potential for biocontrol. Lett Appl Microbiol. 2008;47(6):486-491. Doi: https://doi.org/10.1111/j.1472-765X.2008.02428.xLinks ]

Ramli ANM, Mahadi NM, Rabu A, Murad AMA, Bakar FDA, lllias RM. Molecular cloning, expression and biochemical characterisation of a cold-adapted novel recombinant chitinase from Glaciozyma antarctica PI12. Microb Cell Fact. 2011;10:94. Doi: https://doi.org/10.1186/1475-2859-10-94Links ]

Rashad YM, Al-Askar AA, Ghoneem KM, Saber WIA, Hafez EE. Chitinolytic Streptomyces griseorubens E44G enhances the biocontrol efficacy against Fusarium wilt disease of tomato. Phytoparasitica. 2017;45(2):227-237. Doi: https://doi.org/10.1007/s12600-017-0580-3Links ]

Rosen PC, Seyedsayamdost MR. Though Much Is Taken, Much Abides: Finding New Antibiotics Using Old Ones. Biochemistry. 2017;56(37):4925-4926. Doi: https://doi.org/10.1021/acs.biochem.7b00782Links ]

Sangorrín MP, Lopes CA, Vero S, Wisniewski M. Cold-adapted yeasts as biocontrol agents: Biodiversity, adaptation strategies and biocontrol potential. In: Buzzini P, Margesin R, editors. Cold-adapted YeastsBiodiversity, Adapt. Strateg. Biotechnol. Significance, Berlin, Heidelberg: Springer; 2014. Doi: https//10.1007/978-3-642-39681-6. [ Links ]

Shuping DSS, Eloff JN. The use of plants to protect plants and food against fungal pathogens: A review. African J Tradit Complement Altern Med AJTCAM. 2017;14(4):120-127. Doi: https://athmsi.org/journals/index.php/ajtcam/article/view/4728Links ]

Son SW, Kim HY, Choi GJ, Lim HK, Jang KS, Lee SO, et al. Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against Phytophthora infestans. J Appl Microbiol. 2008;104(3):692-698. Doi: https://doi.org/10.1111/j.1365-2672.2007.03581.xLinks ]

Vero S, Garmendia G, González MB, Bentancur O, Wisniewski M. Evaluation of yeasts obtained from Antarctic soil samples as biocontrol agents for the management of postharvest diseases of apple (Malus x domestica). FEMS Yeast Res. 2013;13(2):189-199. Doi: https://doi.org/10.111 1/1567-1364.12021Links ]

Weinstein MP, Zimmerl BL, Cockerill FR, Wiker MA, Alder J, Dudley MN, et al. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Clin Lab Stand Inst. 2012;11:1-91. [ Links ]

Wibberg D, Andersson L, Tzelepis G, Rupp O, Blom J, Jelonek L, et al. Genome analysis of the sugar beet pathogen Rhizoctonia solani AG2-2IIIB revealed high numbers in secreted proteins and cell wall degrading enzymes. BMC Genomics. 2016;17:245. Doi: https://doi.org/10.1186/s12864-016-2561-1Links ]

Wietz M, Mansson M, Gotfredsen CH, Larsen TO, Gram L. Antibacterial compounds from marine Vibrionaceae isolated on a global expedition. Mar Drugs. 2010;8(12):2946-2960. Doi: https://doi.org/10.3390/md8122946Links ]

Yellamanda B, Vijayalakshmi M, Kavitha A, Reddy DK, Venkateswarlu Y. Extraction and bioactive profile of the compounds produced by Rhodococcus sp. VLD-10. 3 Biotech. 2016;6:261. Doi: https://doi.org/10.1007/s13205-016-0576-6Links ]

Associate Editor: Juan F. González.

Citation/Citar este artículo como: Santos A, Núñez-Montero K, Lamilla C, Pavez M, Quezada-Solís D, Barrientos L. Antifungal activity screening of Antarctic Actinobacteria against Phytopathogenic Fungi. Acta biol. Colomb. 2020;25(2):353-358. DOI: http://dx.doi.org/10.15446/abc.v25n2.76405

CONFLICT OF INTEREST The authors declare that there is no conflict of interest

Received: November 23, 2018; Revised: May 17, 2019; Accepted: May 28, 2019

* For correspondence: leticia.barrientos@ufrontera.cl

These authors contributed equally to this work.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License