First report of Akanthomyces dipterigenus (Hypocreales: Cordycipitaceae) in the Iberian Peninsula
DOI:
https://doi.org/10.6092/issn.2531-7342/18993Keywords:
aphid, bait, Lecanicillium, fungi, isolation, entomopathogenicAbstract
Akanthomyces dipterigenus is a species of entomopathogenic fungus (Hypocreales: Cordycipitaceae) that has undergone several reclassifications in recent decades. While it has been utilized for biological control, information on its distribution and ecology remains limited. Furthermore, this species has only recently been reported in continental European countries. Our research provides the first report of A. dipterigenus in the Iberian Peninsula. Fungal isolation was achieved via a modified baiting technique featuring Rhopalosiphum padi aphids. Results suggest that the isolation methodologies and ecological traits of the fungus may either aid or hinder its detection. Additional research is necessary to assess its distribution throughout the Peninsula and neighbouring European countries, and to examine its potential as a biological control agent.
References
Ali-Shtayeh MS, Mara'i AB, Jamous RM (2002) Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area. Mycopathologia 156(3):235‒44 http://doi.org/10.1023/a:1023339103522
Araújo JPM, Hughes DP (2016) Diversity of entomopathogenic fungi: which groups conquered the insect body? In: Advances in Genetics, vol. 94 (Lovett B, Leger RJS, eds). Academic Press, Elsevier, pp 1‒39. https://doi.org/10.1016/bs.adgen.2016.01.001
Asensio L, Carbonell T, López-Jiménez JA, López-Llorca LV (2003) Entomopathogenic fungi in soils from Alicante province [Spain]. Spanish Journal of Agricultural Research 1(3):37. https://doi.org/10.5424/sjar/2003013-33
Bengtsson-Palme J, Veldre V, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, Bertrand Y, De Wit P, Sánchez-García M, et al. (2013) ITSx: Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for use in environmental sequencing. Methods in Ecology and Evolution 4:914-919. https://doi.org/10.1111/2041-210X.12073
Berlanga-Padilla AM, Ayala-Zermeño MA, Gallou A, Serna-Domínguez MG, Montesinos-Matías R, Arredondo-Bernal HC (2018) Report of the sexual stage of Lecanicillium longisporum in Melanaphis sacchari. Scientia Fungorum 47:73–77. https://doi.org/10.33885/sf.2018.47.1195
Bueno-Pallero FA, Blanco-Pérez R, Vicente-Díez I, Rodríguez-Martín AA, Dionísio L, Campos-Herrera R (2020) Patterns of occurrence and activity of entomopathogenic fungi in the Algarve (Portugal) using different isolation methods. Insects 11:352. https://doi.org/10.3390/insects11060352
Díaz B, Oggerin M, Lastra CCL, Rubio VJ, Fereres A (2009) Characterization and virulence of Lecanicillium lecanii against different aphid species. Biocontrol 54(6):825–835. https://doi.org/10.1007/s10526-009-9218-9
Feng M, Johnson JB, Kish LP (1990) Survey of entomopathogenic fungi naturally infecting cereal aphids (Homoptera: Aphididae) of irrigated grain crops in southwestern Idaho. Environmental entomology 19(5):1534–1542. https://doi.org/10.1093/ee/19.5.1534
González-Baca G, Venegas-Barrera CS, González-Gaona OJ, Vargas-Madriz H, Jiménez-Gómez MA, Pérez E, Ausencio A, Domínguez A (2019) Abundancia y distribución de hongos entomopatógenos en diferentes localidades y ambientes del sur de Tamaulipas. Revista Mexicana de Ciencias Agrícolas 10(3). https://doi.org/10.29312/remexca.v10i3.1550
Irinyi L, Lackner M, Sybren de Hoog G, Meyer W (2016) DNA barcoding of fungi causing infections in humans and animals. Fungal Biology 120(2):125–136.
Hallouti A, Ait Hamza M, Zahidi A, Ait Hammou R, Bouharroud R, Ait Ben Aoumar A, Boubaker H (2020) Diversity of entomopathogenic fungi associated with Mediterranean fruit fly (Ceratitis capitata (Diptera: Tephritidae)) in Moroccan Argan forests and nearby area: impact of soil factors on their distribution. BMC Ecology 20:64. https://doi.org/10.1186/s12898-020-00334-2
Jabbour R, Barbercheck ME (2009) Soil management effects on entomopathogenic fungi during the transition to organic agriculture in a feed grain rotation. Biological Control 51(3):435–443. https://doi.org/10.1016/j.biocontrol.2009.08.004
Jaronski S (2008) Soil ecology of the entomopathogenic Ascomycetes: a critical examination of what we (think) we know. In: Use of Entomopathogenic Fungi in Biological Pest management (Ekesi S, Maniania NK, eds). Research Signpost,Trivandrum, India, pp 91–144.
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108
Kepler RM, Luangsa-Ard JJ, Hywel-Jones NL, Quandt CA, Sung GH, Rehner SA, Aime MC, Henkel TW, Sanjuan T, Zare R et al. (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus 8(2):335–353. https://doi.org/10.5598/imafungus.2017.08.02.08
Kouvelis VN, Sialakouma A, Typas MA (2008) Mitochondrial gene sequences alone or combined with ITS region sequences provide firm molecular criteria for the classification of Lecanicillium species. Mycological research 112(7):829–844. https://doi.org/10.1016/j.mycres.2008.01.016
Kovač M, Tkaczuk C, Pernek M (2021) First report of entomopathogenic fungi occurrence in forest soils in Croatia. Forests 12:1690. https://doi.org/10.3390/f12121690
Lacey LA (2012) Manual of techniques in invertebrate pathology, 2nd edition. Academic Press, London, UK.
Lebert H (1858) Ueber einige neue oder unvollkommen gekannte Krankheiten der Insekten, welche durch Entwicklung niederer Pflanzen im lebenden Körper enstehen. Zeitschrift für wissenschaftliche Zoologie 9:439–453.
Liu SL, Wang XW, Li GJ, Deng CY, Rossi W, Leonardi M, Liimatainen K, Kekki T, Niskanen T et al. (2024) Fungal diversity notes 1717–1817: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity 124:1–216. https://doi.org/10.1007/s13225-023-00529-0
Lopes RB, Souza TA, Mascarin GM, Souza DA, Bettiol W, De Souza HN, Faria M (2023) Akanthomyces diversity in Brazil and their pathogenicity to plant-sucking insects. Journal of invertebrate pathology 200:107955. https://doi.org/10.1016/j.jip.2023.107955
López-Lastra CCL, Lecuona RE (2019) Micopatologia de artrópodos. Ediciones INTA, Buenos Aires, Argentina.
Manfrino R, Gutierrez A, Diez del Valle F, Schuster C, Ben Gharsa H, López Lastra C, Leclerque A (2022) First description of Akanthomyces uredinophilus comb. nov. from hemipteran insects in America. Diversity 14:1118. https://doi.org/10.3390/d14121118
Medo J, Cagáň L (2011) Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biocontrol 59(2):200–208. https://doi.org/10.1016/j.biocontrol.2011.07.020
Meyling NV, Eilenberg J (2006). Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agriculture, Ecosystems and Environment 113:336–341. https://doi.org/10.1016/j.agee.2005.10.011
Meyling NV, Thorup-Kristensen K, Eilenberg J (2011) Below- and aboveground abundance and distribution of fungal entomopathogens in experimental conventional and organic cropping systems. Biological Control 59:180–186. https://doi.org/10.1016/j.biocontrol.2011.07.017
Mora MAE, Rouws JRC, Fraga ME (2016) Occurrence of entomopathogenic fungi in Atlantic forest soils. Microbiology discovery 4(1):1.
Nicoletti R, Becchimanzi A (2020) Endophytism of Lecanicillium and Akanthomyces. Agriculture 10:205. https://doi.org/10.3390/agriculture10060205
Nielsen C, Hajek AE, Humber RA, Bresciani J, Eilenberg J (2003) Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biocontrol 28(1):92–100. https://doi.org/10.1016/s1049-9644(03)00033-1
Olivares CM, López-Llorca LV (2002) Fungal egg-parasites of plant-parasitic nematodes from Spanish soils. Revista iberoamericana de micologia 19(2):104–110. https://www.reviberoammicol.com/2002-19/104110.pdf
Quesada‐Moraga E, González-Mas N, Yousef-Yousef M, Garrido‐Jurado I, Fernández‐Bravo M (2023) Key role of environmental competence in successful use of entomopathogenic fungi in microbial pest control. Journal of Pest Science 97:1–15 https://doi.org/10.1007/s10340-023-01622-8
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C (2007) Factors affecting the occurrence and distribution ofentomopathogenic fungi in natural and cultivated soils. Mycological research 111:947–966. https://doi.org/10.1016/j.mycres.2007.06.006
Ramanujam B, Balachander M, Roopa G, Rangeshwaran R, Karmakar P (2011) ITS sequencing of Indian isolates of Lecanicillium species. Journal of Biological Chemistry 25(4):337–341.
Rivas F, Núñez PI, Jackson TA, Altier N (2013) Effect of temperature and water activity on mycelia radial growth, conidial production and germination of Lecanicillium spp. isolates and their virulence against Trialeurodes vaporariorum on tomato plants. BioControl 59(1):99–109. https://doi.org/10.1007/s10526-013-9542-y
Scorsetti AC, Humber RA, García JJ, López-Lastra CC (2007) Natural occurrence of entomopathogenic fungi (Zygomycetes: Entomophthorales) of aphid (Hemiptera: Aphididae) pests of horticultural crops in Argentina. BioControl 52:641–655. https://doi.org/10.1007/s10526-006-9045-1
Sharma L, Oliveira I, Torres L, Marques G (2018) Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 38:1–23. https://doi.org/10.3897/mycokeys.38.26790
Soares F, Trovão J, Portugal A (2022) Phototrophic and fungal communities inhabiting the Roman cryptoporticus of the national museum Machado de Castro (UNESCO site, Coimbra, Portugal). World Journal of Microbiology and Biotechnology 38:157. https://doi.org/10.1007/s11274-022-03345-x
Sun, B, Yu H, Chen AJ, Liu X (2008) Insect-associated fungi in soils of field crops and orchards. Journal of Crop Protection 27(11):1421–1426. https://doi.org/10.1016/j.cropro.2008.07.010
Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57:5–59. https://doi.org/10.3114/sim.2007.57.01
Sung GH, Spatafora JW, Zare R, Hodge KT, Gams W (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae). Nova Hedwigia 72(3–4):311–328 https://doi.org/10.1127/nova.hedwigia/72/2001/311
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Villarreal-Ruiz L, Vasco-Palacios AM, Thu PQ, Suija A et al. (2014) Fungal biogeography. Global diversity and geography of soil fungi. Science 346(6213):1256688. https://doi.org/10.1126/science.1256688
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44(W1):W232–W235. https://doi.org/10.1093/nar/gkw256
Trovão J, Mesquita N, Paiva DS, Paiva de Carvalho H, Avelar L, Portugal A (2013) Can arthropods act as vectors of fungal dispersion in heritage collections? A case study on the archive of the University of Coimbra, Portugal. International biodeterioration & biodegradation 79:49–55. https://doi.org/10.1016/j.ibiod.2012.10.015
Uzman D, Pliester J, Leyer I, Entling MH, Reineke A (2019) Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils. Applied Soil Ecology 133:89–97. https://doi.org/10.1016/j.apsoil.2018.09.004
Wang Y, Wang Z, Luo R, Souvanhnachit S, Thanarut C, Dao V, Yu H (2024) Species diversity and major host–substrate associations of the genus Akanthomyces. Research Square https://doi.org/10.21203/rs.3.rs-2907259/v1
Zare R, Gams W (2001a) A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia 72:47–55. https://doi.org/10.1127/nova.hedwigia/72/2001/329
Zare R, Gams W (2001b) A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia 73:1–50.
Zare R, Gams W (2003a) Lecanicillium lecanii. IMI Descriptions of Fungi and Bacteria 1565:1–3. https://doi.org/10.1079/DFB/20056401565
Zare R, Gams W (2003b) Lecanicillium longisporum. IMI Descriptions of Fungi and Bacteria 1566:1–2. https://doi.org/10.1079/dfb/20056401566
Zare R, Gams W (2003c) Lecanicillium muscarium. IMI Descriptions of Fungi and Bacteria 1567:1–6. https://doi.org/10.1079/dfb/20056401567
Zare R, Gams W, Culham A (2000) A revision of Verticillium sect. Prostrata I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71(3–4):465–480. https://doi.org/10.1127/nova/71/2000/465
Zimmermann G (1986) The ‘Galleria bait method’ for detection of entomopathogenic fungi in soil. Journal of Applied Entomology 102(1–5):213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Paula Caride, Josefina Garrido, Mauro Rivas-Ferreiro, Iria Villar, Marisa Castro
This work is licensed under a Creative Commons Attribution 4.0 International License.
