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Pasteuria Spp.: Systematics and Phylogeny of These Bacterial Parasites of Phytopathogenic Nematodes1

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Pasteuria Spp.: Systematics and Phylogeny of These Bacterial Parasites of Phytopathogenic Nematodes1 Journal of Nematology 35(2):198–207. 2003. © The Society of Nematologists 2003. Pasteuria spp.: Systematics and Phylogeny of These Bacterial Parasites of Phytopathogenic Nematodes1 J. F. Preston,2 D. W. Dickson,3 J. E. Maruniak,3 G. Nong,2 J. A. Brito,4 L. M. Schmidt,2 and R. M. Giblin-Davis5 Abstract: Pasteuria spp. include endospore-forming bacterial pathogens of cladoceran crustaceans and plant-parasitic nematodes. Propagation of these nematode pathogens requires attachment of soilborne endospores to nematode hosts, infection, growth, sporulation, and release of endospores to repeat the cycle of infection and propagation. The ability of these bacteria to suppress the levels of plant-parasitic nematodes in the field has made them particularly promising candidates for biocontrol of nematode diseases of plants. Genes encoding 16S ribosomal RNA have been sequenced forthe cladoceran(waterflea) parasiteand type species, Pasteuria ramosa, and for Pasteuria spp. isolated from root-knot (Meloidogyne arenaria race 1 and Meloidogyne sp.), soybean cyst (Heterodera glycines), and sting (Belonolaimus longicaudatus) nematodes. These have provideda phylogenetic basis fortheirdesigna- tion to a distinct clade within the family Alicyclobacillaceae of the gram-positive endospore-forming bacteria. Two apparent biotypes of P. penetrans demonstrating a host preference for different Meloidogyne spp. showed identical 16S rDNA sequences, suggesting host-recognition evolves within a given species. The sequences of genes encoding sporulation transcription factors, sigE and sigF, from P. penetrans biotype P-20 show different phylogenetic relationships to other endospore-forming bacteria, supporting their application to further discriminate Pasteuria spp. and biotypes. Distribution of an adhesin-associated epitope on polypeptides from different Pasteuria isolates provides an immunochemical approach to differentiate species and biotypes with specific host prefer- ences. Application of bioinformatics to genomic data, as well as further characterization of the biochemical basis for host recog- nition, will facilitate development of Pasteuria spp. as benign alternatives to chemical nematicides. Key words: biological control, cladocerans, endospore, Meloidogyne arenaria, nematode, Pasteuria penetrans, Pasteuria ramosa, phy- logeny. As obligate parasites of plant-parasitic nematodes, juvenile (J2) may be sufficient to allow infection and species of the endospore-forming genus Pasteuria have propagation of the bacteria. The infection process has arguably become the most promising agents for biocon- not been differentiated from germination of the spore, trol of many nematodes that cause extensive damage to and germination may in fact trigger infection. After field crops, vegetables, turf grasses, and ornamentals. A germination the cells proliferate through a series of relationship has been established between levels of soil- developmentally distinct vegetative stages prior to the borne endospores of Pasteuria spp. and suppression of onset of endospore formation. Discrete stages of spore nematode infection of plant roots (Chen and Dickson, formation comparable to those found in other endo- 1998). The basis fortheirbiocontrolpotential is due in spore-forming bacteria occur (Chen et al., 1997a; Sayre part to the fact that the propagation of the bacteria and Starr, 1988). As many as2×106 mature endospores within the pseudocoel of the infected nematode host are released as the female nematode ruptures. If each results in a loss of fecundity. The nematode host serves gall contains a Pasteuria-infected nematode, a single to amplify the infective endospores that are released plant may release 107 to 108 endospores into the soil. into the soil to repeat a cycle of infection and amplifi- As the density of soilborne endospores of a particular cation. This process has been studied most extensively species and biotype of Pasteuria increases, those soils in the infection of root-knot nematodes by P. penetrans may become more suppressive to a population of nema- as depicted in Figure 1. todes susceptible to infection by that particular species The binding of a single endospore to a second-stage and biotype of Pasteuria. In addition to the loss of fe- cundity, the attachment of a significant numberof en- dospores to the cuticle of a J2 may encumber the nema- Received forpublication 24 June 2002. tode to an extent that it is unable to reach and infect 1 Symposium paperpresentedat the 40th Annual Meeting of The Society of Nematologists, 25–29 August 2001, Salt Lake City, UT. Florida Agricultural the root tip of a prospective host plant. While the num- Experiment Station Journal Series no. R-09140. Supported in part by CRIS berof bound endosporesthat effectively encumbera projects MCS 03703 and ENY 03703 from the University of Florida Agricultural Experiment Station, and by CRIS projects MCS-03798 and ENY-03798 from NE soilborne juvenile is known only approximately, a num- 171 Regional Project USDA-CSREES. ber greater than 40 likely will prevent root infection 2 Professor, Post-doctoral Associate, and graduate student, respectively, Mi- crobiology and Cell Science Department, University of Florida, Gainesville, FL (Stirling, 1984). As shown in Figure 2, more than 100 32611. endospores may bind to the cuticle of the nematode, 3 Professor and Associate Professor, respectively, Entomology and Nematol- ogy Department, University of Florida, Gainesville, FL 32611. predicting that a significant range in the density of soil- 4 Biological Scientist, Division of Agricultural and Consumer Services, borne endospores that will effectively suppress the in- Florida Department of Agriculture, Gainesville, FL 32614. 5 Professor, Entomology and Nematology Department, University of Florida, fection of target plants by their respective parasitic Fort Lauderdale Research and Education Center, Davie, FL 33314. nematodes. The authors gratefully acknowledge Jon H. Charnecki and John D. Rice for the isolation and characterization of the monoclonal antibody, Greg R. Noel The relationship between the levels of soilborne Pas- forproviding Pasteuria sp. Hg, and K. T. Shanmugam foradvice and assistance teuria endospores and suppression of infection of plants with the cloning and sequencing of sigE and sigF genes. E-mail: jpreston@ufl.edu by Meloidogyne spp. has been particularly well docu- This paperwas edited by B. C. Hyman. mented (Chen et al., 1997b; Weibelzahl-Fulton et al., 198 Systematics and Phylogeny of Pasteuria spp.: Preston et al. 199 Fig. 1. The life cycle of a root-knot nematode, Meloidogyne sp., with (innerportionof outercircle)and without (outerportionof out er circle) infection by Pasteuria penetrans. The innercircledepicts the stages of P. penetrans following infection to release of endospores: (1) Entry of soilborne second-stage juveniles into root tip of plant host; (2) intracellular migration of J2 in cortex; (3) establishment of feeding site in vascularsystem (attached P. penetrans endospores germinate and infect); (4) molt to third-stage juvenile; (5) molt to fourth-stage juvenile; (6) development of young females; (7) egg formation in healthy female; little orno egg formationin female infected with Pasteuria; (8,9) healthy female releases egg masses; infected female releases mature endospores. The inner circle describes the life cycle of the P. penetrans: (a) mature endospores in the soil; (b) endospore attached to the cuticle of Meloidogyne sp.; (c) germination and formation of infection tube; (d) appearance of a microcolony of dichotomously branched septate mycelium; (e) release of colonies through lysis of intercalary cells, with rapid cell proliferation; (f) further differentiation with increase in numbers of colonies, containing larger cells; (g) formation of quartets and then diads that represent sporangia for onset of sporulation; (h) formation of forespore within mother cell; (i) engulfment and maturation with formation of parasporal fibers; (j) completion of maturation to form disk-shaped spores with polar orientation of parasporal fibers; (k) release of mature endospores into the environment (Weibelzahl-Fulton, 1998). 1996). In the case of P. penetrans P20, 10,000 endo- ships with their respective hosts. Comprehensive re- spores/g of soil have been demonstrated to effectively views have been published on the genus Pasteuria and suppress the infection of peanut plants by Meloidogyne the species and isolates that have been implicated in arenaria race 1 (Chen et al., 1996). There is evidence the control of plant-parasitic nematodes (Chen and that most, if not all, plant-parasitic nematodes propa- Dickson, 1998; Sayre, 1993; Sayre and Starr, 1988). The gate a species of Pasteuria that restricts the fecundity of discussion presented here will extend these reviews to the nematode host. It is thus not surprising that these consider the phylogenic relationships of these bacteria bacteria have received ever-increasing attention, with as now discerned through DNA sequencing and immu- several research groups addressing the etiology and bio- nochemical properties of spore adhesins. chemistry of the basis for developing parasitic relation- Definition of genus Pasteuria: The type species of the 200 Journal of Nematology, Volume 35, No. 2, June 2003 endospore-forming bacterium was not generally ac- cepted until nearly a century later, when the similarities to parasitic bacterial pathogens of plant-parasitic nema- todes were considered (Sayre et al., 1983). From the early 20th century, observations
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