Entomopathogenic fungus

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Entomopathogenic fungi are parasitic unicellular or multicellular microorganisms belonging to the kingdom of Fungi, that can infect and seriously disable or kill insects.

Contents

Pathogenicity for insects is widely distributed in the kingdom of fungi and occur in six fungal phyla (Ascomycota, Oomycetes, Basidiomycota, Chytridiomycota, Zygomycota, and Microsporidia). [1] It plays a vital ecological role in controlling insect populations by impacting 19 out of 30 known insect orders. [1] [2] Some fungal entomopathogens are opportunistic whereas some have evolved into highly specific pathogens of insects. [1]

Mode of infection

Unlike many other insect pathogens (entomopathogenic viruses, nematodes, or bacteria), most entomopathogenic fungi do not require entry through ingestion or oral intake and instead directly attack the insect cuticle and penetrate the insect body through the exoskeleton. [3] These fungi use a broad spectrum of virulence factors such as adhesins (to attach to insect cuticles), lytic enzymes (to hydrolyze insect cuticles), and secondary metabolites. [4]

Typical life cycle and general biology

Green peach aphid, Myzus persicae, killed by the fungus Pandora neoaphidis (Zygomycota: Entomophthorales) Scale bar = 0.3 mm Pandora neoaphidis.jpg
Green peach aphid, Myzus persicae, killed by the fungus Pandora neoaphidis (Zygomycota: Entomophthorales) Scale bar = 0.3 mm

Entomopathogenic fungi show a diversity of lifecycles, with differences across lineages, as well as within lineages, between species, and even between isolates within species. [5] Some fungal entomopathogens are opportunistic whereas some have evolved into highly specific pathogens of insects. [1]

Entomopathogenic fungi all typically disperse through the environment through the use of microscopic spores (usually asexual or Conidia) that commonly use hydrophobins and adhesins to attach to and recognize the host cuticle. [4] Germination is environmentally triggered under specific temperature and humidity conditions. Up on germination, many filamentous fungal pathogens begin growing hyphae and colonize the insect's cuticle. Some also produce structures called appressoria. [4] [5] These appressoria (also produced by plant pathogenic fungi) apply mechanical force onto the insect cuticle to support entry of the pathogen into the insect body.

Fungi penetrate the insect exoskeleton by boring through it using enzymatic hydrolysis. When the infection reaches the insects' body cavity (hemocoel), the fungal cells proliferate in the host body cavity, usually as walled hyphae or in the form of wall-less protoplasts (depending on the fungus involved).

Regardless of whether the infecting fungus is a host generalist or a specialist, the infection usually leads to the death of the insect, upon which the fungus emerges and sporulates on the dead insect. Sporulation usually takes place on the external surface of the cadaver. However, it can also occur on the internal surfaces of the cadaver depending on the environmental humidity. Some fungi keep the insect cadavers attached to foliage using rhizoids to ensure that they remain in the same environment where it is more likely to encounter suitable new hosts. [5]

Entomopathogenic fungi differ in virulence. Some (usually those with a broad spectrum of hosts - host generalists) immediately kill the insect using various toxins (e.g. Metarhizium robertsii) and grow on the dead insect body, digesting it for nutrients. Others (usually fungi that have evolved host-specificity) keep the host alive longer and progress onto systematically invading and infecting host tissues [6] (e.g. Ophiocordyceps spp.). Some host specialist entomopathogenic fungi have even evolved mechanisms of behavioral manipulation (e.g. Ophiocordyceps unilateralis - Zombie ant fungus) of their hosts. [7] These fungi hijack the insect nervous systems using various secondary metabolites and manipulate insect behavior to move the infected insect to a place which is appropriate for the fungus to grow, sporulate and acquire new hosts. [7]

Diversity

Recent classification efforts based on genomic data resulted in major re-arrangements of the phyla in kingdom fungi: one major change included lifting the subphylum Entomophthoromycotina into a separate phylum Entomophthoromycota. [8] Eight phyla contain Entomopathogenic fungi:  Ascomycota, Basidiomycota, Chytridiomycota, Microsporidia, Oomycetes, Entomophthoromycota, Blastocladiomycota and, Kickxellomycotina. [8] [9] [4] [7] Microsporidia infect the greatest number insect orders (13) followed by Ascomycota and Entomophthoromycota (13 and 10). Fungi in Chytridiomycota and Basidiomycota infect 3 and 2 insect orders, respectively. [10] [11]

Ascomycota

Two of three subphyla of the phylum Ascomycota contain insect pathogens. [12] Most ascomycetes are filamentous fungi that produce septate hyphae and have characteristics sexual phase in which they produce sexual spores called ascospores. [1] Most entomopathogenic fungi in the Phylum Ascomycota infect and proliferate in the insect body in a parasitic phase before eventually killing the host. Upon the death of the host, these fungi have the ability to grow saprophytically in and on the insect cadaver and produce and release spores. The most characteristic group of insect pathogens in the Phylum Ascomycota is the order Hypocreales which include genera such as Ophiocordyceps, Cordyceps, and Hypocrella. [1] Some insect pathogens in this phylum manipulate host behavior during the parasitic phase of their infection. [7] One well studied and popular example is the insect pathogen Ophiocordyceps unilateralis , which alters the behavior of the infected insect to leave the nest and move to an area where the environment conditions better suited for the growth of the fungi. [13] Upon the death of the host, the O. unilateralis produces a stalk-like structure erupting from the head of the dead ant from which spores are released to the peripheral environment. [13] this process enables the fungi to infect more ants and, in the process, creates high densities of dead ants in the forest environment known as 'graveyards'. [13]

Basidiomycota

The phylum Basidiomycota are commonly known as "superior fungi" due to their production of well-developed septate hyphae and fruiting bodies. Some basidiomycetes commonly produce visible structures such as mushrooms and puffballs. They are characterized by the asexual production of Basidiospores. [14] Fibulorhizoctonia, Uredinella, and Septobasidium are the only known genera in the phylum Basidiomycota that infect insects. [1]

Chytridiomycota

Phylum Chytridiomycota is considered one of the earliest branching true-fungi in the fungal kingdom. They are also the only true-fungi to produce motile zoospores in their lifecycle. [1]

Few genera of entomopathogenic fungi belong to the Phylum Chytridiomycota. [15] The genus Myrmicinosporidium include M. durum which is an endoparasite of ants. [15] The genus Nephridiophaga include unicellular endoparasites of cockroaches and genus Myiophagus include unicellular endoparasites of scale insects. [1]

Microsporidia

Microsporidia are obligately unicellular spore forming organisms and are strictly intracellular parasites, [16] and are generally host-specific [1] and extremely dependent on their host. [16] Almost all stages of their lifecycle can only take place inside the host cells due to their characteristics lack of mitochondria and inability to perform oxidative phosphorylation. [15] These fungi can only survive outside of their host as spores.

Microsporidia infects 69 insect genera [1] forming one of the largest groups of insect infecting fungi. Amblyospora spp.(a Microsporidian fungi) known to attack 79 different insect species in the order Diptera alone. Another economically important Microsporidian entomopathogen is Nosema bombycis which is known to be responsible for agricultural loss through infecting and killing bees through widespread infections. [1]

Entomophthoromycota

The phylum Entomophthoromycota are a group of true fungi which was previously classified under now rejected phylum Zygomycota. These include above 250 species of entomopathogens and some saprobes. [17]

Most of the entomopathogens in the phylum Entomophthoromycota belong to the order Entomophthorales. Most of Entomophthorales are obligate insect pathogens and are mostly host specific [18] making them ideal for use in insect biological control. Some prominent examples of Entomophthoralean entomopathogens include Zoopthora radicans, Z. phalloides, and Pandora neoaphidis. [18]

Oomycetes

Although traditionally considered as a group of fungi, Oomycetes do not share a common ancestor with fungi. [1] However, they are still considered fungi-like organisms due their growth and nutritional habits. For example, Oomycetes are mostly filamentous similar to fungi and acquire nutrients through external digestion of complex substrates and absorption of digestion products through cell membranes. And they also reproduce through spores. [15] However, their production of biflagellate zoospores during asexual reproduction and their cell wall structure sets them apart from most fungi. [1] [15]

Most animal pathogenic Oomycetes belong to either class Saprolegniomycetes or class Peronosporomycetes. [1] There are 12 species of entomopathogenic oomycetes. [15] Of these most notable is Lagenidium giganteum which is found in natural aerated freshwater systems. L. giganteum is known to be facultative parasites of mosquito larvae and is proposed to be of use in mosquito biocontrol. [15] [1]

Evolution of entomopathogenicity in Fungi

The widespread taxonomic distribution of entomopathogenic fungi—with representatives including unicellular fungal parasites (e.g. Microsporidia) to more derived groups such as Ascomycota and Basidiomycota—indicates multiple evolutionary origins of pathogenicity for insects. Even within fungal orders, pathogenicity for insects may have multiple evolutionarily-indepdent origins. For example, three families in the order Hypocreales (Clavicipitaceae, Cordycipitaceae and, Ophiocordycipitaceae) appear to have independently developed this nutritional habit. [19]

Interkingdom host jumping may be one evolutionary mechanism for the origin of entomophagy. Cordycipitaceae fungi appear to have jumped from insect to plant to truffle, [20] demonstrating the high flexibility of fungi for different hosts. Furthermore, acquisition and loss of entomophagy may have occurred multiple times during the evolutionary history of fungi [19] .   

Human use

Biological control

Entomopathogenic fungi are a potential eco-friendly alternative to chemical insecticides. [21] [5] In classical biological control, there are two demonstrated examples of potential use of entomopathogenic fungi against exotic insect species affecting agriculture. The oldest example is the use of Entomophthora maimaiga against the Spongy moth (Lymantria dispar) in the United States during early 1900s. The spongy moth was introduced into the United States accidentally in 1860s. Similarly, the E. maimaiga was also suspected to be an accidental introduction. Despite the accidental nature of introduction, several subsequent research has found that E. maimaiga is effectively keeping the spongy moth populations at control preventing outbreaks in North-east USA. [22] The second example is the use of Zoophthora radicans against spotted alfalfa aphid (Therioaphis trifolii f. maculata) in Australia during 1979. The spotted alfalfa aphid is an exotic insect pathogen of legumes introduced to Australian pastures during 1970s. Z. radicans is an entomopathogenic fungi native to Israel and capable of infecting alfalfa aphids. Research suggests that introduction of Z. radicans was effective in controlling spotted alfalfa population in Australia. [22]

Bioremediation

Entomopathogenic fungi may be able to accumulate anthropogenic toxic compounds and therefore be used in bioremediation. [4] For example, Metarhizium robertsii and M. brunneum have found to be highly efficient in degrading branched nonylphenols. [23] [4] Similarly, various strains of entomopathogenic fungi have shown efficient substrate removal of a diverse range of anthropogenic pollutants including Triazine, Synthetic estrogens, n-alkanes etc. [4]

Cordyceps fungi are parasitoids of various arthropod species. Here is a wasp parasitized by the fungus Cordyceps. Cordyceps.jpg
Cordyceps fungi are parasitoids of various arthropod species. Here is a wasp parasitized by the fungus Cordyceps.

Host relationship chemical cues

Entomopathogenic fungi such as Beauveria bassiana and Metarhizium spp. successfully infect susceptible host populations through conidia . [24] [25] The signaling cues between these fungi and their host targets are under investigation. The ability to sense these parasites can increase fitness for the host targets. Evidence suggests that signal recognition occurs within some hosts, but not others. For example, the ectoparasite Cephalonomia tarsalis is susceptible to B. bassiana but it cannot detect the presence of free conidia of this fungus or infected hosts. [26] Because they cannot detect these parasites, either the host or the host's offspring become infected and/or die. In contrast, termites detect and avoid some lethal conidia strains. [27] Other soil-dwelling insects have evolved the ability to detect and avoid certain entomopathogenic fungi.[ citation needed ]

See also

Related Research Articles

<i>Cordyceps</i> Genus of fungi

Cordyceps is a genus of ascomycete fungi that includes over 260 species worldwide, many of which are parasitic. Diverse variants of cordyceps have had more than 1,500 years of use in Chinese medicine. Most Cordyceps species are endoparasitoids, parasitic mainly on insects and other arthropods ; a few are parasitic on other fungi.

<i>Beauveria bassiana</i> Species of fungus

Beauveria bassiana is a fungus that grows naturally in soils throughout the world and acts as a parasite on various arthropod species, causing white muscardine disease; it thus belongs to the group of entomopathogenic fungi. It is used as a biological insecticide to control a number of pests, including termites, thrips, whiteflies, aphids and various beetles. Its use in the control of bed bugs and malaria-transmitting mosquitos is under investigation.

Metarhizium robertsii is a fungus that grows naturally in soils throughout the world and causes disease in various insects by acting as a parasitoid. It is a mitosporic fungus with asexual reproduction, which was formerly classified in the form class Hyphomycetes of the phylum Deuteromycota.

Hyphomycetes are a form classification of fungi, part of what has often been referred to as fungi imperfecti, Deuteromycota, or anamorphic fungi. Hyphomycetes lack closed fruit bodies, and are often referred to as moulds. Most hyphomycetes are now assigned to the Ascomycota, on the basis of genetic connections made by life-cycle studies or by phylogenetic analysis of DNA sequences; many remain unassigned phylogenetically.

Clonostachys rosea f. rosea, also known as Gliocladium roseum, is a species of fungus in the family Bionectriaceae. It colonizes living plants as an endophyte, digests material in soil as a saprophyte and is also known as a parasite of other fungi and of nematodes. It produces a wide range of volatile organic compounds which are toxic to organisms including other fungi, bacteria, and insects, and is of interest as a biological pest control agent.

Raymond J. St. Leger is an American mycologist, entomologist, molecular biologist and biotechnologist who currently holds the rank of Distinguished University Professor in the Department of Entomology at the University of Maryland, College Park.

<span class="mw-page-title-main">Fungus</span> Biological kingdom, separate from plants and animals

A fungus is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as one of the traditional eukaryotic kingdoms, along with Animalia, Plantae, and either Protista or Protozoa and Chromista.

<i>Metarhizium acridum</i> Grasshopper- and locust-killing fungus

Metarhizium acridum is the new name given to a group of fungal isolates that are known to be virulent and specific to the Acrididea (grasshoppers). Previously, this species has had variety status in Metarhizium anisopliae ; before that, reference had been made to M. flavoviride or Metarhizium sp. describing an "apparently homologous and distinctive group" of isolates that were most virulent against Schistocerca gregaria in early screening bioassays.

<i>Metarhizium flavoviride</i> Species of fungus

Metarhizium flavoviride is a Sordariomycete in the order Hypocreales and family Clavicipitaceae. The genus Metarhizium currently consists of over 70 described species and are a group of fungal isolates that are known to be virulent against Hemiptera and some Coleoptera. M. flavoviride is described as its own species, but there also exists a variety of M. flavoviride, which is M. flavoviride var. flavoviride. Previously described varieties of M. flavoviride have been documented, however recent random amplified polymorphic DNA (RAPD) markers have assigned these varieties as new species. The reassigned species are as follows: M. flavoviride Type E is now M. brasiliense; M. flavoviride var. minus is now M. minus; M. flavoviride var. novozealandicum is now M. novozealandicum; and M. flavoviride var. pemphigi is now M. pemphigi.

<span class="mw-page-title-main">Entorrhizomycetes</span> Class of fungi

Entorrhizomycetes is the sole class in the phylum Entorrhizomycota, within the Fungi subkingdom Dikarya along with Basidiomycota and Ascomycota. It contains three genera and is a small group of teliosporic root parasites that form galls on plants in the Juncaceae (rush) and Cyperaceae (sedge) families. Prior to 2015 this phylum was placed under the subdivision Ustilaginomycotina. A 2015 study did a "comprehensive five-gene analyses" of Entorrhiza and concluded that the former class Entorrhizomycetes is possibly either a close sister group to the rest of Dikarya or Basidiomycota.

<span class="mw-page-title-main">Muscardine</span> Fungal disease of insects

Muscardine is a disease of insects. It is caused by many species of entomopathogenic fungus. Many muscardines are known for affecting silkworms. Muscardine may also be called calcino.

Zoophthora is a genus of fungi in the family Entomophthoraceae. Like other taxa in this family, Zoophthora species cause disease in insects and as such are considered entomopathogenic fungi.

Entomophaga grylli is a fungal pathogen which infects and kills grasshoppers. It is the causal agent of one of the most widespread diseases affecting grasshoppers. This is sometimes known as summit disease because infected insects climb to the upper part of a plant and grip the tip of the stem as they die; this ensures widespread dispersal of the fungal spores. The fungus is a species complex with several different pathotypes, each one of which seems to be host-specific to different subfamilies of grasshoppers. The pathogen is being investigated for its possible use in biological pest control of grasshoppers.

<span class="mw-page-title-main">Mycobiome</span> The fungal community in and on an organism

The mycobiome, mycobiota, or fungal microbiome, is the fungal community in and on an organism.

<i>Isaria fumosorosea</i> Species of fungus

Isaria fumosorosea is an entomopathogenic fungus, formerly known as Paecilomyces fumosoroseus. It shows promise as a biological pesticide with an extensive host range.

Donald W. Roberts was an American insect pathologist and one of the originators of that field. He was especially known for research into biological pest control of Lepidoptera by Metarhizium but also Beauveria bassiana. He was a Research Professor Emeritus in the Biology Department of Utah State University.

<i>Metarhizium anisopliae</i> Species of fungus

Metarhizium anisopliae is the type species in its genus of fungi, that grows naturally in soils throughout the world and causes disease in various insects by acting as a parasitoid. Ilya I. Mechnikov named it Entomophthora anisopliae (basionym) after the insect species from which it was originally isolated – the beetle Anisoplia austriaca and from these early days, fungi such as this have been seen as potentially important tools for pest management. It is a mitosporic fungus with asexual reproduction, which was formerly classified in the form class Hyphomycetes of the phylum Deuteromycota.

Batkoa major is a naturally occurring fungus that infects insects.

<i>Ophiocordyceps dipterigena</i> Species of fungus

Ophiocordyceps dipterigena is an entomopathogenic fungi species from the genus Ophiocordyceps. This species was originally described in 2007.

<i>Beauveria brongniartii</i> Species of fungus

Beauveria brongniartii is an entomopathogenic ascomycete fungus prevalent in various ecosystems, including forest soils, alpine grasslands, and peat bogs. Known for its effectiveness against coleopteran pests, particularly the European cockchafer and forest cockchafer, B. brongniartii has been widely adopted in biological control strategies across Europe, primarily within agriculture and forestry. Since the early 1990s, commercial formulations like Melocont, Pilzgerste and Beauveria–Schweizer have been used extensively to control cockchafer populations. These products typically use sterile barley kernels colonized with fungal spores, which are applied to soil to target cockchafer larvae and other life stages, demonstrating significant efficacy in reducing pest populations

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  24. ↑ Vandenburg, J.D., Ramos, M. & Altre, J.A. (1998) Dose –response and age- and temperature-related susceptibility of the diamondback moth (Lepidoptera: Plutellidae) to two isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environmental Entomology, 27, 1017–1021.
  25. ↑ Hughes, W.O.H., Petersen, K.S., Ugelvig, L.V., Pedersen, D., Thomsen, L., Poulsen, M. et al. (2004) Density-dependence and within-host competition in a semelparous parasite of leafcutting ants. BMC Evolutionary Biology, 4, 45.
  26. ↑ Lord, J.C. (2001) Response of the wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as free conidia or infection in its host, the sawtoothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biological Control, 21, 300–304.
  27. ↑ Myles, T.G. (2002) Alarm, aggregation, and defense by Reticulitermes flavipes in response to a naturally occurring isolate of Metarhizium anisopliae. Sociobiology, 40, 243–255.
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