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Advances in Entomopathogen Isolation: a Case of Bacteria and Fungi

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Advances in Entomopathogen Isolation: a Case of Bacteria and Fungi microorganisms Review Advances in Entomopathogen Isolation: A Case of Bacteria and Fungi Lav Sharma 1,*, Nitin Bohra 2 , Vishnu D. Rajput 3 , Francisco Roberto Quiroz-Figueroa 4, Rupesh Kumar Singh 5 and Guilhermina Marques 1 1 Centre for the Research and Technology of Agro-Environment and Biological Sciences, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real, Portugal; [email protected] 2 Max Planck School Matter to Life, Max Planck Institute for Medical Research, Jahnstraße 29, 69120 Heidelberg, Germany; [email protected] 3 Soil Science and Land Evaluation Department, Academy of Biology and Biotechnology, Southern Federal University, 344090 Rostov-on-Don, Russia; [email protected] 4 Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Sinaloa (CIIDIR-IPN Unidad Sinaloa), Laboratorio de Fitomejoramiento Molecular, Blvd. Juan de Dios Bátiz Paredes no. 250, Col. San Joachín, C.P., Guasave 81101, Mexico; labfi[email protected] 5 Centro de Química de Vila Real, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real, Portugal; [email protected] * Correspondence: [email protected]; Tel.: +351-25-9350-2472 Abstract: Entomopathogenic bacteria and fungi are quite frequently found in soils and insect cadav- ers. The first step in utilizing these microbes as biopesticides is to isolate them, and several culture media and insect baiting procedures have been tested in this direction. In this work, the authors review the current techniques that have been developed so far, in the last five decades, and display brief protocols which can be adopted for the isolations of these entomopathogens. Among bacteria, this review focuses on Serratia spp. and bacteria from the class Bacilli. Among fungi, the review focuses those from the order Hypocreales, for example, genera Beauveria, Clonostachys, Lecanicillium, Metarhizium, and Purpureocillium. The authors chose these groups of entomopathogenic bacteria and fungi based on their importance in the microbial biopesticide market. Citation: Sharma, L.; Bohra, N.; Rajput, V.D.; Quiroz-Figueroa, F.R.; Keywords: Beauveria; Metarhizium; Hypocreales; Bacillus thuringiensis; Serratia Singh, R.K.; Marques, G. Advances in Entomopathogen Isolation: A Case of Bacteria and Fungi. Microorganisms 2021, 9, 16. https://dx.doi.org/ 1. Introduction 10.3390/microorganisms9010016 The global biopesticide market is expected to reach around USD 7.7 billion with a Received: 13 November 2020 compound annual growth rate of 14.1% [1]. It is also estimated that microbial biopesticides Accepted: 20 December 2020 will account for 3% of the total pesticide market [2]. The shift toward microbial biopesticides Published: 23 December 2020 is increasing as European legislation is continuously pressing to minimize the residue levels of synthetic chemical pesticides. Moreover, forthcoming directive (EC 91/414) demands Publisher’s Note: MDPI stays neu- a ban of chemical pesticides that are deemed to be the disruptors of human endocrine tral with regard to jurisdictional claims system. Microbial biocontrol agents are the new hope in this direction, and governments in published maps and institutional and scientists in Europe have simplified the European microbial pesticide registration affiliations. procedures outlined in the Regulation of Biological Control Agents (REBECA), with an objective to facilitate the development of microbial biocontrol agents [3]. Entomopathogenic bacteria (EPB) and entomopathogenic fungi (EPF) are the natural Copyright: © 2020 by the authors. Li- enemies of insect-pests. Hence, their importance in agriculture is quite high [4–8]. The ma- censee MDPI, Basel, Switzerland. This jority of the EPB belong to a few bacterial families, such as Bacillaceae, Enterobacteriaceae, article is an open access article distributed Micrococcaceae, Pseudomonadaceae, and Streptococcaceae. Bacillus thuringiensis (Bt) is under the terms and conditions of the arguably the most widely studied and used bacterial entomopathogen [9]. At present, Creative Commons Attribution (CC BY) there are over 40 Bt products for insect biological control, which account for 1% of the license (https://creativecommons.org/ total global insecticide market and approximately a market of USD 210 million per an- licenses/by/4.0/). Microorganisms 2021, 9, 16. https://dx.doi.org/10.3390/microorganisms9010016 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 16 2 of 28 num [3,10,11]. Other bacterial biopesticides account for approximately USD 50 million per annum. A list of commercial EPB and their target insect groups is presented in the Table1. Table 1. Examples of common commercially available entomopathogenic bacteria (EPB) and their target insect groups. Bacteria Target Pest Crops PRODUCT (Company, Country) CRYMAX (Certis, USA) DELIVER (Certis, USA) JAVELIN WG (Certis, USA) COSTAR JARDIN; COSTAR WG (Mitsui AgriScience International NV, Belgium) LEPINOX PLUS (CBC, Europe) B. acillus thuringiensis Lepidoptera Row crops, forests, orchards, subsp. kurstaki forests turfs BACTOSPEINE JARDIN EC (Duphar BV, The Netherlands) DOLPHIN (Andermatt Biocontrol, Switzerland) BMP 123 (Becker, USA) DIPEL DF (Valent Biosciences, USA) LEAP (Valent Biosciences, USA) FORAY 48 B (Valent Biosciences, USA) CRYMAX (Certis, USA) AGREE 50 WG (Certis, USA) B. thuringiensis subsp. Lepidoptera Row crops, orchards aizawai XENTARI (Valent Biosciences, USA) FLORBAC (Bayer, Germany) B. thuringiensis subsp. Coleoptera: Potatoes, tomatoes, eggplant, TRIDENT (Certis USA) Chrysomelidae tenebrionis elm trees NOVODOR FC (Valent Biosciences, USA) AQUABAC DF3000, (Becker Microbial Products Inc, USA) VECTOPRIME (Valent Biosciences, USA) Diverse lentic and lotic B. thuringiensis subsp. Diptera TEKNAR (Valent Biosciences, USA) israelensis aquatic habitats VECTOBAC (Valent Biosciences, USA) BACTIMOS (Valent Biosciences, USA) SOLBAC (Andermatt Biocontrol, Switzerland) Lysinibacillus sphaericus Diptera: Culicidae Lentic aquatic habitats VECTOLEX (Valent Biosciences, USA) Coleoptera: BIOSHIELD GRASS GRUB Serratia entomophila Pastures Scarabaeidae (Biostart, New Zealand) Japanese beetle Lawns, flowers, mulch beds, MILKY SPORE POWDER (St. Gabriel Paenibacillus popilliae larvae/grub gardens Organics, USA) Similarly, over 170 biopesticides based on fungi have been developed since 1960, and 75% are either still in use or have been registered [10,11]. This accounts for at least USD 77 million annually [3,10,11]. Their popularity can be attributed to the fact that EPF pose lesser risks for nontarget arthropods, such as bees, predatory beetles, and parasitic wasps. Hypocrealean fungi such as Beauveria, Metarhizium, Cordyceps, and Lecanicillium are some of the well-known fungal entomopathogens [7]. A list of commercially available EPF along with their target insect groups is presented in the Table2. Microorganisms 2021, 9, 16 3 of 28 Table 2. Examples of common commercially available entomopathogenic fungi (EPF) and their target insect groups. Fungi Target Pest Crop Product and Company Psyllids, whiteflies, thrips, crops BOTE GHA (Certis, USA) aphids, mites Flies, mites, thrips, NATURALIS (Troy cotton, glasshouse crops leafhoppers, and weevils Biosciences, USA) CONIDIA (AgroEvo, Coffee berry borer coffee Germany) Whiteflies, aphids, thrips field crops MYCOTROL (Bioworks, USA) BOTANIGRAD (Bioworks, Whiteflies, aphids, thrips field crops Beauveria bassiana sensu lato USA) OSTRINIL (Arysta Lifescience, Corn borer maize France) Spotted mite, eucalyptus BOVERIL (Koppert, weevil, coffee borer, and crops The Netherlands) whitefly BALANCE (Rincon-Vitova Flies Insectaries, USA) BEAUVERIA BASSIANA As soil treatment crops PLUS, (BuildASoil, USA) peppers, tomatoes, potatoes, BEA-SIN (Agrobionsa, Whitefly eggplants Mexico) MELOCONT PILZGERSTE forests, vegetables, fruits, May beetle (Samen-schwarzenberger, grasslands Austria) BEAUPRO (Andermatt B. brongniartii Cockchafer larvae Fruits, Meadows Biocontrol, Switzerland) BETEL (Natural Plant Scarabs beetle larvae sugarcane Protection, France) BEAUVERIA-SCHWEIZER Cockchafer fruits, Meadows (Eric Schweizer, Switzerland) METARRIL WP Sugar cane root leafhopper sugarcane (Koppert, The Netherlands) Cockroaches houses BIO-PATH (EcoScience, USA) Vine weevils, sciarid flies, glasshouse, ornamental crops BIO 1020 (Bayer, Germany) wireworms and thrips pupae Metarhizium anisopliae sensu lato White grubs sugarcane BIOCANE (BASF, Australia) termites BIOBLAST (Paragon, USA) Black vine weevil, strawberry stored grains and crops MET-52 (Novozymes, USA) root weevil, thrips META-SIN (Agrobionsa, Pepper weevil chili and bell peppers Mexico) GREEN GUARD M. acridum Locusts and grasshoppers crops (BASF, Australia) M. frigidum Scarab larvae crops BIOGREEN (BASF, Australia) ATTRACAP (Biocare, M. brunneum Wireworms potato and asparagus crops Germany) Microorganisms 2021, 9, 16 4 of 28 Table 2. Cont. Fungi Target Pest Crop Product and Company PREFERAL WG Whiteflies glasshouse crops (Biobest, Belgium) Cordyceps fumosorosea Aphids, Citrus psyllid, spider PFR-97 20% WDG wide range of crops mite, thrips, whitefly (Certis, USA) Peppers, tomatoes, potatoes, BEA-SIN (Agrobionsa, Whitefly eggplants Mexico) Cotton bullworm, Citrus CHALLENGER (Koppert, Field crops psyllid The Netherlands) VERTALEC (Koppert, Aphids crops Lecanicillium longisporum The Netherlands) MYCOTAL (Koppert, Whiteflies, thrips crops The Netherlands) peppers, tomatoes, potatoes, VERTI-SIN (Agrobionsa,
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