Progress in Plant Protection

Bakterie symbiotyczne związane z nicieniami owadobójczymi z rodziny Steinernematidae i Heterorhabditidae w biologicznej ochronie roślin
Symbiotic bacteria associated with entomopathogenic nematodes in the families Steinernematidae and Heterorhabditidae in biological plant protection

Katarzyna Dubaj, e-mail: k.dubaj@iorpib.poznan.pl

Instytut Ochrony Roślin – Państwowy Instytut Badawczy, Władysława Węgorka 20, 60-318 Poznań, Polska

Anna Filipiak, e-mail: a.filipiak@iorpib.poznan.pl

Instytut Ochrony Roślin – Państwowy Instytut Badawczy, Władysława Węgorka 20, 60-318 Poznań, Polska
Abstract

Nicienie owadobójcze z rodziny Steinernematidae (Filipjev, 1934) i Heterorhabditidae (Poinar, 1976) obejmują ponad 90 gatunkówi związane są symbiotycznie z bakteriami z rodzaju Xenorhabdus (Poinar, 1979) i Photorhabdus (Boemare, 1993). Nicienie te uznane są za obiecujące czynniki biologicznego zwalczania wielu gatunków owadów szkodliwych w uprawach. Nicienie pełnią rolę wektorów, umożli­wiając bakteriom wniknięcie do ciała owada, natomiast bakterie po zabiciu owada zapewniają nicieniom stały dostęp do pożywienia oraz środowisko do rozmnażania. Bakterie Xenorhabdus i Photorhabdus wykazują bliskie pokrewieństwo filogenetyczne, jednak różnią się specyficznością względem żywicieli oraz wytwarzaniem różnych antybiotyków i toksyn owadobójczych. Dzięki tej symbiozie, ze względu na silne właściwości owadobójcze oraz szeroki zakres działania, z powodzeniem zostały wdrożone w programach integrowanej ochrony roślin przed szkodnikami na całym świecie. W pracy przedstawiono przegląd literatury dotyczącej symbiozy między bakteriami a nicienia­mi oraz ich zależność w biologicznej ochronie roślin.

 

Entomopathogenic nematodes in the family Steinernematidae (Filipjev, 1934) and Heterorhabditidae (Poinar, 1976) include more than 90 species and are symbiotically related to bacteria in the genera Xenorhabdus (Poinar, 1979) and Photorhabdus (Boemare, 1993). These nematodes are recognized as promising agents for biological control of many insect pest species in crops. The nematodes act as vectors, allowing the bacteria to enter the insect’s body, while the bacteria, after killing the insect, provide the nematodes with continued access to food and an environment for reproduction. Xenorhabdus and Photorhabdus bacteria are closely related phylogenetically, but differ in their host specificity and production of different antibiotics and insecticidal toxins. Due to this symbiosis, they have been successfully implemented in integrated pest management programs around the world due to their strong insecticidal properties and wide range of action. This work presents a review of the symbiosis between bacteria and nematodes and their relationship in biological plant protec­tion.

Key words
nicienie owadobójcze; bakterie Xenorhabdus i Photorhabdus; symbioza mutualistyczna;  entomopathogenic nematodes; Xenorhabdus and Photorhabdus bacteria; mutualistic symbiosis
References

Abd-Elgawad M.M.M. 2022. Xenorhabdus spp.: an overview of the useful facets of mutualistic bacteria of entomopathogenic nematodes. Life 12 (9): 1360. DOI: 10.3390/life12091360

 

Abd El-Raheem A.M., Elmasry A.M.A., Elbrense H., Vergara-Pineda S. 2022. Photorhabdus and Xenorhabdus as symbiotic bac­teria for bio-control housefly (Musca domestica L.). Pakistan Journal of Biological Sciences 25 (7): 586–601. DOI: 10.3923/ pjbs.2022.586.601

 

Akhurst R.J. 1980. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. Microbiology 121 (2): 303–309. DOI: 10.1099/00221287- 121-2-303

 

Akhurst R.J., Boemare N.E. 1988. A numerical taxonomic study of the genus Xenorhabdus (enterobacteriacea) and propo­sed elevation of the subspecies of X. nematophilus to species. Journal of General Microbiology 134 (7): 1835–1845. DOI: 10.1099/00221287-134-7-1835

 

Akhurst R.J., Boemare N.E. 1993. Validation of the publication of new names and new combinations previously effectively publi­shed outside the IJSB: List no. 47. International Journal of Systematic and Evolutionary Microbiology 43 (4): 864–865. DOI: 10.1099/00207713-43-4-864

 

Askary T.H. 2010. Nematodes as biocontrol agents. s. 347–378. W: Sociology, Organic Farming, Climate Change and Soil Science (E. Lichtfouse, red.). Springer, Dordrecht, Netherlands. DOI: 10.1007/978-90-481-3333-8_13

 

Boemare N., Laumond C., Mauleon H. 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and verte­brate safety. Biocontrol Science and Technology 6 (3): 333–346. DOI: 10.1080/09583159631316

 

Chaston J.M., Suen G., Tucker S.L., Andersen A.W., Bhasin A., Bode E., Bode H.B., Brachmann A.O., Cowles C.E., Cowles K.N., Darby C., de Léon L., Drace K., Du Z., Givaudan A., Herbert Tran E.E., Jewell K.A., Knack J.J., Krasomil-Osterfeld K.C., Go­odrich-Blair H. 2011. The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes. PLOS ONE 6 (11): e27909. DOI: 10.1371/journal.pone.0027909

 

Ciche T.A., Ensign J.C. 2003. For the insect pathogen Photorhabdus luminescens, which end of a nematode is out? Applied and Environmental Microbiology 69 (4): 1890–1897. DOI: 10.1128/AEM.69.4.1890-1897.2003

 

Dowds B.C., Peters A. 2002. Virulence mechanisms. s. 79–98. W: Entomopathogenic Nematology (R. Gaugler, red.). CABI Publi­shing, Wallingford, UK. ISBN 9780851995670. DOI: 10.1079/9780851995670.0099

 

Duncan L.W., Graham J.H., Dunn D.C., Zellers J., McCoy C.W., Nguyen K. 2003. Incidence of endemic entomopathogenic ne­matodes following application of Steinernema riobrave for control of Diaprepes abbreviatus. Journal of Nematology 35 (2): 178–186.

 

Ekspertyza 2021. Zwiększenie efektywności integrowanej ochrony rzepaku ozimego zgodnie z założeniami Europejskiego Zielo­nego Ładu. Wydanie II (M. Mrówczyński, red.). Polskie Stowarzyszenie Producentów Oleju, Instytut Ochrony Roślin – Pań­stwowy Instytut Badawczy, 182 ss.

 

Elbrense H., Elmasry A.M.A., Seleiman M.F., Al-Harbi M.S., El-Raheem A.M.A. 2021. Can symbiotic bacteria (Xenorhabdus and Photorhabdus) be more efficient than their entomopathogenic nematodes against pieris rapae and pentodon algerinus larvae? Biology 10 (10): 999. DOI: 10.3390/BIOLOGY10100999

 

Forst S., Dowds B., Boemare N., Stackebrandt E. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annual Review of Microbiology 51 (1): 47–72. DOI: 10.1146/annurev.micro.51.1.47

 

Forst S., Nealson K. 1996. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Mi­crobiological Reviews 60 (1): 21–43. DOI: 10.1128/mmbr.60.1.21-43.1996

 

Georgis R., Poinar Jr G.O. 1984. Greenhouse control of the black vine weevil Otiorhynchus sulcatus (Coleoptera: Curculio­nidae) by Heterorhabditid and Steinernematid nematodes. Environmental Entomology 13 (4): 1138–1140. DOI: 10.1093/ ee/13.4.1138

 

Guy A., Gaffney M., Kapranas A., Griffin C.T. 2017. Conditioning the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis by pre-application storage improves efficacy against black vine weevil, Otiorhynchus sulca­tus (Coleoptera: Curculionidae) at low and moderate temperatures. Biological Control 108: 40–46. DOI: 10.1016/j.biocon­trol.2017.02.005

 

Hinchliffe S.J. 2013. Insecticidal toxins from the Photorhabdus and Xenorhabdus bacteria. The Open Toxinology Journal 3 (1): 101–118. DOI: 10.2174/1875414701003010101

 

Imhoff J.F. 2005. Enterobacteriales. s. 587–850. W: Bergey’s Manual® of Systematic Bacteriology. Springer, Boston, MA. DOI: 10.1007/s13199-019-00660-0

 

Jaffuel G., Mäder P., Blanco-Perez R., Chiriboga X., Fliessbach A., Turlings T.C.J., Campos-Herrera R. 2016. Prevalence and activity of entomopathogenic nematodes and their antagonists in soils that are subject to different agricultural practices. Agri­culture, Ecosystems and Environment 230: 329–340. DOI: 10.1016/j.agee.2016.06.009

 

Journey A.M., Ostlie K.R. 2000. Biological control of the western cornrootworm (Coleoptera: Chrysomelidae) using the ento­mopathogenic nematode, Steinernema carpocapsae. Environmental Entomology 29 (4): 822–831. DOI: 10.1603/0046-225X- 29.4.822

 

Kowalska J. 2001. Próba zastosowania nicieni owadobójczych oraz metody integrowanej w zwalczaniu pędraków chrabąszcza majowego Melolontha melolontha L. w uprawie leśnej. [An attempt to use insect-killing nematodes and an integrated method to control May beetle Melolontha melolontha L. grubs in a young forest culture]. Sylwan 2: 89–95.

 

Kowalska J. 2006. Wzajemne powiązania pomiędzy nicieniami owadobójczymi, owadami i bakteriami oraz ich wykorzystanie w praktyce. [Entomopathogenic nematodes, insects, bacteria and their relationship used in practice]. Wiadomości Parazytolo­giczne 52 (2): 93–98.

 

Kruk K., Dzięgielewska M. 2019. Wykorzystanie nicieni owadobójczych w biologicznej ochronie roślin. [The use of enthomopa­thogenic nematodes in biological plant protection]. Młodzi Naukowcy 11: 72–76.

 

Lewis E.E., Grewal P.S. 2005. Interactions with plant-parasitic nematodes. s. 349–361. W: Nematodes as Biocontrol Agent (P.S. Grewal, R.U. Ehlers, D.I. Shapiro-Ilan, red.). CABI Publishing, Wallingford, UK. ISBN 9780851990170. DOI: 10.1079/9780851990170.0349

 

Liu J., Berry R., Poinar G., Moldenke A. 1997. Phylogeny of Photorhabdus and Xenorhabdus species and strains as determined by comparison of partial 16s rRNA gene sequences. International Journal of Systematic Bacteriology 47 (4): 948–951. DOI: 10.1099/00207713-47-4-948

 

Lortkipanidze M.A., Gorgadze O.A., Kajaia G.S., Gratiashvili N.G., Kuchava M.A. 2016. Foraging behavior and virulence of some entomopathogenic nematodes. Annals of Agrarian Science 14 (2): 99–103. DOI: 10.1016/j.aasci.2016.05.009

 

Martens E.C., Vivas E.I., Heungens K., Cowles C.E., Goodrich-Blair H. 2004. Investigating mutualism between entomopathogenic bacteria and nematodes. s. 447–462. W: Proceedings of the Fourth International Congress of Nematology. Brill in Spain, June 8–13, 2002. DOI: 10.1163/9789004475236_045

 

Matuska-Łyżwa J., Huruk S., Wiatr M. 2012. Możliwości wykorzystania rodzimych populacji nicieni entomopatogennych w zwalczaniu pędraków chrabąszczowatych (Melolonthinae). [Potential of autochthonicpopulation of entomopathogenic nematodes in application to control of cockchafer grubs (Melolonthinae)]. Proceedings of ECOpole 6 (1): 293–296. DOI: 10.2429/proc.2012.6(1)040

 

Mráček Z., Bečvář S., Kindlmann P., Jersáková J. 2005. Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biological Control 34 (1): 27–37. DOI: 10.1016/j.biocontrol.2005.03.023

 

Poinar G.O. 1990. Biology and taxonomy of Steinernematidae and Heterorhabditidae. s. 23–62. W: Entomopathogenic Nematodes in Biological Control (R. Gaugler, H.K. Kaya, red.). CRC Press, Boca Raton, FL, 381 ss. eBook ISBN 9781351071741. DOI: 10.1201/9781351071741

 

Qin X., Kao R., Yang H., Zhang G. 1998. Study on application of entomopathogenic nematodes of Steinernema bibionis and S. feltiae to control Anoplophora glabripennis and Holococerus insularis. Forest Research 1 (2): 179–185.

 

Sicard M., Tabart J., Boemare N.E., Thaler O., Moulia C. 2005. Effect of phenotypic variation in Xenorhabdus nematophila on its mutualistic relationship with the entomopathogenic nematode Steinernema carpocapsae. Parasitology 131 (5): 687–694. DOI: 10.1017/S0031182005008255

 

Simoes N., Rosa J.S. 1998. Pathogenicity of the complex Steinernema carpocapsae-Xenorhabdus nematophilus: molecular aspects related with the virulence. Pathogenicity of entomopathogenic nematodes versus insect defence mechanisms: impact on selec­tion of virulent strains. European Commission, Brussels: 73–83.

 

Skwiercz A.T., Zapałowska A. 2018. Entomopathogenic nematodes in the soil of forests and nurseries. Sylwan 162 (12): 1018– 1028.

 

Tailliez P., Laroui C., Ginibre N., Paule A., Pagès S., Boemare N. 2010. Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. lumine­scens subsp. thracensis as P. temperata subsp. thracensis comb. nov. International Journal of Systematic and Evolutionary Microbiology 60 (8): 1921–1937. DOI: 10.1099/ijs.0.014308-0

 

Testa A.M., Shields E.J. 2017. Low labor “in vivo” mass rearing method for entomopathogenic nematodes. Biological Control 106: 77–82. DOI: 10.1016/j.biocontrol.2017.01.002

 

Thanwisai A., Tandhavanant S., Saiprom N., Waterfield N.R., Ke Long P., Bode H.B., Peacock S.J., Chantratita N. 2012. Diversity of Xenorhabdus and Photorhabdus spp. and their symbiotic entomopathogenic nematodes from Thailand. PLOS ONE 7 (9): e43835. DOI: 10.1371/journal.pone.0043835

 

Thomas G.M., Poinar Jr G.O. 1979. Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic bacteria of the family Ente­robacteriaceae. International Journal of Systematic and Evolutionary Microbiology 29 (4): 352–360. DOI: 10.1099/00207713- 29-4-352

 

Tomalak M. 2000. Wykorzystanie nicieni owadobójczych w ochronie roślin. Ochrona Roślin 9: 2–3.

 

van Lenteren J.C. 2003. Commercial availability of biological control agents. s. 167–179. W: Quality Control and Production of Biological Control Agents. Theory and Testing Procedures. CABI Publishing, Wallingford, UK. ISBN 9780851996882. DOI: 10.1079/9780851996882.0167

 

Vashisth S., Chandel Y.S., Sharma P.K. 2013. Entomopathogenic nematodes – a review. Agricultural Reviews 34 (3): 163. DOI: 10.5958/j.0976-0741.34.3.001

 

Webster J.M., Chen G.H., Hu K., Li J.X. 2002. Bacterial metabolites. s. 99–114. W: Entomopathogenic Nematology (R. Gaugler, red.). CABI Publishing, Wallingford, UK. ISBN 9780851995670. DOI: 10.1079/9780851995670.0099

Progress in Plant Protection (2023) 63: 129-136
First published on-line: 2023-07-25 14:50:56
http://dx.doi.org/10.14199/ppp-2023-014
Full text (.PDF) BibTeX Mendeley Back to list