Abstract
The control of gastrointestinal parasites in animals has become more challenging every year due to parasite resistance to conventional chemical control, which has been observed worldwide. Ovicidal or opportunistic fungi do not form traps to capture larvae. Their mechanism of action is based on a mechanical/enzymatic process, which enables the penetration of their hyphae into helminth eggs, with subsequent internal colonization of these. The biological control with the Pochonia chlamydosporia fungus has been very promising in the treatment of environments and prevention. When used in intermediate hosts of Schistosoma mansoni, the fungus promoted a high percentage decrease in the population density of aquatic snails. Secondary metabolites were also found in P. chlamydosporia. Many of these compounds can be used by the chemical industry in the direction of a commercial product. This review aims to provide a description of P. chlamydosporia and its possible use as a biological parasitic controller. The ovicidal fungus P. chlamydosporia is effective in the control of parasites and goes far beyond the control of verminosis, intermediate hosts, and coccidia. It can also be used not only as biological controllers in natura but also as their metabolites and molecules can have chemical action against these organisms.
Key points
• The use of the fungus P. chlamydosporia is promising in the control of helminths.
• Metabolites and molecules of P. chlamydosporia may have chemical action in control.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data sharing not applicable to this article as no datasets were generated or analysed during the current study.
References
Alves DR, de Morais SM, Tomiotto-Pellissier F, Vasconcelos FR, Freire FDCO, da Silva ING, Cataneo AHD, Miranda-Sapla MM, Pinto GAS, Conchon-Costa I, Noronha AAA, Pavanelli WR (2018) Leishmanicidal and fungicidal activity of lipases obtained from endophytic fungi extracts. PLoS One 13:e0196796. https://doi.org/10.1371/journal.pone.0196796
Aranda-Martinez A, Lenfant N, Escudero N, Zavala-González E, Henrissat B, Lopez-Llorca L (2016) CAZyme content of Pochonia chlamydosporia reflects that chitin and chitosan modification are involved in nematode parasitism. Environ Microbiol 18(11):4200–4215. https://doi.org/10.1111/1462-2920.13544
Aranda-Martinez A, Naranjo Ortiz MÁ, Abihssira García IS, Zavala-Gonzalez EA, Lopez-Llorca LV (2017) Ethanol production from chitosan by the nematophagous fungus Pochonia chlamydosporia and the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Microbiol Res 204:30–39. https://doi.org/10.1016/j.micres.2017.07.009
Araujo JM, de Araújo JV, Braga FR, Carvalho RO, Ferreira SR (2009) Activity of the nematophagous fungi Pochonia chlamydosporia, Duddingtonia flagrans and Monacrosporium thaumasium on egg capsules of Dipylidium caninum. Vet Parasitol 166:86–89. https://doi.org/10.1016/j.vetpar.2009.08.003
Araujo JM, Braga FR, Araújo JV, Benjamin LDA (2010) The ovicidal activity of fungi Pochonia chlamydosporia and Paecilomyces lilacinus on Taenia saginata eggs in laboratory trial. Rev Inst Adolfo Lutz 69(2):165–9. https://doi.org/10.53393/rial.2010.v69.32651
Araujo JM, de Araújo JV, Braga FR, Ferreira SR, Tavela ADO (2013) Predatory activity of chlamydospores of the fungus Pochonia chlamydosporia on Toxocara canis eggs under laboratory conditions. Rev Bras Parasitol Veterinária 22:171–4. https://doi.org/10.1590/s1984-29612013000100033
Araújo JV, Braga FR, Mendoza-de-Gives P, Paz-Silva A, Vilela VLR (2021) Recent advances in the control of helminths of domestic animals by helminthophagous fungi. Parasitologia 1:168–176. https://doi.org/10.3390/parasitologia1030018
Braga FR, Araújo JV (2014) Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Appl Microbiol Biotechnol 98:71–82. https://doi.org/10.1007/s00253-013-5366-z
Braga FR, Araújo JV, Campos AK, Carvalho RO, Silva AR, Tavela AO, Maciel AS (2007) Observação in vitro da ação dos isolados fúngicos Duddingtonia flagrans, Monacrosporium thaumasium e Verticillium chlamydosporium sobre ovos de Ascaris lumbricoides (Lineu, 1758). Rev Soc Bras Med Trop 40:356–358. https://doi.org/10.1590/S0037-86822007000300024
Braga FR, Araújo JV, Carvalho RO, Silva AR, Araujo JM, Soares FEF, Geniêr HLA, Ferreira SR, Queiroz JH (2010a) Ovicidal action of a crude enzymatic extract of the fungus Pochonia chlamydosporia against cyathostomin eggs. Vet Parasitol 172:264–268. https://doi.org/10.1016/j.vetpar.2010.05.011
Braga FR, Araujo JV, Silva AR, Araujo JM, Carvalho RO, Campos AK, Tavela AO, Ferreira SR, Frassy LN, Alves CDF (2010b) Duddingtonia flagrans, Monacrosporium thaumasium and Pochonia chlamydosporia as possible biological control agents of Oxyuris equi and Austroxyuris finlaysoni. J Helminthol 84:21–25. https://doi.org/10.1017/S0022149X09990034
Braga FR, Araújo JV, Silva AR, Carvalho RO, Araujo JM, Ferreira SR, Carvalho GR (2010c) Viability of the nematophagous fungus Pochonia chlamydosporia after passage through the gastrointestinal tract of horses. Vet Parasitol 194:264–268. https://doi.org/10.1016/j.vetpar.2009.11.020
Braga FR, Araújo JV, Silva AS, Carvalho RO, Tavela AO (2008) In vitro evaluation of the action of the nematophagous fungi Duddingtonia flagrans, Monacrosporium sinense and Pochonia chlamydosporia on Fasciola hepatica eggs. World J Microbiol Biotechnol 24:1559–1564. https://doi.org/10.1007/s11274-007-9643-9
Braga FR, Araujo JM, Silva AR, de Araújo JV, Carvalho RO, Soares FEDF, de Queiroz JH, Gênier HLA (2011) Ação ovicida do extrato bruto enzimático do fungo Pochonia chlamydosporia sobre ovos de Ancylostoma sp. Rev Soc Bras Med Trop 44:116–118. https://doi.org/10.1590/S0037-86822011000100027
Braga FR, Araújo JV, Soares FEF, Tavela AO, Araujo JM, Carvalho RO, Fernandes FM, Queiroz JH (2012) Enzymatic analysis and in vitro ovicidal effect of Pochonia chlamydosporia and Paecilomyces lilacinus on Oxyuris equi eggs of horses. Biocontrol Sci Technol 22:685–696. https://doi.org/10.1080/09583157.2012.677807
Braga FR, Ferraz CM, da Silva EN, de Araújo JV (2020) Efficiency of the Bioverm® (Duddingtonia flagrans) fungal formulation to control in vivo and in vitro of Haemonchus contortus and Strongyloides papillosus in sheep. 3 Biotech 10:62. https://doi.org/10.1007/s13205-019-2042-8
Braga FR, Mendoza De Gives P, Paz Silva A, Soares FEDF, Araújo JV De (2014) Zoonotic neglected tropical diseases: New approaches to combat old enemies. Biomed Res. Int. 2. https://doi.org/10.1155/2014/914248
Braga FR, Ricardo A, Araujo JM, Ferreira SR, de Araújo JV, Frassy LN (2009) Ação ovicida do fungo Pochonia chlamydosporia sobre ovos de Enterobius vermicularis. Rev Inst Adolfo Lutz 68:318–321. https://doi.org/10.53393/rial.2009.v68.32734
Carmo TA, Mena MO, Cipriano IA, Favare GM, Guelpa GJ, Pinto SC, Amarante AFT, Araújo JV, Soutello RVG (2023) Biological control of gastrointestinal nematodes in horses fed with grass in association with nematophagus fungi Duddingtonia flagrans and Pochonia chlamydosporia. Biol Control 182:105219. https://doi.org/10.1016/j.biocontrol.2023.105219
Carvalho RO, Araújo JV, Braga FR, Araujo JM, Alves CDF (2010) Ovicidal activity of Pochonia chlamydosporia and Paecilomyces lilacinus on Toxocara canis eggs. Vet Parasitol 169:123–127. https://doi.org/10.1016/j.vetpar.2009.12.037
Carvalho LM, Braga FR, Domingues RR, Araujo JM, Lelis RT, Paula AT, Silveira W, Araújo JV (2013) Interaction of the nematophagous fungus Pochonia chlamydosporia and Parascaris equorum eggs in different culture media. J Basic Microbiol 54:109-S114. https://doi.org/10.1002/jobm.201300586
Castro LS, Martins IVF, Tunholi Alves VM, de Araújo JV, Tunholi-Alves VM, Bittencourt VREP (2019) Ovicidal potential of Pochonia chlamydosporia isolate Pc-10 (Ascomycota: Sordariomycetes) on egg masses of the snail Pseudosuccinea columella (Mollusca: Gastropoda). J Invertebr Pathol 166:107212. https://doi.org/10.1016/J.JIP.2019.107212
Castro LS, Martins IVF, Alves V, RoldiF Tavares, GP, Araújo, JV, (2020) Effect of the Enzymatic FungalExtract of Pochonia chlamydosporia on the Viability of Fasciolahepatica eggs. J Adv Vet Anim Res 10:135–140
Castro LS, Martins IVF, Tunholi-Alves VM, Amaral LS, Pinheiro J, de Araújo JV, de Oliveira Monteiro CM, Tunholi VM (2022a) Susceptibility of embryos of Biomphalaria tenagophila (Mollusca: Gastropoda) to infection by Pochonia chlamydosporia (Ascomycota: Sordariomycetes). Arch Microbiol 204:271. https://doi.org/10.1007/s00203-022-02894-x
Castro LS, Martins IVF, Tunholi VM, Araújo JV, de Vieira F, PR, (2022b) Enzymatic activity of the fungus Pochonia chlamydosporia (Sordariomycetes: Hypocreales) and its ovicidal potential on eggs of Toxocara canis (Nematoda: Ascaridida). Veterinária Notícias 28:1–10. https://doi.org/10.14393/VTN-v28n1-2022-63919
Chroumpi T, Mäkelä MR, de Vries RP (2020) Engineering of primary carbon metabolism in filamentous fungi. Biotechnol Adv 43:107551. https://doi.org/10.1016/j.biotechadv.2020.107551
Crueger W, Crueger A, Brock TD, Brock TD (1990) Biotechnology: a textbook of industrial microbiology.
Dallemole-Giaretta R, Freitas LG, Cavallin IC, Marmentini GA, Faria CMR, Resende JTV (2013) Evaluation of a Pochonia chlamydosporia based product, for the control of Meloidogyne javanica in culture and in carrot field. Nematropica 43:131–137
de Carvalho LM, Braga FR, Domingues RR, Araujo JM, Lelis RT, de Paula AT, da Silveira WF, de Araújo JV (2014) Interaction of the nematophagous fungus Pochonia chlamydosporia and Parascaris equorum eggs in different culture media. J Basic Microbiol 54:S109–S114. https://doi.org/10.1002/jobm.201300586
Frassy LN, Braga FR, Silva AR, de Araújo JV, Ferreira SR, de Freitas LG (2010) Destruição de ovos de Toxocara canis pelo fungo nematófago Pochonia chlamydosporia. Rev Soc Bras Med Trop 43:102–104. https://doi.org/10.1590/S0037-86822010000100024
de Gouveia AS, Monteiro TSA, Valadares SV, Sufiate BL, de Freitas LG, Ramos HJ de O, de Queiroz JH, (2019) Understanding how Pochonia chlamydosporia increases phosphorus availability. Geomicrobiol J 36:747–751. https://doi.org/10.1080/01490451.2019.1616857
Derntl C, Kluger B, Bueschl C, Schuhmacher R, Mach RL, Mach-Aigner AR (2017) Transcription factor Xpp1 is a switch between primary and secondary fungal metabolism. Proc Natl Acad Sci 114:E560–E569. https://doi.org/10.1073/pnas.1609348114
Dowd CJ, Kelley B (2011) Purification process design and the influence of product and technology platforms. In: Comprehensive Biotechnology. pp 799–810. https://doi.org/10.1016/B978-0-08-088504-9.00137-9
Escudero N, Lopez-Moya F, Ghahremani Z, Zavala-Gonzalez EA, Alaguero-Cordovilla A, Ros-Ibañez C, Lacasa A, Sorribas FJ, Lopez-Llorca LV (2017) Chitosan increases tomato root colonization by pochonia chlamydosporia and their combination reduces root-knot nematode damage. Front Plant Sci 8:1415. https://doi.org/10.3389/fpls.2017.01415
Esteves I, Peteira B, Atkins SD, Magan N, Kerry B (2009) Production of extracellular enzymes by different isolates of Pochonia chlamydosporia. Mycol Res 8:867–876. https://doi.org/10.1016/j.mycres.2009.04.005
Fernandes FM, Aguiar AR, Costa Silva LP, Senna T, de Mello INK, de Oliveira T, Freitas SG, Ferreira Silveira W, Braga FR, Araújo JV (2017) Biological control on gastrointestinal nematodes in cattle with association of nematophagous fungi. Biocontrol Sci Technol 27:1445–1453. https://doi.org/10.1080/09583157.2017.1406063
Fernandes RH, Lopes EA, Borges DF, Bontempo AF, Zanuncio JC, Serrão JE (2017) Survival of Pochonia chlamydosporia on the soil surface after different exposure intervals at ambient conditions. Rev Iberoam Micol 34:241–245. https://doi.org/10.1016/j.riam.2017.04.001
Ferreira SR, de Araújo JV, Braga FR, Araujo JM, Frassy LN, Ferreira AS (2011) Biological control of Ascaris suum eggs by Pochonia chlamydosporia fungus. Vet Res Commun 35:553–558. https://doi.org/10.1007/s11259-011-9494-6
Ferreira SR, Machado ART, Furtado LF, Gomes JHDS, de Almeida RM, de Oliveira Mendes T, Maciel VN, Barbosa FS, Carvalho LM, Bueno LL, Bartholomeu DC, de Araújo JV, Rabelo EML, de Pádua RM, Pimenta LPS, Fujiwara RT (2020) Ketamine can be produced by Pochonia chlamydosporia: an old molecule and a new anthelmintic? Parasit Vectors 13:527. https://doi.org/10.1186/s13071-020-04402-w
Fonseca JD, Ferreira VM, Freitas SG, Vieira ÍS, Araújo JV (2022) Efficacy of a fungal formulation with the nematophagous fungus Pochonia chlamydosporia in the biological control of bovine nematodiosis. Pathogens 11:695. https://doi.org/10.3390/pathogens11060695
Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11:481–487. https://doi.org/10.1016/j.mib.2008.10.007
Hellwig V, Mayer-Bartschmid A, Müller H, Greif G, Kleymann G, Zitzmann W, Tichy H-V, Stadler M (2003) Pochonins A−F, new antiviral and antiparasitic resorcylic acid lactones from Pochonia chlamydosporia var. catenulata. J Nat Prod 66:829–837. https://doi.org/10.1021/np020556v
Lacatena F, Marra R, Mazzei P, Piccolo A, Digilio MC, Giorgini M, Woo SL, Cavallo P, Lorito M, Vinale F (2019) Chlamyphilone, a Novel Pochonia chlamydosporia Metabolite with Insecticidal Activity. Molecules 28:3609. https://doi.org/10.3390/molecules28083609
Lelis RT, Braga FR, de Carvalho LM, de Paula AT, Araujo JM, Fausto MC, Junior AM, Rodrigues JVF, de Freitas Soares FE, Garcia JS, de Araújo JV (2014) Effect of the fungus Pochonia chlamydosporia on Echinostoma paraensei (Trematoda: Echinostomatidae). Acta Trop 139:88–92. https://doi.org/10.1016/j.actatropica.2014.07.006
Li S, Wang D, Gong J, Zhang Y (2022) Individual and combined application of nematophagous fungi as biological control agents against gastrointestinal nematodes in domestic animals. Pathogens 11:172. https://doi.org/10.3390/pathogens11020172
Lýsek H (1976) Classification of ovicide fungi according to type of ovicidity. Acta University Palack Olumue 76:9–13
Lysek G (1977) Role of nutrition in the banding of fungi. Trans Br Mycol Soc 69:154–156. https://doi.org/10.1016/S0007-1536(77)80132-0
Mendoza-de Gives P, Braga FR, de Araújo JV (2022) Nematophagous fungi, an extraordinary tool for controlling ruminant parasitic nematodes and other biotechnological applications. Biocontrol Sci Technol 32:777–793. https://doi.org/10.1080/09583157.2022.2028725
Mi Q, Yang J, Ye F, Gan Z, Wu C, Niu X, Zou C, Zhang K-Q (2010) Cloning and overexpression of Pochonia chlamydosporia chitinase gene pcchi44, a potential virulence factor in infection against nematodes. Process Biochem 45:810–814. https://doi.org/10.1016/j.procbio.2010.01.022
Mota MDA, Campos AK, De Araújo JV (2003) Controle biológico de helmintos parasitos de animais: Estágio atual e perspectivas futuras. Pesqui Vet Bras 23:93–100. https://doi.org/10.1590/S0100-736X2003000300001
Naveed M, Nadeem F, Mehmood T, Bilal M, Anwar Z, Amjad F (2021) Protease—a versatile and ecofriendly biocatalyst with multi-industrial applications: an updated review. Catal Letters 151:307–323. https://doi.org/10.1007/s10562-020-03316-7
Niu XM (2017) Secondary metabolites from Pochonia chlamydosporia and other species of Pochonia. Springer, Cham, pp 131–168
Oliveira IDC, Vieira ÍS, Campos AK, de Araújo JV (2021) In vitro compatibility and nematicidal activity of Monacrosporium sinense and Pochonia chlamydosporia for biological control of bovine parasitic nematodes. Parasitology 148:956–961. https://doi.org/10.1017/S0031182021000652
Rathore AS, Gupta RD (2015) Chitinases from bacteria to human: properties, applications, and future perspectives. Enzyme Res. https://doi.org/10.1155/2015/791907
Rosni SM, Ahmad F, Awang A, Chye FY, Matanjun P (2015) Crude proteins, total soluble proteins, total phenolic contents and SDS-PAGE profile of fifteen varieties of seaweed from Semporna, Sabah, Malaysia. Int Food Res J 22:1483–1493
Soares FEDF, de Queiroz JH, de Araújo JV, Queiroz PV, Gouveia ADS, Hiura E, Braga FR (2015) Nematicidal action of chitinases produced by the fungus Monacrosporium thaumasium under laboratorial conditions. Biocontrol Sci Technol 3:337–344. https://doi.org/10.1080/09583157.2014.979133
Sufiate BL, Soares FE, Gouveia AS, Moreira SS, Cardoso E, Tavares GP, Queiroz JH (2018a) Statistical tools application on dextranase production from Pochonia chlamydosporia (VC4) and its application on dextran removal from sugarcane juice. An Acad Bras Ciênc 90:461–470. https://doi.org/10.1590/0001-3765201820160333
Sufiate BL, Soares FEDF, Moreira SS, Gouveia ADS, Cardoso EF, Braga FR, de Queiroz JH (2018b) In vitro and in silico characterization of a novel dextranase from Pochonia chlamydosporia. 3 Biotech 8:1–9. https://doi.org/10.1007/s13205-018-1192-4
Tavela AO, Araújo JV, Braga FR, Araujo JM, Magalhães LQ, Silveira WF, Borges LA (2012) In vitro association of nematophagous fungi Duddingtonia flagrans (AC001), Monacrosporium thaumasium (NF34) and Pochonia chlamydosporia (VC1) to control horse cyathostomin (Nematoda: Strongylidae). Biocontrol Sci Technol 22:607–610. https://doi.org/10.1080/09583157.2012.672952
Thambugala KM, Daranagama DA, Phillips AJL, Kannangara SD, Promputtha I (2020) Fungi vs. fungi in biocontrol: an overview of fungal antagonists applied against fungal plant pathogens. Front Cell Infect Microbiol 10:604923. https://doi.org/10.3389/fcimb.2020.604923
Thapa S, Mejer H, Thamsborg SM, Lekfeldt JDS, Wang R, Jensen B, Magid J, Meyling NV (2017) Survival of chicken ascarid eggs exposed to different soil types and fungi. Appl Soil Ecol 121:143–151. https://doi.org/10.1016/j.apsoil.2017.10.001
Valadão MC, Millena de Carvalho L, Vieira ÍS, Neves PH, Ferreira VM, Campos AK, de Freitas Elias, Soares F, Ferraz CM, Ribeiro Vilela VL, Braga FR, Araújo JV (2020) Germination capacity of the Pochonia chlamydosporia fungus after its passage through the gastrointestinal tract of domestic chickens (Gallus gallus domesticus). Exp Parasitol 216:107936. https://doi.org/10.1016/j.exppara.2020.107936
Vieira IS, Oliveira ID, Freitas SG, Campos AK, de Araujo JV (2020) Arthrobotrys cladodes and Pochonia chlamydosporia in the biological control of nematodiosis in extensive bovine production system. Parasitology 147(6):699–705. https://doi.org/10.1017/S0031182020000098
Vieira ÍS, Oliveira IDC, Campos AK, de Araújo JV (2020) In vitro biological control of bovine parasitic nematodes by Arthrobotrys cladodes, Duddingtonia flagrans and Pochonia chlamydosporia under different temperature conditions. J Helminthol 94:e194. https://doi.org/10.1017/S0022149X20000796
Vieira ÍS, Oliveira IDC, Campos AK, Araújo JV (2020) Arthrobotrys cladodes and Pochonia chlamydosporia: nematicidal effects of single and combined use after passage through cattle gastrointestinal tract. Exp Parasitol 218:108005. https://doi.org/10.1016/j.exppara.2020.108005
World Health Organization & UNICEF/UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases. (2017). Global vector control response 2017–2030. World Health Organization. https://apps.who.int/iris/handle/10665/259205
Zhang Y, Li S, Li H, Wang R, Zhang K-Q, Xu J (2020) Fungi–nematode interactions: diversity, ecology, and biocontrol prospects in agriculture. J Fungi 6:206. https://doi.org/10.3390/jof6040206
Funding
This research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The authors thank CNPq, CAPES, FAPES, FAPEMIG, and Cooperação CAPES/FAPES (Programa de Desenvolvimento da Pós-Graduação—PDPG) for all the financial support throughout the group’s research.
This article does not contain any studies with human or animal participants performed by any of the authors.
Author information
Authors and Affiliations
Contributions
JVA and JSF came up with the idea for the article. All authors of the manuscript performed the literature search, wrote, and critically reviewed the work.
Corresponding author
Ethics declarations
Informed consent
Not applicable.
Conflicts of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
dos Santos Fonseca, J., Altoé, L.S.C., de Carvalho, L.M. et al. Nematophagous fungus Pochonia chlamydosporia to control parasitic diseases in animals. Appl Microbiol Biotechnol 107, 3859–3868 (2023). https://doi.org/10.1007/s00253-023-12525-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-023-12525-0