Abstract
Insects and fungal pathogens pose constant problems to public health and agriculture, especially in resource-limited parts of the world; and the use of chemical pesticides continues to be the main methods for the control of these organisms. Photorhabdus spp. and Xenorhabdus spp., (Fam; Morganellaceae), enteric symbionts of Steinernema, and Heterorhabditis nematodes are naturally found in soil on all continents, except Antarctic, and on many islands throughout the world. These bacteria produce diverse secondary metabolites that have important biological and ecological functions. Secondary metabolites include non-ribosomal peptides, polyketides, and/or hybrid natural products that are synthesized using polyketide synthetase (PRS), non-ribosomal peptide synthetase (NRPS), or similar enzymes and are sources of new pesticide/drug compounds and/or can serve as lead molecules for the design and synthesize of new alternatives that could replace current ones. This review addresses the effects of these bacterial symbionts on insect pests, fungal phytopathogens, and animal pathogens and discusses the substances, mechanisms, and impacts on agriculture and public health.
Key points
• Insects and fungi are a constant menace to agricultural and public health.
• Chemical-based control results in resistance development.
• Photorhabdus and Xenorhabdus are compelling sources of biopesticides.
Graphical abstract
Similar content being viewed by others
References
Abebew D, Sayedain FS, Bode E, Bode HB (2022) Uncovering nematicidal natural products from Xenorhabdus bacteria. J Agric Food Chem 70(2):498–506
Adams TB, Cohen SM, Doull J, Feron VJ, Goodman JI, Marnett LJ, Munro IC, Portoghese PS, Smith RL, Waddell WJ, Wagner BM (2005) The FEMA GRAS assessment of benzyl derivatives used as flavor ingredients. Food Chem Toxicol 43(8):1207–1240
Ahantarig A, Chantawat N, Waterfield NR, Ffrench-Constant R, Kittayapong P (2009) PirAB toxin from Photorhabdus asymbiotica as a larvicide against dengue vectors. Appl Environ Microbiol 75(13):4627–4629
Ahn JY, Lee JY, Yang EJ, Lee YJ, Koo KB, Song KS, Lee KY (2013) Mosquitocidal activity of anthraquinones isolated from symbiotic bacteria Photorhabdus of entomopathogenic nematode. J Asia Pac Entomol 16:317–320
Akhurst RJ (1980) Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J Gen Microbiol 121:303–309
Almeida F, Rodrigues ML, Coelho C (2019) The still underestimated problem of fungal diseases worldwide. Front Microbiol 10:214
Andersen A (2006) Final report on the safety assessment of benzaldehyde. Int J Toxicol 25:11–27
Bickers D, Calow P, Greim H, Hanifin JM, Rogers AE, Saurat JH, Sipes IG, Smith RL, Tagami H (2005) A toxicologic and dermatologic assessment of cinnamyl alcohol, cinnamaldehyde and cinnamic acid when used as fragrance ingredients: the RIFM expert panel. Food Chem Toxicol 43(6):799–836
Bock CH, Shapiro-Ilan DI, Wedge D, Cantrell CH (2014) Identification of the antifungal compound, trans cinnamic acid, produced by Photorhabdus luminescens, a potential biopesticide. J Pest Sci 87:155–162
Bode HB (2009) Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol 13:1–7
Bode HB, Müller R (2005) The impact of bacterial genomics on natural product research. Angew Chem Int Ed 44(42):6828–6846
Bode E, Brachmann AO, Kegler C, Şimşek R, Dauth C, Zhou Q, Kaiser M, Klemmt P, Bode HB (2015) Simple “on-demand” production of bioactive natural products. ChemBioChem 16:1115–1119
Bode E, Heinrich AK, Hirschmann M, Abebew D, Shi YN, Vo TD, Wesche F, Shi YM, Grün P, Simonyi S, Keller N, Engel Y, Wenski S, Bennet R, Beyer S, Bischoff I, Buaya A, Brandt S, Cakmak I, Cimen H, Eckstein S, Frank D, Fürst R, Gand M, Geisslinger G, Hazir S, Henke M, Heermann R, Lecaudey V, Schäfer W, Schiffmann S, Schüffler A, Schwenk R, Skaljac M, Thines E, Thines M, Ulshöfer T, Vilcinskas A, Wichelhaus TA, Bode HB (2019) Promoter activation in Δhfq mutants as an efficient tool for specialized metabolite production enabling direct bioactivity testing. Angew Chem Int Ed 131:19133–19139
Boemare NE (2002) Biology taxonomy and systematics of Photorhabdus and Xenorhabdus. In: Gaugler R (ed) Entomopathogenic nematology. CABI, Wallingford, UK, pp 35–56
Booysen E, Dicks LMT (2020) Does the future of antibiotics lie in secondary metabolites produced by Xenorhabdus spp.? A review. Probiotics Antimicrob Proteins 12(4):1310–1320
Boszormenyi E, Ersek T, Fodor A, Fodor AM, Foldes LS, Hevesi M, Hogan JS, Katona Z, Klein MG, Kormany A, Pekar S, Szentirmai A, Sztaricskai F, Taylor RAJ (2009) Isolation and activity of Xenorhabdus antimicrobial compounds against the plant pathogens Erwinia amylovora and Phytophthora nicotianae. J Appl Microbiol 107:764–759
Bowen DJ, Ensign JC (1998) Purification and characterization of a high-molecular-weight insecticidal protein complex produced by the entomopathogenic bacterium Photorhabdus luminescens. Appl Environ Microbiol 64(8):3029–3035
Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R, ffrench-Constant RH (1998) Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280:2129–2132
Bussaman P, Sermswan RW, Grewal PS (2006) Toxicity of the entomopathogenic bacteria Photorhabdus and Xenorhabdus to the mushroom mite (Luciaphorus sp.; Acari: Pygmephoridae). Biocontrol Sci Technol 16(3):245–256
Bussaman P, Sobanboa S, Grewal PS, Chandrapatya A (2009) Pathogenicity of additional strains of Photorhabdus and Xenorhabdus (Enterobacteriaceae) to the mushroom mite Luciaphorus perniciosus (Acari: Pygmephoridae). App Entomol Zool 44(2):293–299
Bussaman P, Sa-Uth C, Rattanasena P, Chandrapatya A (2012) Acaricidal activities of whole cell suspension, cell-free supernatant, and crude cell extract of Xenorhabdus stokiae against mushroom mite (Luciaphorus sp.). J Zhejiang Uni Sci B 13(4):261–6
Cai X, Nowak S, Wesche F, Bischoff I, Kaiser M, Fürst R, Bode HB (2017) Entomopathogenic bacteria use multiple mechanisms for bioactive peptide library design. Nat Chem 9:379–386
Cevizci D, Ulug D, Cimen H, Touray M, Hazir S, Cakmak I (2020) Mode of entry of secondary metabolites of the bacteria Xenorhabdus szentirmaii and X. nematophila into Tetranychus urticae, and their toxicity to the predatory mites Phytoseiulus persimilis and Neoseiulus californicus. J Invertebr Pathol 174:107418
Chacón Orozco JG, CJr B, Shapiro Ilan DI, Hazir S, Leite LG, Harakava R (2020) Antifungal activity of Xenorhabdus spp. and Photorhabdus spp. against the soybean pathogenic Sclerotinia sclerotiorum. Sci Rep 10:20649
Challinor VL, Bode HB (2015) Bioactive natural products from novel microbial sources. Ann N Y Acad Sci 1354(1):82–97
Chang DZ, Serra L, Lu D, Mortazavi A, Dillman AR (2019) A core set of venom proteins is released by entomopathogenic nematodes in the genus Steinernema. PLoS Pathog 15(5):e1007626
Chen G, Dunphy GB, Webster JM (1994) Antifungal activity of two Xenorhabdus species and Photorhabdus luminescens, bacteria associated with the nematodes Steinernema species and Heterorhabditis megidis. Biol Control 4(2):157–162
Cheng SS, Liu JY, Huang CG, Hsui YR, Chen WJ, Chang ST (2009) Insecticidal activities of leaf essential oils from Cinnamomum osmophloeum against three mosquito species. Bioresour Technol 100:457–464
Cimen H, Touray M, Gulsen SH, Erincik O, Wenski SL, Bode HB, Shapiro-Ilan DI, Hazir S (2021) Antifungal activity of different Xenorhabdus and Photorhabdus species against various fungal phytopathogens and identification of the antifungal compounds from X. szentirmaii. Appl Microbiol Biotechnol 105(13):5517–5528
Clifford MN (1999) Chlorogenic acids and other cinnamates–nature, occurrence and dietary burden. J Sci Food Agric 79(3):362–372
Council of Europe (2000) Partial agreement in the social and public health field. Chemically-defined flavouring substances. Groups: 2.2 aromatic alcohols, 5.2 aromatic aldehydes, 8.2 aromatic acids. Pages 74, 119, 205. Numbers, 22, 65, 102. Council of Europe Publishing, Strasbourg
Daborn PJ, Waterfield N, Silva CP, Au CP, Sharma S, ffrench-Constant RH (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Nat Acad Sci 99(16):10742–10747
Donmez Ozkan H, Cimen H, Ulug D, Wenski S, Yigit Ozer S, Telli M, Aydin N, Bode HB, Hazir S (2019) Nematode-associated bacteria: production of antimicrobial agent as a presumptive nominee for curing endodontic infections caused by Enterococcus faecalis. Front Microbiol 10:2672
Dreyer J, Malan AP, Dicks LMT (2018) Bacteria of the genus Xenorhabdus, a novel source of bioactive compounds. Front Microbiol 9:1–14
Ensign JC, Lan Q, Dyer D (2014) Mosquitocidal Xenorhabdus, lipopeptide and methods. US Patent US20140274880A1
Eom S, Park Y, Kim H, Kim Y (2014) Development of a high efficient “dual Bt-plus” insecticide using a primary form of an entomopathogenic bacterium, Xenorhabdus nematophila. J Microbiol Biotechnol 24:507–521
Eroglu C, Cimen H, Ulug D, Karagoz M, Hazir S, Cakmak I (2019) Acaricidal effect of cell-free supernatants from Xenorhabdus and Photorhabdus bacteria against Tetranychus urticae (Acari: Tetranychidae). J Invertebr Pathol 1(160):61–66
European Chemicals Agency (ECHA) Registered substances, benzaldehyde (CAS number: 100–52–7) (EC Number: 202–860–4)
Fang XL, Li ZZ, Wang YH, Zhang X (2011) In vitro and in vivo antimicrobial activity of Xenorhabdus bovienii YL002 against Phytophthora capsici and Botrytis cinerea. J Appl Microbiol 111(1):145–154
Fang X, Zhang M, Tang Q, Wang Y, Zhang X (2014) Inhibitory effect of Xenorhabdus nematophila TB on plant pathogens Phytophthora capsici and Botrytis cinerea in vitro and in planta. Sci Rep 4:1–7
FAO (2021) The State of Food and Agriculture 2021. Making agrifood systems more resilient to shocks and stresses. Rome, FAO
Fisher MC, Hawkins NJ, Sanglard D, Gurr SJ (2018) Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360:739–742
Fisher MC, Gurr SJ, Cuomo CA, Blehert DS, Jin H, Stukenbrock EH, Stajich JE, Kahmann R, Boone C, Denning DW, Gow N, Klein BS, Kronstad JW, Sheppard DC, Taylor JW, Wright GD, Heitman J, Casadevall A, Cowen LE (2020) Threats posed by the fungal kingdom to humans wildlife and agriculture. mBio 11(3):e00449-20
Forst S, Dowds B, Boemare N, Stackebrandt E (1997) Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51:47–72
Fuchs SW, Grundmann F, Kurz M, Kaiser M, Bode HB (2014) Fabclavines: bioactive peptide-polyketide-polyamino hybrids from Xenorhabdus. ChemBioChem 15(4):512–516
Fukruksa C, Yimthin T, Suwannaroj M, Muangpat P, Tandhavanant S, Thanwisai A, Vitta A (2017) Isolation and identification of Xenorhabdus and Photorhabdus bacteria associated with entomopathogenic nematodes and their larvicidal activity against Aedes aegypti. Parasites Vectors 10(1):1–10
Furgani G, Boszormenyi E, Fodor A, Fodor AM, Forst S, Hogan J, Katona Z, Klein MG, Stackebrandt E, Szentirmai A, Sztaricskai F, Wolf S (2008) Xenorhabdus antibiotics: a comparative analysis and potential utility for controlling mastitis caused by bacteria. J Appl Microbiol 104:745–758
García-Lara S, Serna Saldivar SO (2016) Insect pests. In: Caballero B, Finglas P, Toldrá F (eds) Encyclopedia of food and health. Academic Press, pp 432–436
Grundmann F, Kaiser M, Schiell M, Batzer A, Kurz M, Thanwisai A, Chantratita N, Bode HB (2014) Antiparasitic chaiyaphumines from entomopathogenic Xenorhabdus sp PB61.4. J Nat Prod 77(4):779–783
Gu LS, Kim JR, Ling J, Choi KK, Pashley DH, Tay FR (2009) Review of contemporary irrigant agitation techniques and devices. J Endod 35:791–804
Gulcu B (2022) Field efficacy of trans-cinnamic acid against powdery mildew disease, Erysiphe corylacearum, in hazelnut fields. Phytoparasitica 29:1–6
Gulsen SH, Tileklioğlu E, Bode E, Cimen H, Ertabaklar H, Ulug D, Ertug S, Wenski SL, Touray M, Hazir C, Bilecenoglu DK (2022) Antiprotozoal activity of different Xenorhabdus and Photorhabdus bacterial secondary metabolites and identification of bioactive compounds using the easyPACId approach. Sci Rep
Guo S, Zhang S, Fang X, Liu Q, Gao J, Bilal M, Wang Y, Zhang X (2017) Regulation of antimicrobial activity and xenocoumacins biosynthesis by pH in Xenorhabdus nematophila. Microb Cell Factories 16(1):1–14
Guzman JD (2014) Natural cinnamic acids, synthetic derivatives and hybrids with antimicrobial activity. Molecules 19(12):19292–19349
Hapeshi A, Waterfield NR (2016) Photorhabdus asymbiotica as an insect and human pathogen. Curr Top Microbiol Immunol 402:159–177
Hazir S, Kaya HK, Stock SP, Keskin N (2003) Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turk J Biol 27:181–202
Hazir S, Shapiro-Ilan DI, Bock CH, Hazir C, Leite LG, Hotchkiss MW (2016) Relative potency of culture supernatants of Xenorhabdus and Photorhabdus spp. on growth of some fungal phytopathogens. Eur J Plant Pathol 146:369–381
Hazir S, Shapiro-Ilan DI, Bock CH, Leite LG (2017) Trans-cinnamic acid and Xenorhabdus szentirmaii metabolites synergize the potency of some commercial fungicides. J Invertebr Pathol 145:1–8
Hinchliffe SJ, Hares MC, Dowling AJ (2010) Insecticidal toxins from the Photorhabdus and Xenorhabdus bacteria. The Open Toxinol J 3:83–100
Houard J, Aumelas A, Noel T, Pages S, Givaudan A, Fitton- Ouhabi V, Villain-Guillot P, Gualtieri M (2013) Cabanillasin, a new antifungal metabolite, produced by entomopathogenic Xenorhabdus cabanillasii JM26. J Antibiot 66:617–620
İmai Y, Meyer KJ, Iinishi A, Favre-Godal Q, Green R, Manuse S, Caboni M, Mori M, Niles S, Ghiglieri M, Honrao C, Ma X, Guo JJ, Makriyannis A, Linares-Otoya L, Böhringer N, Wuisan ZG, Kaur H, Wu R, Mateus A, Typas A, Savitski MM, Espinoza JL, O’Rourke A, Nelson KE, Hiller S, Noinaj N, Schaberle TF, D’Onofrio A, Lewis K (2019) A new antibiotic selectively kills gram-negative pathogens. Nature 576(7787):459–464
Incedayi G, Cimen H, Ulug D, Touray M, Bode E, Bode HB, Orenlili Yaylagul E, Hazir S, Cakmak I (2021) Relative potency of a novel acaricidal compound from Xenorhabdus, a bacterial genus mutualistically associated with entomopathogenic nematodes. Sci Rep 11:11253
JECFA (Joint Expert Committee on Food Additives) (2000) Cinnamyl alcohol and related flavouring agents. WHO Food Additives Series: 46. Prepared by the fifty-fifth meeting of the Joint FAO/WHO Expert Committee on Food Additives, June 6–15, Geneva, Switzerland. World Health Organization
Joyce SA, Brachmann AO, Glazer I, Lango L, Schwär G, Clarke DJ, Bode HB (2008) Bacterial biosynthesis of a multipotent stilbene. Angew Chem Int Ed 47(10):1942–1945
Jung S, Kim Y (2006) Synergistic effect of Xenorhabdus nematophila K1 and Bacillus thuringiensis subsp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Biol Control 39(2):201–209
Jung S, Kim Y (2007) Synergistic effect of entomopathogenic bacteria (Xenorhabdus sp. and Photorhabdus temperata ssp. temperata) on the pathogenicity of Bacillus thuringiensis ssp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Environ Entomol 35(6):1584–1589
Kainz K, Bauer MA, Madeo F, Carmona-Gutierrez D (2020) Fungal infections in humans: the silent crisis. Microb Cell 7(6):143
Kajla MK (2019) Symbiotic bacteria as potential agents for mosquito control. Trends Parasitol 36(1):4–7
Katz L, Baltz RH (2016) Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 43(3):155–176
Kaya HK, Aguillera MM, Alumai A, Choo HY, De la Torre M, Fodor A, Ganguly S, Hazir S, Lakatos T, Pye A, Wilson M, Yamanaka S, Yang H, Ehlers RU (2006) Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world. Biol Control 38:134–155
Kim E, Jeoung S, Park Y, Kim K, Kim Y (2015) A novel formulation of Bacillus thuringiensis for the control of brassica leaf beetle, Phaedon brassicae (Coleoptera: Chrysomelidae). J Econ Entomol 108:2556–2565
Kim IH, Aryal SK, Aghai DT, Casanova-Torres ÁM, Hillman K, Kozuch MP, Mans EJ, Mauer TJ, Ogier JC, Ensign JC, Gaudriault S, Goodman WG, Goodrich-Blair H, Dillman AR (2017) The insect pathogenic bacterium Xenorhabdus innexi has attenuated virulence in multiple insect model hosts yet encodes a potent mosquitocidal toxin. BMC Genom 18(1):927
Kim IH, Ensign J, Kim DY, Jung HY, Kim NR, Choi BH, Park SM, Lan Q, Goodman WG (2017) Specificity and putative mode of action of a mosquito larvicidal toxin from the bacterium Xenorhabdus innexi. J Invertebr Pathol 149:21–28
Koppenhöfer AM, Shapiro-Ilan DI, Hiltpold I (2020) Entomopathogenic nematodes in sustainable food production. Front Sustain Food Syst 4:125
Korošec B, Sova M, Turk S, Kraševec N, Novak M, Lah L, Stojan J, Podobnik B, Berne S, Zupanec N, Bunc M (2014) Antifungal activity of cinnamic acid derivatives involves inhibition of benzoate 4-hydroxylase (CYP 53). J Appl Microbiol 116(4):955–966
Lacey LA (2007) Bacillus thuringiensis sero variety israelensis and Bacillus sphaericus for mosquito control. J Am Mosq Control Assoc 23(2):133–163
Lewis EE, Hazir S, Hodson A, Gulcu B (2015) Trophic relationships of entomopathogenic nematodes in agricultural habitats. In: Campos-Herrera R (ed) Nematode pathogenesis of insects and other pests. Springer, International Publishing Switzerland, pp 139–163
Liu D, Burton S, Glancy T, Li ZS, Hampton R, Meade T, Merlo DJ (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat Biotechnol 21:1222–1228
Machado RA, Thönen L, Arce C, Theepan V, Prada F, Wüthrich D, Robert CA, Vogiatzaki E, Shi YM, Schaeren OP, Notter M (2020) Engineering bacterial symbionts of nematodes improves their biocontrol potential to counter the western corn rootworm. Nat Biotechnol 38(5):600–608
Masschelein J, Clauwers C, Awodi UR, Stalmans K, Vermaelen W, Lescrinier E, Aertsen A, Michiels C, Challis GL, Lavigne R (2015) A combination of polyunsaturated fatty acid, nonribosomal peptide and polyketide biosynthetic machinery is used to assemble the zeamine antibiotics. Chem Sci 6(2):923–929
McInerney BV, Taylor WC, Lacey MJ, Akhurst RJ, Gregson RP (1991) Biologically active metabolites from Xenorhabdus spp. Part 2. Benzopyran-1-one derivatives with gastroprotective activity. J Nat Prod 54:785–795
Mollah MI, Kim Y (2020) Virulent secondary metabolites of entomopathogenic bacteria genera, Xenorhabdus and Photorhabdus, inhibit phospholipase A2 to suppress host insect immunity. BMC Microbiol 20:359
Nermuť J, Zemek R, Mráček Z, Palevsky E, Půža V (2019) Entomopathogenic nematodes as natural enemies for control of Rhizoglyphus robini (Acari: Acaridae)? Biol Control 1(128):102–110
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Public Health Front 4:148
Oerke EC (2006) Crop losses to pests. J Agric Sci 144(1):31–43
Park Y (2015) Entomopathogenic bacterium, Xenorhabdus nematophila and Photorhabdus luminescens, enhances Bacillus thuringiensis Cry4Ba toxicity against yellow fever mosquito, Aedes aegypti (Diptera: Culicidae). J Asia Pac Entomol 18(3):459–463
Park D, Ciezki K, Van Der Hoeven R, Singh S, Reimer D, Bode HB, Forst S (2009) Genetic analysis of xenocoumacin antibiotic production in the mutualistic bacterium Xenorhabdus nematophila. Mol Microbiol 73(5):938–949
Park Y, Kyo Jung J, Kim Y (2016) A mixture of Bacillus thuringiensis subsp. israelensis with Xenorhabdus nematophila-cultured broth enhances toxicity against mosquitoes Aedes albopictus and Culex pipiens pallens (Diptera: Culicidae). J Econ Entomol 109(3):1086–1093
Peng Y, Li SJ, Yan J, Tang Y, Cheng JP, Gao AJ, Yao X, Ruan JJ, Xu BL (2021) Research progress on phytopathogenic fungi and their role as biocontrol agents. Front Microbiol 12
Raja RK, Arun A, Touray M, Gulsen SH, Cimen H, Gulcu B, Hazir C, Aiswarya D, Ulug D, Cakmak I, Kaya HK, Hazir S (2021) Antagonists and defense mechanisms of entomopathogenic nematodes and their mutualistic bacteria. Biol Control 152:104452
Reen FJ, Romano S, Dobson AD, O’Gara F (2015) The sound of silence: activating silent biosynthetic gene clusters in marine microorganisms. Mar Drugs 13(8):4754–4783
Reimer D, Luxenburger E, Brachmann AO, Bode HB (2009) A new type of pyrrolidine biosynthesis is involved in the late steps of xenocoumacin production in Xenorhabdus nematophila. ChemBioChem 10:1997–2001
Reinheimer C, Büttner D, Proschak E, Bode HB, Kempf VA, Wichelhaus TA (2018). Anti-tubercular activity of a natural stilbene and its synthetic derivatives. GMS Infect Dis 6
Riviere C, Pawlus AD, Merillon JM (2012) Natural stilbenoids: distribution in the plant kingdom and chemotaxonomic interest in Vitaceae. Nat Prod Rep 29(11):1317–1333
Ruwizhi N, Aderibigbe BA (2020) Cinnamic acid derivatives and their biological efficacy. Int J Mol Sci 21(16):5712
San-Blas E, Carrillo Z, Parra Y (2012) Effect of Xenorhabdus and Photorhabdus bacteria and their exudates on Moniliophthora roreri. Arch Phytopathol Plant Protect 45:1950–1967
San-Blas E, Parra Y, Carrillo Z (2013) Effect of Xenorhabdus and Photorhabdus bacteria (Enterobacteriales: Enterobacteriaceae) and their exudates on the apical rotten fruit disease caused by Dothiorella sp. in guava (Psidium guajava). Arch Phytopathol Plant Protect 46:2294–2303
Savary S, Teng PS, Willocquet L, Nutter FW Jr (2006) Quantification and modeling of crop losses: a review of purposes. Annu Rev Phytopathol 44:89–112
Savary S, Ficke A, Aubertot JN, Hollier C (2012) Crop losses due to diseases and their implications for global food production losses and food security. Food Secur 4:519–537
Scholte EJ, Takken W, Knols BG (2007) Infection of adult Aedes aegypti and Ae. albopictus mosquitoes with the entomopathogenic fungus Metarhizium anisopliae. Acta Trop 102:151–158
Seo S, Lee S, Hong Y, Kim Y (2012) Phospholipase A2 inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl Environ Microbiol 78(11):3816–3823
Sergeant M, Baxter L, Jarrett P, Shaw E, Ousley M, Winstanley C, Morgan JAW (2006) Identification, typing, and insecticidal activity of Xenorhabdus isolates from entomopathogenic nematodes in United Kingdom soil and characterization of the xpt toxin loci. Appl Environ Microbiol 72:5895–5907
Shah FA, Abdoarrahem MM, Berry C, Touray M, Hazir S, Butt TM (2021) Indiscriminate ingestion of entomopathogenic nematodes and their symbiotic bacteria by Aedes aegypti larvae: a novel strategy to control the vector of Chikungunya, dengue and yellow fever. Turk J Zool 45:372–383
Shapiro-Ilan DI, Reilly CC, Hotchkiss MW (2009) Suppressive effects of metabolites from Photorhabdus and Xenorhabdus spp. on phytopathogens of peach and pecan. Arch Phytopathol Plant Protect 42:715–728
Shapiro-Ilan DI, Bock CH, Hotchkiss MW (2014) Suppression of pecan and peach pathogens on different substrates using Xenorhabdus bovienii and Photorhabdus luminescens. Biol Control 77:1–6
Shapiro-Ilan DI, Hazir S, Glazer I (2019) Advances in use of entomopathogenic nematodes in IPM. In: Kogan M, Higley L (eds) Integrated management of insect pests: current and future developments. Burleigh Dodds Science Publishing, London, pp 649–678
Shapiro-Ilan D, Hazir S, Glaser I (2020) Advances in use of entomopathogenic nematodes in integrated pest management. In: Kogan M, Heinrichs EA (eds) Integrated management of insect pests: current and future developments. Burleigh Dodds Science Publishing, Cambridge, UK, pp 91–105
Sharma K, Walia S, Ganguli S, Kundu A (2016) Analytical characterization of secondary metabolites from Indian Xenorhabdus species the symbiotic bacteria of entomopatathogenic nematode (Steinernema spp.) as antifungal agent. Natl Acad Sci Lett 39:175–180
Sharma A, Shukla A, Attri K, Kumar M, Kumar P, Suttee A, Singh G, Barnwal RP, Singla N (2020) Global trends in pesticides: a looming threat and viable alternatives. Ecotox Environ Saf 201:110812
Shawer R, Donati I, Cellini A, Spinelli F, Mori N (2018) Insecticidal activity of Photorhabdus luminescens against Drosophila suzukii. Insects 9(4):148
Shen T, Wang XN, Lou HX (2009) Natural stilbenes: an overview. Nat Prod Rep 26(7):916–935
Shi YM, Bode HB (2018) Chemical language and warfare of bacterial natural products in bacteria–nematode–insect interactions. Nat Prod Rep 35:309–335
Shi H, Zeng H, Yang X, Zhao J, Chen M, Qiu D (2012) An insecticidal protein from Xenorhabdus ehlersii triggers prophenoloxidase activation and hemocyte decrease in Galleria mellonella. Curr Microbiol 64:604–610
Shi H, Zeng H, Yang X, Liu Z, Qiu D (2013) An insecticidal protein from Xenorhabdus ehlersii stimulates the innate immune response in Galleria mellonella. World J Microbiol Biotechnol 29:1705–1711
Shi D, An R, Zhang W, Zhang G, Yu Z (2017) Stilbene derivatives from Photorhabdus temperata SN259 and their antifungal activities against phytopathogenic fungi. J Agric Food Chem 65(1):60–65
Silva OS, Prado GR, Da Silva JLR, Silva CE, Da Costa M, Heermann R (2013) Oral toxicity of Photorhabdus luminescens and Xenorhabdus nematophila (Enterobacteriaceae) against Aedes aegypti (Diptera: Culicidae). Parasitol Res 112:2891–2896
Silva LRJ, Undurraga SF, Eugênio SC, da Costa M, Heermann R, Santos da Silva O (2017) Larvicidal and growth-inhibitory activity of entomopathogenic bacteria culture fluids against Aedes aegypti (Diptera: Culicidae). J Econ Entomol 110(2):378–385
Silva WJ, Pilz-Júnior HL, Heermann R, Silva OS (2020) The great potential of entomopathogenic bacteria Xenorhabdus and Photorhabdus for mosquito control: a review. Parasit Vectors 13(1):1–14
Sirero JA, Rodríguez ML, Mena S, Asensi MA, Estrela JM, Ortega AL (2016) Role of natural stilbenes in the prevention of cancer. Oxid Med Cell Longev 2016:3128951
Spielman A, Pollack RJ, Kiszewski AE, Telford SR III (2001) Issues in public health entomology. Vector-Borne Zoonotic Dis 1(1):3–19
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43(1):83–116
Sun S, Hoy MJ, Heitman J (2020) Fungal pathogens. Curr Biol 30(19):R1163–R1169
Talbot NJ (2010) Living the sweet life: how does a plant pathogenic fungus acquire sugar from plants? PLoS Biol 8(2):e1000308
Tang FH, Lenzen M, McBratney A, Maggi F (2021) Risk of pesticide pollution at the global scale. Nat Geosci 14(4):206–210
Tobias NJ, Wolff H, Djahanschiri B, Grundmann F, Kronenwerth M, Shi YM, Simonyi S, Grün P, Shapiro-Ilan D, Pidot SJ, Stinear TP (2017) Natural product diversity associated with the nematode symbionts Photorhabdus and Xenorhabdus. Nat Microbiol 2(12):1676–1685
Tobias NJ, Shi YM, Bode HB (2018) Refining the natural product repertoire in entomopathogenic bacteria. Trends Microbiol 26(10):833–840
Ullah I, Khan AL, Ali L, Khan AR, Waqas M, Hussain J, Lee IJ, Shin JH (2015) Benzaldehyde as an insecticidal, antimicrobial, and antioxidant compound produced by Photorhabdus temperata M1021. J Microbiol 53(2):127–133
van der Meijden E (2015) Herbivorous insects—a threat for crop production. In: Lugtenberg B (Ed) Principles of plant-microbe interactions. Springer, Cham
Vicente-Díez I, Blanco-Pérez R, Chelkha M, Puelles M, Pou A, Campos-Herrera R (2021) Exploring the use of entomopathogenic nematodes and the natural products derived from their symbiotic bacteria to control the grapevine moth, Lobesia botrana (Lepidoptera: Tortricidae). Insects 12(11):1033
Vitta A, Thimpoo P, Meesil W, Yimthin T, Fukruksa C, Polseela R, Mangkit B, Tandhavanant S, Thanwisai A (2018) Larvicidal activity of Xenorhabdus and Photorhabdus bacteria against Aedes aegypti and Aedes albopictus. Asian Pac J Trop Biomed 8(1):31–36
Wagutu GK, Mwangi W, Waturu CN (2017) Entomopathogenic bacteria: Xenorhabdus spp and Photorhabdus spp from Steinernema karii and Heterorhabditis indica for the control of mosquito larvae. J Agric Sci Technol 18(2):21–38
Wang H, Dong H, Qian H, Xia R, Cong B (2013) Isolation, bioassay and characterisation of Xenorhabdus sp. SY5, a highly virulent symbiotic bacterium of an entomopathogenic nematode isolated from China. Nematol 15:153–163
Wang Y, Sun Y, Wang J, Zhou M, Wang M, Feng J (2019) Antifungal activity and action mechanism of the natural product cinnamic acid against Sclerotinia sclerotiorum. Plant Dis 103(5):944–950
Waterfield NR, Bowen DJ, Fetherston JD, Perry RD (2001) The tc genes of Photorhabdus: a growing family. Trends Microbiol 9(4):185–191
Waterfield NR, Daborn PJ, Dowling AJ, Yang G, Hares M, ffrench-Constant RH (2003) The insecticidal toxin makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen. FEMS Microbiol Lett 229(2):265–270
Webster JM, Chen G, Hu K, Li J (2002) Bacterial metabolites. In: Gaugler R (ed) Entomopathogenic nematology. CABI International, London, pp 99–114
Wenski SL, Kolbert D, Grammbitter GL, Bode HB (2019) Fabclavine biosynthesis in X. szentirmaii: shortened derivatives and characterization of the thioester reductase FclG and the condensation domain-like protein FclL. J Ind Microbiol Biotech 46(3–4):565–72
Wenski SL, Cimen H, Berghaus N, Fuchs SW, Hazir S, Bode HB (2020) Fabclavine diversity in Xenorhabdus bacteria. Beilstein J Org Chem 16(1):956–965
Xiao Y, Meng F, Qiu D, Yang X (2012) Two novel antimicrobial peptides purified from the symbiotic bacteria Xenorhabdus budapestensis NMC-10. Peptides 35:253–260
Xing-zhong LU, Dan-shu S, Chun-zhi G, Xiao-mei T, Yu-hui B (2016) Isolation and identification of secondary metabolites from Xenorhabdus budapestensis. Nat Prod Res Dev 28:828–832
Xue L, Liu G (2019) Introduction to global food losses and food waste. In: Galanakis CM (ed) Saving food, production, supply chain, food waste, and food consumption. Academic Press, pp 1–31
Yang X, Qiu D, Yang H, Liu Z, Zeng H, Yuan J (2011) Antifungal activity of xenocoumacin 1 from Xenorhabdus nematophilus var. pekingensis against Phytophthora infestans. World J Microbiol Biotechnol 27(3):523–528
Yooyangket T, Muangpat P, Polseela R, Tandhavanant S, Thanwisai A, Vitta A (2018) Identification of entomopathogenic nematodes and symbiotic bacteria from Nam Nao National Park in Thailand and larvicidal activity of symbiotic bacteria against Aedes aegypti and Aedes albopictus. PLoS One 13:e0195681
Zhang J, Li L, Lv Q, Yan L, Wang Y, Jiang Y (2019) The fungal CYP51s: their functions, structures, related drug resistance, and inhibitors. Front Microbiol 10:691
Zhao L, Kaiser M, Bode HB (2018) Rhabdopeptide/xenortide-like peptides from Xenorhabdus innexi with terminal amines showing potent antiprotozoal activity. Org Lett 20(17):5116–5120
Zhao L, Vo TD, Kaiser M, Bode HB (2020) Phototemtide A, a cyclic lipopeptide heterologously expressed from Photorhabdus temperata Meg1, shows selective antiprotozoal activity. ChemBioChem 21(9):1288–1292
Zhou J, Zhang H, Wu J, Liu Q, Xi P, Lee J, Liao J, Jiang Z, Zhang LH (2011) A novel multidomain polyketide synthase is essential for zeamine production and the virulence of Dickeya zeae. Mol Plant Microbe Interact 24:1156–1164
Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, Payraudeau S, Rasmussen JJ, Rohr J, Scharmüller A, Smalling K, Stehle S, Schulz R, Schäfer RB (2019) Fungicides: an overlooked pesticide class? Environ Sci Technol 53(7):3347–3365
Ahantarig A, Chantawat N, Waterfield NR, Ffrench-Constant R, Kittayapong P (2009) PirAB toxin from Photorhabdus asymbiotica as a larvicide against dengue vectors. Appl Environ Microbiol 75(13):4627–4629
Acknowledgements
We thank Dr. Harry K. Kaya (University of California, Davis, CA, USA) for editing the manuscripts and for his helpful comments.
Author information
Authors and Affiliations
Contributions
HC, MT, SHG, and SH designed the research and wrote this manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interests
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
About this article
Cite this article
Cimen, H., Touray, M., Gulsen, S.H. et al. Natural products from Photorhabdus and Xenorhabdus: mechanisms and impacts. Appl Microbiol Biotechnol 106, 4387–4399 (2022). https://doi.org/10.1007/s00253-022-12023-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-022-12023-9