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Bionomics of a Phoretic Association Between Paenibacillus Sp Journal of Nematology 37(1):18–25. 2005. © The Society of Nematologists 2005. Bionomics of a Phoretic Association Between Paenibacillus sp. and the Entomopathogenic Nematode Steinernema diaprepesi1 F. E. El-Borai,2 L. W. Duncan,2 and J. F. Preston3 Abstract: Spores of an unidentified bacterium were discovered adhering to cuticles of third-stage infective juvenile (IJ) Steinernema diaprepesi endemic in a central Florida citrus orchard. The spores were cup-shaped, 5 to 6 mm in length, and contained a central endospore. Based on 16S rDNA gene sequencing, the bacterium is closely related to the insect pathogens Paenibacillus popilliae and P. lentimorbus. However, unlike the latter bacteria, the Paenibacillus sp. is non-fastidious and grew readily on several standard media. The bacterium did not attach to cuticles of several entomopathogenic or plant-parasitic nematodes tested, suggesting host specificity to S. diaprepesi. Attachment of Paenibacillus sp. to the third-stage cuticle of S. diaprepesi differed from Paenibacillus spp. associated with heterorhabditid entomopathogenic nematodes, which attach to the IJ sheath (second-stage cuticle). The inability to detect endo- spores within the body of S. diaprepesi indicates that the bacterial association with the nematode is phoretic. The Paenibacillus sp. showed limited virulence to Diaprepes abbreviatus, requiring inoculation of larvae with 108 spores to achieve death of the insect and reproduction of the bacterium. The effect of the bacterium on the nematode population biology was studied in 25-cm-long vertical sand columns. A single D. abbreviatus larva was confined below 15-cm depth, and the soil surface was inoculated with either spore-free or spore-encumbered IJ nematodes. After 7 days, the proportion of IJ below 5-cm depth was seven-fold greater for spore-free IJ than for spore-encumbered nematodes. Mortality of D. abbreviatus larvae was 72% greater (P Յ 0.01) for spore-free compared to spore-encumbered S. diaprepesi. More than 5 times as many progeny IJs (P Յ 0.01) were produced by spore-free compared to spore-encumbered nematodes. These data suggest that the bacterium is a component of the D. abbreviatus food web with some potential to regulate a natural enemy of the insect. Key words: Antagonism, competition, Diaprepes abbreviatus, entomopathogenic nematode, Paenibacillus, phoresis, 16S rDNA, Stein- ernema diaprepesi, Xenorhabdus sp. Entomopathogenic nematodes (EPN) are used (1993) reported that Steinernema scapterisci carried bac- widely in Florida citrus groves to help manage the citrus terial species in addition to Xenorhabdus spp. inside the root weevil Diaprepes abbreviatus (Bullock et al., 1999; nematode. All of those bacteria species were capable of Duncan et al., 2000, 2003a,b; McCoy et al., 2000, 2002). killing the insect host, although they were less virulent In nature, enterobacteria in the genera Photorhabdus than Xenorhabdus sp. and Xenorhabdus are obligate symbionts of Heterorhabdi- Several Paenibacillus species have been reported asso- tis spp. and Steinernema spp., respectively (Akhurst and ciated with insects. Some are obligate insect pathogens Boemare, 1990; Boemare et al., 1993; Forst and Neal- such as P. popilliae, P. lentimorbus, and P. larvae (Petters- son, 1996). These bacteria carried within the digestive son et al., 1999), whereas others are facultative patho- tract of the EPN are released following infection of a gens such as P. apiarus (Nakamura, 1996) and P. alvei host and are responsible for the death of the insect. (Krieg, 1981). Paenibacillus popilliae and P. lentimorbus Nematodes are able to complete several generations (Walsh and Webster, 2003) are the causal agent of types within the insect cadaver by feeding on the bacterial A and B milky disease in Japanese beetle and other symbiont and on insect tissues conditioned by bacterial scarab larvae and have been used as biocontrol agents enzymes (Hu and Webster, 2000; Thaler et al., 1997). against these insects (Cappaert and Smitley, 2002; Klein Antibiotics produced by the bacterial symbiont greatly and Kaya, 1995; Koppenho¨fer et al., 2000). There are reduce colonization of the insect cadaver by other mi- some reports of associations between EPN and Paeniba- croorganisms (Akhurst, 1982; Hu and Webster, 2000; cillus spp. These bacteria attach to the nematode cuticle Richardson et al., 1988). and reproduce within insects infected by the nematode. Lysenko and Weiser (1974) reported a number of Enright et al. (2001, 2003) described a phoretic asso- bacterial species other than Xenorhabdus spp. associated ciation between Heterorhabditis spp. and P. nematophilus. with the genus Steinernema, but none were highly patho- Spores of the bacterium attached to the sheath (sec- genic to Galleria mellonella larvae. Aguillera and Smart ond-stage cuticle) of the third-stage juveniles of all tested Heterorhabditis species and some close relatives in the order Strongylida but not to several species of Stein- Received for publication 12 July 2004. 1 This research was supported by the Florida Agricultural Experiment Sta- ernema or other soil-inhabiting nematodes. Marti and tion, including CRIS projects LAL-03924 and MCS-03703, and by CRIS project Timper (1999) reported an association between several MCS-03798 from USDA-CSREES NE-171 Regional Project, and a grant from the Florida Citrus Production Research Advisory Council, and approved for publi- Heterorhabditis sp. isolates and a putative Bacillus species cation as Journal Series No. R-10331. that was morphologically similar to the Paenibacillus 2 Postdoctoral Research Scientist, Professor, University of Florida, IFAS, Cit- rus Research and Education Center, 700 Experiment Station Rd., Lake Alfred spp. reported by Enwright et al. (2003). FL 33850. During surveys of the prevalence of endemic ento- 3 Professor, Microbiology and Cell Science Dept., IFAS, University of Florida, P. O. Box 110700, Gainesville, FL 32611. mopathogenic nematodes in Florida orchards (Duncan The authors thank Guang Nong of the Department of Microbiology and Cell and El-Borai, unpubl. Duncan et al., 2003b), spores Science for assistance with DNA alignment and phylogenetic analysis. E-mail: [email protected]fl.edu morphologically similar to those reported by Enright et This manuscript was edited by S. Patricia Stock. al. (2003) and Marti and Timper (1999) were fre- 18 Paenibacillus and Entomopathogenic Nematodes: El-Borai et al. 19 quently found attached to H. indica and H. zealandica evaluate the nematode vector specificity of the bacte- emerging from cadavers of D. abbreviatus (Fig. 1A). rium. Spores of unidentified and morphologically dissimilar bacteria were also found adhering in large numbers to Materials and Methods the cuticle of third-stage infective juvenile (IJ) S. dia- prepesi (Fig. 1B). In this paper, we report results of stud- Bacterium isolation: A bacterium was isolated from in- ies to (i) characterize the bacterium associated with S. fective third-stage S. diaprepesi that emerged from D. diaprepesi based on fatty acid methyl ester (FAME) pro- abbreviatus sentinel larvae recovered from the type lo- files and 16S rDNA gene sequencing; (ii) evaluate viru- cality of S. diaprepesi (Nguyen and Duncan, 2002). lence of the bacterium to D. abbreviatus larvae; (iii) de- Spore-encumbered IJ were harvested, rinsed several termine the effect of the bacterium on the motility, times with sterile-distilled water, and placed in sterile infectivity, and reproduction of S. diaprepesi; and (iv) Eppendorf tubes in a water bath (80 °C) for 15 minutes. The tubes were cooled and shaken, and 200-µl suspen- sions were streaked onto 1.5% nutrient agar (NA) (Sigma Chemical Company, St. Louis, MO) and incu- bated at room temperature (∼ 25 °C). After 96 hours, single cell colonies were isolated on NA, grown for 72 hours, and sampled for microscopic observation (1000×). Colonies with combinations of rod-shaped bacteria and cup-shaped spores were re-isolated. The ability of spores to attach to S. diaprepesi was confirmed by surface-disinfesting spore-free nematodes with 0.2% streptomycin sulfate for 24 hours, rinsing repeatedly, and placing nematodes onto bacterial cultures. After 48 hours, the nematodes were rinsed repeatedly and ex- amined microscopically. Colonies producing spores that attached to nematodes were maintained in vivo by exposing larvae of the weevil D. abbreviatus to spore- encumbered, infective third-stage S. diaprepesi, and in vitro on nutrient agar and Luria-Bertani (LB) agar (Fisher Scientific, Pittsburgh, PA). Nematode preparation: Spore-encumbered S. diaprepesi used in all experiments were prepared by exposing sur- face-disinfested IJ, freshly harvested from D. abbreviatus, to 7-day-old colonies of the bacterium on NA or Luria- Bertani medium agar (LBA). Spore-free IJ were recov- ered from petri dishes of NA after equivalent exposure times. Bacterium characterization: The bacteria were culti- vated on either 1.5% agar (LBA) or broth (LB) at 30 °C (Davis et al., 1980). Stocks were maintained on LBA and transferred to 2-ml standing broth cultures to de- termine substrate requirements. For genus and species determination, LBA plates containing isolated colonies were sent to MIDI Labs (Newark, DE) for typing by FAME and 16S rDNA sequence analysis. The FAME analysis was also conducted on colonies obtained from Fig. 1. A) Scanning electron micrographs of spindle-shaped spores attached to Heterorhabditis zealandica emerging from cadavers tryptone soy agar in the diagnostic laboratory of the of
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