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. 2026 Feb 9;82(5):4089–4103. doi: 10.1002/ps.70621

Lecanicillium aphanocladii : a biocontrol agent against insect pests and phytopathogens

Qianhe Liu 1,✉, Richard Johnson 1, Kwasi Adusei‐Fosu 1
PMCID: PMC13071199  PMID: 41664564

Abstract

Fungi in the genus Lecanicillium include a group of important entomopathogenic species affecting insect pests and phytopathogens. Lecanicillium aphanocladii, one of 21 recognised Lecanicillium species, has been recently reported as a potential biocontrol agent in agricultural and forestry ecosystems with more than 95 L. aphanocladii strains having been recorded globally. Lecanicillium aphanocladii is a cosmopolitan fungus capable of infecting a broad range of insects, plants and other fungal species. As interest grows in alternative environmentally sustainable insect and plant disease control tools, L. aphanocladii appears to be a promising biocontrol option for the agricultural industry. In this review, we highlight recent research findings on the potential of L. aphanocladii against insect pests and we provide insights into possible modes of action. Additionally, we review the parasitic nature of L. aphanocladii against plant diseases. © 2026 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Keywords: Lecanicillium spp., entomopathogenic fungi, plant protection, biological control agent

Recent research findings on the biocontrol potential of Lecanicillium aphanocladii fungus against insect‐pests and plant diseases were highlighted. This review indicates that several L. aphanocladii strains show great potential to be developed as multipurpose biocontrol agents active against several insect‐pests, plant diseases and plant parasitic nematodes.

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1. INTRODUCTION

Globally, crop losses caused by insect pests range from 18% to 26% of annual production, totalling US$470 billion per year. 1 , 2 The use of entomopathogens as biological control agents is becoming important, due to negative effects on the environment and non‐target organisms, including mammals, from synthetic chemicals currently used for insect pest control. 1 Additionally, there is an increasing prevalence of resistance of some pests to these synthetic chemicals and evidence of secondary pest resurgence.

Entomopathogenic fungi are widely used as biopesticides and are expected to have an increasing role in the future. Worldwide, it has been reported that over 700 fungal species belonging to approximately 90 genera are pathogenic to insects. 1 , 3 , 4 Mitosporic fungi such as Beauveria spp., Metarhizium spp., Lecanicillium spp., and Isaria spp. (previously Paecilomyces spp.) are well known entomopathogens that have been developed commercially as biopesticides. 5 , 6 , 7 , 8 , 9 The use and management of these pathogens as biological control agents has been the subject of several major reviews. 1 , 3 , 7 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20

Fungi in the genus Lecanicillium are a group of important insect pathogens. 6 Lecanicillium is in the order Hypocreales and is described as anamorphic Cordycipitaceae. Some Lecanicillium species are widely known entomopathogens, such as Lecanicillium lecanii (previously named Verticillium lecanii). There are up to 21 species currently described in the Lecanicillium genus, 21 including L. lecanii, Lecanicillium aphanocladii, Lecanicillium attenuatum, Lecanicillium longisporum, Lecanicillium muscarium, Lecanicillium nodulosum and Lecanicillium psalliotae. 22 These species have been isolated from various hosts exhibiting a wide host range 22 and have been comprehensively reviewed. 6 , 7 , 13 , 23 There are at least 26 products based upon Lecanicillium species or strains that have been, or are in the process of being developed commercially as biopesticides targeting a variety of pests across several countries. 6 , 7 , 24 , 25

Recently, the entomopathogenic fungus L. aphanocladii has been considered as a potential biocontrol agent for both agricultural and forestry ecosystems. To date, more than 95 L. aphanocladii strains are reported in either peer reviewed publications or in the National Centre for Biotechnology Information (NCBI) database (https://www.ncbi.nlm.nih.gov/), based upon GenBank sequencing data. Some strains are reported as control agents of plant pests and have activity against the horse‐chestnut leaf miner moth Cameraria ohridella and the lime leaf miner moth Phyllonorycter (Lithocolletis) issikii, 26 , 27 aphids Rhopalosiphum spp., 28 the flour moth Ephestia kuehniella, 29 and the meadow spittlebug Philaenus spumarius. 30 Lecanicillium aphanocladii is also a fungicolous species that feeds on Agaricus bisporus, Agaricus bitorquis, the powdery mildew Podosphaera (Erysiphe) fuliginea, Podosphaera pannosa, and the rusts Puccinia spp. and Uromyces savulescui. 31

Published evidence would suggest there is one registered product named L. aphanocladii‐Hu 1 that has been patented in China as a biocontrol agent against green peach aphid Myzus persicae (Sulzer) (CN119320701A 32 ). A product based on a fungus described as Aphanocladium album (Preuss) W. Gams MX95 was also claimed to be a biocontrol agent (patent MI2006A000503; also see D'Ambrosio et al. 33 ). However, molecular studies have shown that the Aphanocladium album MX95 is likely a strain of L. aphanocladii (see Section 3). Therefore, in this present review the former name, Aphanocladium album MX95, is referred to as L. aphanocladii MX95 to avoid confusion unless the name of Aphanocladium album is specified (e.g., in Figs 1 and 2).

Figure 1.

Figure 1

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A phylogenetic analysis of internal transcribed spacer (ITS) sequences of selected strains of Lecanicillium aphanocladii and Aphanocladium album. Sequences were trimmed to match ITS length of the Type strain of L. aphanocladii AJ292430 prior to producing the phylogenetic tree. The phylogenetic tree was created by Geneious Tree Builder using the Neighbour‐Joining tree building method and the Tamura‐Nei model.

Figure 2.

Figure 2

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Comparison of partial sequences of small‐subunit rRNA (SSU) (A) and large‐subunit rRNA (LSU) (B) in Aphanocladium album strain MX95 with those in known Lecanicillium aphanocladii strains. SSU and LSU sequences of Aphanocladium album MX95 and L. aphanocladii MBC 099 were extracted from genome assemblies of GCA_0.29218145 and GCA_030411675, respectively. The remaining sequences were selected from GenBank with the Accession numbers listed.

2. LITERATURE SEARCH APPROACH AND SOURCE OF INFORMATION

An analysis of publications and patents available from online platforms was performed using Google Scholar, Scopus, Web of Science, CAB abstracts, CABI Digital Library, PubMed, Food Science and Technology Abstracts, BIOSIS Previews, NCBI, and five patent search engines and databases including Google Patents, Lens, Espacenet, Patentscope, and the United States Patent and Trademark Office (USPTO). There were 11 keywords used for retrieving information ‘Lecanicillium spp.’, ‘Lecanicillium aphanocladii’, ‘L. aphanocladii’, ‘Aphanocladium album’, ‘A. album’, ‘MX95’, ‘MX‐95’, ‘Aphanocladium aranearum’, ‘Acremonium aranearum’, ‘A. aranearum’, and ‘entomopathogenic fungi’.

3. RENAMING OF APHANOCLADIUM ALBUM MX95

Lecanicillium aphanocladii was previously called Aphanocladium aranearum and Acremonium aranearum and was first described by Zare and Gams 22 as a fungicolous fungus. Historically, many L. aphanocladii strains had been misidentified as Aphanocladium album, 34 for example, strain ARSEF 6433 35 , 36 , 37 (see more misidentified strains at Table 1). The generic name Aphanocladium album is linked to Aphanocladium album sensu stricto, whose phylogenetic position is not yet resolved. 22 Generally, Aphanocladium album sensu stricto grows more slowly and is known only as a parasite of slime moulds, while L. aphanocladii grows rapidly 22 and most of its strains produce red pigments in agar. 22 , 68 The morphological and molecular characteristics of L. aphanocladii and Aphanocladium album have been documented. 22 , 30 , 31 , 76

Table 1.

Strains of Lecanicillium aphanocladii collected from NCBI GenBank and published articles. Same strains may vary in strain ID depending on the collection. ITS, SSU, LSU and Tef1α in National Centre for Biotechnology Information (NCBI) accession represent the gene sequences of internal transcribed spacer, small‐subunit rRNA, large‐subunit rRNA and translation elongation factor 1‐alpha, respectively.

Strain Name change NCBI accession Host/source Country Reference
Lecanicillium aphanocladii CEP556 Insect (Araneae spp.) Argentina 38
Lecanicillium aphanocladii Insect (Aphididae sp.) Iran 28
Lecanicillium aphanocladii MBC 100 GCA_030411675 Insect (Aphididae sp.) USA GenBank
Lecanicillium aphanocladii clone DP‐11LA KC574075_ITS Insect (Cameraria ohridella; Phyllonorycter issikii) Lithuania 26 , 27
Lecanicillium aphanocladii GMSL58A LT220793_Tef1α Insect (Galleria mellonella) Portugal GenBank
Lecanicillium aphanocladii DSF Insect (Philaenus spumarius) Italy 30
Lecanicillium aphanocladii OP321409_ITS Insect (Monochamus alternatus) China

39

Lecanicillium aphanocladii LPV‐3 KY433313_ITS Insect (Pseudips mexicanus) Mexico

40

Lecanicillium aphanocladii F28’ Insect (Ephestia kuehniella) Tunisian 29

Lecanicillium aphanocladii R801‐2

(IRAN‐3692 C)

 OR327068_ITS Insect (Tetranychus urtica) Iran 41
Lecanicillium aphanocladii Insect (Melolontha melolontha) Switzerland 42
Lecanicillium aphanocladii Cyst nematode (Globodera sp.) Iran 43
Lecanicillium aphanocladii AF15 PP380387_ITS Plant (Astragalus sp.) China 44
Lecanicillium aphanocladii CBS 274.76 Aphanocladium aranearum Aphanocladium album Plant (Abelmoschus esculentus) Bulgaria 22
Lecanicillium aphanocladii CBS 581.66 Aphanocladium album MH858887_ITS MH870552_LSU Plant (Acacia karroo) South Africa 22
Lecanicillium aphanocladii NW‐52 MG596648_ITS Plant (Anacardium occidentale nut) South Africa GenBank
Lecanicillium aphanocladii Aphanocladium aranearum Plant (Eusideroxylon zwageri) Malaysia 45
Lecanicillium aphanocladii Plant (Pinus greggii) Mexico 46
Lecanicillium aphanocladii Plant (Hordeum vulgare) Kazakhstan 47
Lecanicillium aphanocladii NWU12 MT079280_ITS Plant (Arachis hypogaea) South Africa 48
Lecanicillium aphanocladii NWUSeq12 MK841424_ITS Plant (Arachis hypogaea) South Africa GenBank
Lecanicillium aphanocladii BC stem cutting 2 MW130744_ITS Plant (Cannabis sativa stem) Canada GenBank
Lecanicillium aphanocladii stems MT311365_ITS Plant (Cannabis sativa stem) Canada GenBank
Lecanicillium aphanocladii PDD42022 Plant (Cyphomandra betacea) New Zealand Landcare Research
Lecanicillium aphanocladii IHEM:03304 OW983117_ITS Plant (Fagus sylvatica) Belgium GenBank
Lecanicillium aphanocladii IHEM:3234 OW983089_ITS Plant (Fagus sylvatica) Belgium GenBank
Lecanicillium aphanocladii FL17 KP689173‐ITS Plant (Huperzia serrata) China 49
Lecanicillium aphanocladii GL0836 JX241644_ITS Plant (Malus pumila) China 50
Lecanicillium aphanocladii FJTA KJ495738‐ITS Plant (Nicotiana tabacum) China GenBank
Lecanicillium aphanocladii FJTL KJ162356_ITS Plant (Nicotiana tabacum) China GenBank
Lecanicillium aphanocladii FF31 KR912316_ITS Plant (Pyrus communis fruit) South Africa GenBank
Lecanicillium aphanocladii MX95 Aphanocladium album MX95 GCA_029218145 Plant (Solanum melongena) Italia GenBank
Lecanicillium aphanocladii IT45 OR131317_ITS OR131325_SSU OR131326_LSU Plant (Solanum torvum seed) Italy GenBank
Lecanicillium aphanocladii SGP‐4 Plant (Morus alba) China 51
Lecanicillium aphanocladii N11 MK304173_ITS Plant endophyte (Ageratina adenophora) China GenBank
Lecanicillium aphanocladii KH24 MH594215_ITS Plant endophyte (Hemidesmus indicus) India 52
Lecanicillium aphanocladii N15 MK304090_ITS Plant endophyte (Ageratina adenophora) China GenBank
Lecanicillium aphanocladii N63 MK304418_ITS Plant endophyte (Ageratina adenophora) China GenBank
Lecanicillium aphanocladii FS13 KP689216_ITS Plant endophyte (Huperzia serrata) China 49
Lecanicillium aphanocladii BLH_238 OM436882_ITS Plant endophyte (Macleaya cordata) China GenBank
Lecanicillium aphanocladii EF‐WCH‐51 OQ806916_ITS OQ807035_SSU OQ807036_LSU OQ857508_Tef1α Plant endophyte (Magnolia denudata cv. Hailuo) China 53
Lecanicillium aphanocladii AAH4‐1 OQ162343_ITS Plant endophyte (Physalis peruviana seed) Iran GenBank
Lecanicillium aphanocladii Plant endophyte (Picea mariana) Canada 54
Lecanicillium aphanocladii BCR‐427 Aphanocladium aranearum ON740940_ITS Plant endophyte (Bupleurum chinense) China 55
Lecanicillium aphanocladii voucher EXF‐2447 Plant endophyte (Zea mays W22 seed) Slovenia 56
Lecanicillium aphanocladii PDD42012 Fungi (Altenaria tenius) New Zealand Landcare Research
Lecanicillium aphanocladii CBS 376.77 Aphanocladium aranearum AJ292431 _ITS Mushroom fungi (Agaricus bitorquis) The Netherlands 30
Lecanicillium aphanocladii CBS 774.83 Aphanocladium album Mushroom fungi (Agaricus bitorquis) Unknown 22
Lecanicillium aphanocladii CBS 797.84 Aphanocladium aranearum Aphanocladium album KM283763_SSU KM283787_LSU KM283811_Tef1α Mushroom fungi (Agaricus bitorquis) China 22
Lecanicillium aphanocladii CBS 798.84 Aphanocladium aranearum Aphanocladium album Mushroom fungi (Agaricus bitorquis) China 22
Lecanicillium aphanocladii CBS 101286 Aphanocladium aranearum IMI 96000b Verticillium psalliotae AJ292430_ITS Mushroom fungi (Agaricus bitorquis) UK GenBank
Lecanicillium aphanocladii G1 OL629617‐ITS Mushroom fungi (Morchella spp.) China 57
Lecanicillium aphanocladii JAUCC5994 OR225843_ITS OR333513_LSU Mushroom fungi (Schizophyllum commune) China 58
Lecanicillium aphanocladii KX530079_ITS Mushrrom fungi (Tremella fuciformis) China 59
Lecanicillium aphanocladii Bx‐Ljb OR077442_ITS OR206377_SSU OR206378_LSU OR204702_Tef1α Mushroom fungi (Sparassis latifolia) China 60
Lecanicillium aphanocladii GMSL01 LT220701_ITS LT220793_Tef1α Vineyard soil Portugal 61
Lecanicillium aphanocladii GMSL02 LT220702_ITS Vineyard soil Portugal 61
Lecanicillium aphanocladii GZUIFR‐lun1505 MN944423_ITS MN963920_SSU Forest soil China 62
Lecanicillium aphanocladii ZNF15 OP379501_ITS Rhizosphere soil of Astragalus forrestii China 63
Lecanicillium aphanocladii GZUIFR.SP477 KX021371_ITS Wheat soil China GenBank
Lecanicillium aphanocladii CML2970 Cave soil Brazil 64
Lecanicillium aphanocladii CML2971 Soil Iraq 65
Lecanicillium aphanocladii MUT<ITA>:242 MG593981_ITS Oil contaminated soil Russia 66 , 67
Lecanicillium aphanocladii YARK7 OP020444_ITS Soil and water Iraq GenBank
Lecanicillium aphanocladii IFM 64743 LC553279_ITS LC553289_SSU LC553284_LSU LC553294_Tef1α Tengu‐no‐Mugimeshi soil Japan 68
Lecanicillium aphanocladii fki‐9593 Tengu‐no‐Mugimeshi soil Japan 69
Lecanicillium aphanocladii IHEM:26758 OW985864_ITS Environment (rubber carpet) Belgium GenBank
Lecanicillium aphanocladii 170915GAR11K1 MW826143_ITS Environment (air) Spain 70
Lecanicillium aphanocladii voucher CML 2970 KR261451_ITS Environment (air) Brazil 71
Lecanicillium aphanocladii sample759 LC745692_ITS Environment (house dust) Japan GenBank
Lecanicillium aphanocladii KBP F‐23 PQ606631_ITS Environment (indoor air) Russia GenBank
Lecanicillium aphanocladii IHEM:03485 OW983161_ITS Environment (indoor air) Belgium GenBank
Lecanicillium aphanocladii QH69 JF911775_ITS Environment (lake water) China GenBank
Lecanicillium aphanocladii GS73 MN511328_ITS Environment (sawdust) South Korea GenBank
Lecanicillium aphanocladii BN35 MH484024_ITS Envrionment (air) China GenBank
Lecanicillium aphanocladii Z06 KT189155_ITS Envrionment (crude oil and wax) China GenBank
Lecanicillium aphanocladii NNIBRFG2172 OK090967_ITS OK090991_LSU OK235317_Tef1α Envrionment (freshwater foam) South Korea 72
Lecanicillium aphanocladii IHEM:28037 OU989389_ITS Bat fur (Plecotus auritus) Belgium GenBank
Lecanicillium aphanocladii AUMC11913 Contaminated potato dextrose agar (PDA) plate Egypt 73
Lecanicillium aphanocladii wb293 Aphanocladium aranearum AF455489_ITS Human patients Austria 74
Lecanicillium aphanocladii wb578 Aphanocladium aranearum AF455405_ITS Human patients Austria 74
Lecanicillium aphanocladii Tr247 PP564874_ITS PP729101_Tef1α Human patients Turkey Genbank
Lecanicillium aphanocladii D05 MH346472_ITS Human patients Brazil 75
Lecanicillium aphanocladii IHEM:19176 OW987919_ITS Human patients Belgium GenBank
Lecanicillium aphanocladii CBS 165.45 Aphanocladium aranerum Aphanocladium album The Netherlands 22
Lecanicillium aphanocladii CBS 458.82 Aphanocladium album Not reported South Africa 22
Lecanicillium aphanocladii ARSEF 6433 Aphanocladium album Not reported 35 , 36 , 37
Lecanicillium aphanocladii SJL10.5–3 PP467451 Not reported China GenBank
Lecanicillium aphanocladii HBU‐2019‐225 ON077432_ITS Not reported China GenBank
Lecanicillium aphanocladii MB#144303 Aphanocladium aranearum Not reported 73
Lecanicillium aphanocladii MB#308804 Aphanocladium aranearum Not reported 73
Lecanicillium aphanocladii N14 Not reported GenBank
Lecanicillium aphanocladii BEOFB4710m OL336789_ITS Not reported Serbia GenBank
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The formerly named Aphanocladium album MX95 is a known parasite of phytopathogenic fungi and has been extensively studied as a possible agent for plant protection (patent MI2006A000503). Nevertheless, the species identity of MX95 is not clearly defined. As such, we conducted a sequence comparison for some key genes to determine the species identity of MX95. In 2023, a complete genome sequence of MX95 was published in GenBank (Accession GCA_029218145.1; University of Milan, Italy). Similarly, in the same year a genome assembly for L. aphanocladii strain MBC 099 was also published by USDA‐ARS‐NCAUR (GenBank Accession GCA_030411675.1). MX95 was initially isolated from eggplant in Italy and seems to have been reported first by Ciccarese et al., 77 whereas L. aphanocladii MBC 099 was isolated from an aphid in France. To compare these two fungal strains we extracted equivalent sequences from the available genomes of fungal strains of MX95 and L. aphanocladii MBC 099. The hypothetical non‐ribosomal peptide synthetase (NRPS) gene (GenBank Accession KAJ6780765) and the internal transcribed spacer (ITS), small‐subunit rRNA (SSU) and large‐subunit rRNA (LSU) sequences were the primary focus of analysis. The similarity of the NRPS gene sequence within MX95 and L. aphanocladii MBC 099 was compared. The equivalent ITS, SSU and LSU sequences from these two strains were also compared with other strains of Aphanocladium album and L. aphanocladii selected from GenBank.

Phylogenetic analysis of ITS sequences (Fig. 1) showed that MX95 was in the same clade as L. aphanocladii CBS101286 (GenBank Accession AJ292430) but was in a different clade to the Aphanocladium album strain CBS 401.70 (GenBank Accession AJ292401). There were similarities among sequences of MX95 and L. aphanocladii in the SSU (Fig. 2(A)) and LSU (Fig. 2(B)) genes. The SSU sequence of strain MX95 showed higher similarity with known L. aphanocladii strains, such as CBS797.84 and MBC 009 with GenBank Accessions KM283763 and GCA_030411675.1, respectively, but was dissimilar to Aphanocladium album CBS401.70 with GenBank Accession AF339568 (Fig. 2(A)). For the LSU region comparisons, strain MX95 showed 100% similarity with sequences of L. aphanocladii strains MBC 099 (GenBank Accession GCA_030411675.1), CBS797.84 (GenBank Accession KM283787), IFM64743 (GenBank Accession LC553284) and Bx‐Ljb (GenBank Accession OR206378), among others. However, it was distinct from Aphanocladium album strain CBS411.34 with GenBank Accession MH867096 at the C‐terminal region (Fig. 2(B)). Most interestingly, the hypothetical NRPS protein in MX95 (KAJ6780765), which codes 6958 amino acids (20 877 bp nucleotides), showed > 98% similarity to the NRPS protein of L. aphanocladii MBC 099 (contig JAPERO010000154 of genome GCA_030411675), for both amino acid and nucleotide sequences.

This molecular evidence suggests that MX95 is likely to be a strain of L. aphanocladii. Therefore, the current species designation of MX95 as Aphanocladium album is probably incorrect. The strain MX95 has been studied extensively in previous research which suggests that L. aphanocladii strains are likely to be effective against several plant diseases and plant parasitic nematodes (see more discussions later).

4. GEO‐DISTRIBUTION AND HOST DIVERSITY OF L. APHANOCLADII

Lecanicillium aphanocladii is a cosmopolitan fungus and is widely distributed across Asia, Europe, Africa and the Americas (Table 1). This fungus has been reported to be vulnerable to heat, with conidia failing to germinate at 45 °C, 35 and sensitive to ultraviolet (UV) light as it exhibits lower tolerance to UV‐B radiation compared to other entomopathogenic fungi such as Metarhizium anisopliae. 35 , 37 , 78 , 79

The wide host range of L. aphanocladii includes insects in the orders Hemiptera, Lepidoptera and Coleoptera. Lecanicillium aphanocladii has also been reported in association with mosquitoes (Culicidae), 80 greenhouse whitefly Trialeurodes vaporariorum, 81 silkworm Bombyx mori, 82 lace bug Leptopharsa heveae, 36 aphids Rhopalosiphum spp., 28 cyst nematodes Globodera spp., 43 spider Stenoterommata platensis, 38 cockchafer beetle Melolontha melolontha, 42 tobacco moth Ephestia elutella, 62 flour moth Ephestia kuehniella, 29 meadow spittlebug Philaenus spumarius, 22 western flower thrips Frankliniella occidentalis, 83 pine bark beetle Pseudips mexicanus, 40 horse‐chestnut leaf miner Cameraria ohridella and lime leaf miner Phyllonorycter (Lithocolletis) issikii, 26 , 27 and pine sawyer beetle Monochamus alternatus. 39 This demonstrates that L. aphanocladii infects a broad range of insect hosts.

About 36% of all the reported strains of L. aphanocladii in Table 1 were isolated from plants. These host plants of L. aphanocladii range from agricultural to forest species. Several L. aphanocladii isolates from plant hosts were reported as endophytes that caused no visible disease, for example, Hemidesmus indicus, 52 Huperzia serrata, 49 Ageratina adenophora (NCBI submission), Magnolia denudata cv. Hailuo, 53 Bupleurum chinense, 55 Picea mariana 54 and Zea mays 56 (Table 1). Research on endophyte–insect–plant interactions is critical to advance our knowledge of entomopathogenic fungi as a sustainable pest management approach. 84 Further exploration and characterisation of a wider range of endophytic L. aphanocladii, particularly those with potent entomopathogenic properties against important agricultural pests and diseases, are required in future studies.

There are several reports that L. aphanocladii has been isolated from different species of mushrooms (Table 1), causing diseases such as cobweb and spotting diseases in Agaricus bisporus in Europe, 30 as well as recently reported cobweb disease in Schizophyllum commune, 58 and rot diseases in Sparassis latifolia, 60 Tremella fuciformis, 59 and Morchella sextelata 85 in China. Lecanicillium aphanocladii is also a fungicolous species that associates with Agaricus bitorquis, Podosphaera (Erysiphe) fuliginea, Podosphaera pannosa, Uromyces savulescui, 31 Puccinia spp, 86 , 87 and Altenaria tenius (PDD 42012, NZFungi database, Landcare Research, New Zealand).

Lecanicillium aphanocladii has also been isolated from soil samples (11%; Table 1), environmental materials (12%) and other types of specimens (18%), including unknown sources. Notably, a few strains have been isolated from human nasal mucus, 74 a dermatophyte infection, 75 and bat fur (GenBank Accession OU989389). While fungi, in general, can be opportunistic pathogens in severely immunocompromised humans, due to its specific entomopathogenic characteristics L. aphanocladii is considered to have low or negligible infection risk to mammals and humans. Related species such as L. lecanii are considered safe to humans and non‐target organisms, and have a favourable environmental risk profile. 88

5. BIOPESTICIDE ACTIVITY OF L. APHANOCLADII

Several L. aphanocladii strains have been reported to be active against a range of insect pest species, including aphids that cause damage in many agricultural crops. 89 , 90 For instance, the corn leaf aphid (Rhopalosiphum maidis) is a common pest of maize and other related crops globally. 91 Different species of entomopathogenic fungi from the phyla Ascomycota and Entomophthoromycota are associated with aphids, but only a few of these are specific for aphids. 28 Lecanicillium aphanocladii is one of the most important hypocrealean pathogens of aphids. In a glasshouse trial studying barley yellow dwarf virus on cereal crops in Iran, Zare and Mohammad 28 observed that aphids of Rhopalosiphum maidis, Rhopalosiphum padi, Schizaphis graminum and Sitobion avenae were heavily colonised by L. aphanocladii, leading to mortality in 7–10 days. Lecanicillium aphanocladii‐Hu 1 has also been patented as a biocontrol agent against green peach aphid Myzus persicae (Sulzer) (Patent CN119320701A 32 ) in China. The high pathogenicity of L. aphanocladii to aphids makes it a potential biological control agent to prevent transmission and dispersal of plant‐pathogenic viruses. 28 Studies on other species of Lecanicillium, such as L. attenuatum, L. lecanii, and L. longisporum, have also demonstrated high efficacy against different aphid species. 6 , 90

Furthermore, the leaf miner moths Cameraria ohridella and Phyllonorycter (Lithocolletis) issikii are pests of horse chestnut (Aesculus hippocastanum) and small‐leaved linden (Tilia cordata) in Lithuania. Lecanicillium aphanocladii was reported to be the most common species recovered from larval cadavers of the leaf miners, with infection frequency ranging from 30% to 42% for Cameraria ohridella and Phyllonorycter issikii, respectively. 26 , 27 The L. aphanocladii isolates showed high pathogenicity in a comparative laboratory bioassay by Nedveckytė et al. 26 Indeed, L. aphanocladii was the most virulent fungal species against Cameraria ohridella, causing 77% mortality in eggs, which was 1.8‐, 2.0‐, and 2.8‐fold higher than Beauveria bassiana, Isaria fumosorosea or L. psalliotae, respectively. Nedveckytė et al. 26 reported that L. aphanocladii was associated with horse chestnut foliage and showed that it was common on leaf surfaces with powdery mildew disease (Erysiphe flexuosa).

Lecanicillium aphanocladii strain F28’ was found in association with insect pests of olive trees (Olea europaea), 29 isolated from olive fly (Bactrocera oleae) as well as from olive psyllid (Euphyllura olivine) cadavers collected from Tunisian olive groves. Strain F28’ was found to be highly pathogenic to Ephestia kuehniella (Mediterranean flour moth) fourth‐instar larvae resulting in 93% mortality. In addition, L. aphanocladii F28’ displayed no phytopathogenic activity against excised olive shoots at 28 days post‐inoculation. 29

Bodino et al. 92 isolated L. aphanocladii and three other entomopathogenic species, Beauveria bassiana, Conidiobolus coronatus and Fusarium equiseti from dead spittlebug (Philaenus spumarius), the key vector of Xylella fastidiosa a plant pathogen transmitted by Philaenus spumarius in Europe. 93 , 94 Subsequent studies showed that a blastospore formulation of L. aphanocladii was lethal to spittlebug nymphs (90% mortality) and also reduced adult emergence with an efficacy that was similar to a commercial insecticide based on Beauveria bassiana, Naturalis®. 92 Zhou et al. 62 applied conidial suspensions of L. aphanocladii GzuiFr‐lun1505 isolated from forest rhizosphere soil in China. Conidia were lethal to third‐instar larvae of the tobacco moth Ephestia elutella with recorded 78% mortality, which was similar to the mortality caused by Isaria cateinannulata (79%) and Beauveria bassiana (65%). Rangel and Correia 36 compared the virulence of L. aphanocladii (ARSEF 6433) with L. (Verticillium) lecani (ARSEF 6430, 6431 and 6432) on a rubber tree pest, lace bug (Leptopharsa heveae) third‐ and fifth‐instar nymphs and adults by applying conidial suspensions, at concentrations of 2.4 × 105–2.4 × 107 conidia per mL. At the highest concentrations L. aphanocladii ARSEF 6433, L. lecani ARSEF 6430 and 6432 showed median lethal time (LT50) values of 2.6, 2.6 and 3.2 days, respectively. Although L. aphanocladii shows good pathogenicity against a range of pests its bioactivity is sometimes lower than some other Lecanicillium species. For example, mortality to Western flower thrips (Frankliniella occidentalis), a pest of numerous crops, was lower than species of L. attenuatum, Lecanicillium cauligalbarum and Lecanicillium araneogenum, 83 indicating that the pathogenicity of L. aphanocladii differs depending on the target pest.

There are some more recently identified hosts of L. aphanocladii such as Pseudips mexicanus (tree bark beetle), 40 Melolontha melolontha larvae (cockchafer beetle) 42 and Monochamus alternatus (pine sawyer beetle), 39 which need to be further studied to understand the impact of L. aphanocladii on coleopteran pests.

6. FUNGICIDAL AND NEMATICIDAL ACTIVITY OF L. APHANOCLADII

Generally, the bioactivity of biological control agents comes in different forms where they act as antagonists against a variety of organisms, including nematodes, fungi and bacteria. Lecanicillium aphanocladii is known as a fungicolous species attacking Podosphaera fuliginea and Podosphaera pannosa, 28 Puccinia spp., 95 and Limonium rust. 96 Earlier studies on L. aphanocladii strains against those pathogenic fungi have been reviewed. 28 , 31 The use of L. aphanocladii as a biocontrol agent against phytopathogenic fungi and phytoparasitic nematodes has been applied practically, 97 , 98 however most studies have focused on strain MX95 (under the name Aphanocladium album) (as discussed later). Studies on other L. aphanocladii strains that have activity against phytopathogens are needed in the future, particularly the strains that show pesticidal activity. There are only two reports of L. aphanocladii being antagonistic against bacteria. 44 , 68 Higo et al. 68 reported that L. aphanocladii (FKI‐9593 = IFM 64743) had weak antibacterial activity against Proteus vulgaris NBRC 3167 and Zhou et al. 44 showed that the ethyl acetate extract from L. aphanocladii AF15 was active against Gram‐positive pathogenic bacteria, including methicillin‐resistant Staphylococcus aureus, Staphylococcus epidermidis, vancomycin‐resistant Enterococcus faecalis and Streptococcus agalactiae. In addition, it has been reported that Bacillus subtilis A9 from morel mushroom (Morchella esculenta) 57 and Pantoea spp. from maize kernels 56 have antagonistic effects on L. aphanocladii.

The L. aphanocladii MX95 was able to inhibit the growth and sporulation of several foliar pathogens including powdery mildew and rust and some soil‐borne plant pathogens, such as nematodes. 33 , 87 , 98 , 99 , 100 MX95 was also a potential biological limiter of the Esca and root rot fungi in grapevine. 98 An in vitro anti‐fungal test showed that MX95 effectively prevented mycelia and conidia spread from colonising pathogenic Fomitiporia mediterranea, Phaeoacremonium minimum and Phaeomoniella chlamydospora on detached grapevine canes. MX95 also controlled postharvest rot diseases of grape preharvest and postharvest, 101 , 102 and demonstrated some suppression against Golovinomyces lycopersici, the causal agent of powdery mildew in tomato and squash, and Podosphaera fusca causing powdery mildew in cucumber. 77 , 103 In tomato, MX95 was reported to limit corky root disease caused by Pseudopyrenochaeta lycopersici. 100 , 104 Others applied MX95 to soil by sub‐surface irrigation to reduce the severity of corky root in tomato, whereas applications to eggplants reduced wilting and vascular discoloration caused by Verticillium dahlia. 105 When MX95 was applied to melon plots, fusarium wilt was significantly reduced, compared to plots treated with the chemical fumigant Dazomet. 106 A recent study showed that in laboratory dual culture tests, MX95 completely suppressed growth of the pathogenic fungi Phytophthora nicotianae and Sclerotinia minor, and reduced the mycelial growth of Fusarium solani and Sclerotinia sclerotiorum by 40% and 20%, respectively. 33 Research has also shown that the application of MX95 significantly increased rhizosphere microbial populations in tomato plants. 97 , 99

The potential nematocidal activity of MX95 against the root‐knot nematode Meloidogyne spp. in infected plants was investigated. 97 , 99 , 101 , 107 The MX95 treatments, applied by sub‐surface irrigation were simultaneously effective against the soil borne pathogen Pseudopyrenochaeta lycopersici and the root‐knot nematode Meloidogyne incognita. 107 MX95 decreased root gall formation by Meloidogyne javanica in infected tomato plants. 99 The MX95 treatment effects on the rhizosphere microbiome were also analysed by a metabarcoding procedure, which revealed that MX95 significantly decreased root gall severity index and soil nematode population of Meloidogyne javanica. 97 This research suggested that MX95 has strong potential as a bionematicide, although no significant effects on Meloidogyne javanica were reported for other L. aphanocladii strains. 108

7. BIO‐INSECTICIDAL AND BIO‐FUNGICIDAL METABOLITES OF L. APHANOCLADII

The efficacy of L. aphanocladii MX95 against phytopathogens and nematodes may be linked to the production of hydrolytic enzymes such as proteases, glucanases, and several chitinases involved in the cell wall degradation of fungal phytopathogens. 97 Secretion of chitinase A by MX95 was identified as an extracellular, chitin‐inducible enzyme that is essential for its fungicidal activity. 97 The in silico functional annotation of the genome of MX95 allowed the identification of 46 genes encoding chitinolytic enzymes of the GH18 (26 genes), GH20 (eight genes), GH75 (eight genes), and GH3 (four genes) families. 97 These enzymes have either endochitinase or exochitinase activity and play a diversity of roles including interactions with other fungi, the degradation of exogenous chitin for nutrient acquisition, cell wall remodelling, and hyphal growth. 97 , 109 Chitinolytic enzymes are responsible for the total or partial disruption of the cell walls of many phytopathogenic fungi and parasites 97 , 110 and are also necessary for hyphal penetration of the cuticle of insects, nematodes or spiders. 17 , 111 , 112 Other enzyme complexes, such as proteases and β‐glucanases, have similar roles. 17 , 113 , 114 , 115

The production of secondary metabolites by entomopathogenic fungi is critical for pathogenicity and disease development in host insects. For instance, bassianolides from Beauveria bassiana and destruxins from Metarhizium spp. contribute to the biocontrol of pests and pathogenic fungi. 116 , 117 , 118 , 119 , 120 , 121 , 122 , 123 , 124 , 125 However, the roles of secondary metabolites as virulence factors expressed by L. aphanocladii against insect pests are poorly understood. Destruxins are among the most exhaustively researched secondary metabolites of entomopathogenic fungi and have been shown to have both insecticidal and phytotoxic activities. 3 , 120 , 121 , 122 , 123 Most destruxins and their analogues have been isolated from cultures of Metarhizium spp. but are less documented in other fungi, 124 although some derivatives of destruxins have been extracted from Beauveria felina, Alternaria brassicae and Nigrosabulum globosum. 3 , 120 , 125 The presence of destruxin‐like compounds has also been identified from L. longisporum, in which these metabolites were present at significantly higher concentration in stirred aerated cultures compared with static cultures. 124

Lecanicillium aphanocladii has been shown to contain a hypothetical NRPS protein (GenBank Accession KAJ6780765 in strain MX95), which has sequence similarities with destruxin synthetases from various other fungi, particularly Metarhizium species (Table 2), suggesting that L. aphanocladii might have the potential to synthesise destruxin‐like compounds. Repeated extraction and analysis of destruxins from L. longisporum indicated that the production of destruxins was more variable compared to the production by Metarhizium spp., indicating that additional factors probably influence destruxin synthesis. 124

Table 2.

Results of BLASTp search for hypothetical protein of Accession KAJ6780765 (Lecanicillium aphanocladii strain MX95) in National Centre for Biotechnology Information (NCBI) GenBank

Description Scientific name Maximum score Total score Query cover E Value † Per Ident ‡ Acc Len § Accession
Destruxin synthetase Pyrenophora teres f. teres 5447 23 267 100% <1e‐100 42.25 9097 CAE7020799.1
Destruxin synthetase Pyrenophora teres f. teres 4497 15 594 99% <1e‐100 41.82 5906 CAE7021457.1
Destruxins‐like synthetase Tolypocladium ophioglossoides 3518 12 112 100% <1e‐100 37.87 8012 KND86507.1
Destruxins synthetase Metarhizium anisopliae 3457 11 836 100% <1e‐100 37.49 7844 KAK8912138.1
Destruxin synthetase Metarhizium robertsii 3451 12 692 100% <1e‐100 37.43 7913 XP_007826232.2
Destruxin synthetase Metarhizium hybridum 3448 12 640 100% <1e‐100 37.44 7912 KID59658.1
Destruxin synthetase Metarhizium anisopliae 3447 12 613 100% <1e‐100 37.44 7894 KFG77713.1
Destruxin synthetase Metarhizium brunneum 3443 12 641 100% <1e‐100 37.39 7888 XP_065987973.1
Destruxin synthetase Metarhizium brunneum 3442 12 639 100% <1e‐100 37.39 7912 KID61226.1
Destruxins synthetase Beauveria felina 3440 14 675 100% <1e‐100 37.19 8002 QTW21125.1
Destruxin synthetase Metarhizium guizhouense 3436 12 683 100% <1e‐100 37.29 7910 KID82708.1
Destruxin synthetase Metarhizium brunneum 3414 12 579 100% <1e‐100 37.18 7887 KAK9446167.1
Destruxin synthetase Metarhizium anisopliae 3413 12 545 100% <1e‐100 37.17 7907 KAF5121803.1
Destruxin synthetase Cladobotryum mycophilum 3359 13 243 100% <1e‐100 41.03 7989 KAK5991451.1
Destruxin synthetase Metarhizium majus 3251 12 272 100% <1e‐100 39.99 7904 KID94891.1
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†

The E values calculated by BLASTp fall below the display threshold. We use ‘<1e‐100’ to replace value of ‘0’ that was generated by BLASTp.

‡

Percentage identity.

§

Accession length.

Other pigment‐based compounds such as oosporein, orevactaene and dihydrotrichodimerol have been identified in extracts of L. aphanocladii (CML2970). 71 The polyketide metabolite oosporein was also identified from L. aphanocladii strain FKI‐9593 (=IFM 64743). 69 These results suggest that certain strains of L. aphanocladii might serve as novel sources of pigments that could have industrial and biological applications. Oosporein has antifungal activities, 71 , 126 including against Phytophthora infestans, 127 Rhizoctonia solani, Botrytis cinerea and Pythium ultimum, and is reported to inhibit the proliferation of tumour cell lines. 128 Dihydrotrichodimerol reduces feeding in the aphid Schizaphis graminum, one of the most important pests of cereal crops, suggesting possible applications in the control of this pest. 129 In addition, water soluble secondary metabolites synthesised by L. aphanocladii (CML2970) have been reported to be effective in inhibiting snake venom‐induced proteolysis and phospholipase A2 activity, which may be of use in the development of pharmaceuticals of medical interest. 64 Several structurally characterised secondary metabolites from Lecanicillium spp. have been reported including indolosesquiterpenoids, 130 phenopicolinic acid analogues, 131 tetracyclic diterpenoid, 132 pregnanes, 133 cyclic lipodepsipeptides, 134 and lecanicillolide 49 , 135 along with several related compounds, spiciferone, 136 dihydrospiciferone 137 and butoxyl‐spiciferin. 138 These compounds are primarily of interest in biomedical research and drug discovery, especially for their potential anti‐cancer, anti‐inflammatory, and antimicrobial activities. However, these metabolites have not been reported in L. aphanocladii.

8. SUMMARY

Entomopathogenic fungi hold immense potential as biological control agents against insect pests of important agricultural and horticultural crops. The unexplored diversity of entomopathogenic fungi underscores the need for continued bioprospecting and evaluation of novel strains. This review indicates that several L. aphanocladii strains have great potential to be developed as multipurpose biocontrol agents that are active against several insect pests, plant diseases and plant parasitic nematodes. Developing commercial biocontrol agents based on L. aphanocladii would provide eco‐friendly products that could safeguard agricultural production amidst regulatory pressures to reduce synthetic pesticide use. However, some considerations for future studies remain.

The virulence of L. aphanocladii against insect pests has largely been characterised under laboratory conditions with limited field trials. This significantly restricts the broader application of this entomopathogen in pest control. Further studies on fungal application and field efficacy in the natural environment are required. Under field conditions, fungal biopesticides are usually applied using an inundative approach, which often involves exposure of the fungal conidia to unfavourable humidity, temperature and solar radiation conditions. These abiotic factors reduce the persistence and efficacy of fungal products. Formulation technologies and the application of L. aphanocladii need to be considered which maximise biocontrol efficacy by increasing the field persistence, improve shelf life, facilitate product application and increase the virulence of these pathogens.

For L. aphanocladii, some difficulties may occur during mass conidia production in vitro and when considering the stability of propagules for storage and formulation. Mass production methods and advances in the formulation of microbial insecticides have been reviewed previously. 139 , 140 Large scale applications of blastospores in aqueous suspensions have been used for Beauveria brongniartii against European cockchafer, Melolontha melolontha. 141 Successful inoculation of fungal blastospores on plant seeds to produce mycelium and aerial conidia against insect pests has also been reported in other entomopathogenic fungi, such as Beauveria brongniartii on barley seeds. 141 These techniques may be applicable to L. aphanocladii. Development of fungal consortia using combined L. aphanocladii strains against various insect pests and phytopathogens may favour the creation of products with a wider spectrum of action than individual strains. Continued exploration and characterisation of a wider range of endophytic L. aphanocladii, particularly those with potent entomopathogenic properties, is another important objective worth pursuing in future studies. In addition to insect pest control, the ability of endophytic L. aphanocladii to colonise plants will add a new dimension to its utilisation as a biological agent.

Genetic manipulation of biocontrol fungal agents is technically feasible and could provide useful strategies to either increase fungal virulence or enhance resistance to different stress factors. Increases in the pathogenicity of some entomopathogenic fungi has been achieved through genetic interventions involving the incorporation of genes encoding neurotoxic peptides, proteases, antimicrobial peptides, chitinases for cuticle degradation, and peptides that influence insect physiology. 142 Nevertheless, widespread adoption is currently limited by strict and comprehensive regulatory frameworks, which are driven by safety concerns, potential ecological risks, and public perception issues.

The secondary metabolites from entomopathogenic fungi represent an additional aspect of their biocontrol potential and pest control efficacy. However, the roles of secondary metabolites produced by L. aphanocladii are poorly understood. A deeper understanding of the range of compounds produced and their biosynthetic pathways are likely to provide insights into their interactions with insects, plant pathogens and crop plants. In summary, evidence suggests that developing cost‐effective fit‐for‐purpose biological control agents from L. aphanocladii could lead to effective replacements for current synthetic chemical control options with numerous potential benefits for modern agricultural production.

AUTHOR CONTRIBUTIONS

Qianhe Liu: writing – original draft, writing – review and editing. Richard Johnson: writing – review and editing. Kwasi Adusei‐Fosu: writing – review and editing.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest to disclose.

ACKNOWLEDGEMENTS

The authors thank Karoline Arfmann, Thomas Walker, Sandeep Kumar and Gayathri Vaidyanathan (AgResearch Group, Bioeconomy Science Institute, Grasslands Research Centre, New Zealand) for their support, and Wayne Simpson, Daniel Bastias and the Grasslanz Technology Ltd management team, particularly John Caradus, and external referees including Pest Management Science journal editors for reviewing earlier versions of the manuscript. The authors acknowledge the research support provided by AgResearch Group, Bioeconomy Science Institute. Open access publishing facilitated by Bioeconomy Science Institute, as part of the Wiley ‐ Bioeconomy Science Institute agreement via the Council of Australasian University Librarians

DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were created in this study.

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