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Review of Pasteuria Penetrans: Biology, Ecology, and Biological Control Potential 1

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Review of Pasteuria Penetrans: Biology, Ecology, and Biological Control Potential 1 Journal of Nematology 30(3):313-340. 1998. © The Society of Nematologists 1998. Review of Pasteuria penetrans: Biology, Ecology, and Biological Control Potential 1 Z. X. CHEN AND D. W. DICKSON 2 Abstract: Pasteuria penetrans is a mycelial, endospore-forming, bacterial parasite that has shown great potential as a biological control agent of root-knot nematodes. Considerable progress has been made during the last 10 years in understanding its biology and importance as an agent capable of effectively suppressing root-knot nematodes in field soil. The objective of this review is to summarize the current knowledge of the biology, ecology, and biological control potential of P. penetrans and other Pasteuria members. Pasteuria spp. are distributed worldwide and have been reported from 323 nematode species belonging to 116 genera of free-living, predatory, plant-parasitic, and entomopathogenic nematodes. Artificial cultivation of P. penetrans has met with limited success; large-scale production of endospores depends on in vivo cultivation. Temperature affects endospore attachment, germination, pathogenesis, and completion of the life cycle in the nematode pseudocoelom. The biological control potential of Pasteuria sl0p. have been demonstrated on 20 crops; host nematodes include Belonolaimus longicaudatus, Heterodera spp., Meloidogyne spp., and Xiphinema diversicaudatum. Pasteuria penetrans plays an important role in some suppressive soils. The efficacy of the bacterium as a biological control agent has been examined. Approximately 100,000 endospores/g of soil provided immediate control of the peanut root-knot nematode, whereas 1,000 and 5,000 endospores/g of soil each amplified in the host nematode and became suppressive after 3 years. Key words: bacterium, Belonolaimus longicaudatus, biological control, biology, cyst nematode, dagger nematode, ecology, endospore, Heterodera spp., Meloidogyne spp., nematode, Pasteuria penetrans, review, root-knot nematode, sting nematode, Xiphinema diversicaudatum. HISTORICAL BACKGROUND covery in Moina rectirostris Leydig, a member of Daphnidae. The genus Pasteuria Metchnikoff, 1888 Cobb (1906) was the first to report an or- was first described as a bacterial parasite of ganism resembling Pasteuria sp. infecting a water fleas, Daphnia magna Straus. Metchni- nematode, Dorylaimus bulbiferus. He mistak- koff (1888) named the bacterium Pasteuria enly suggested that the spores inside D. bul- ramosa and stated, "Pasteuria sp. was able to biferus were "perhaps monads" of a parasitic undergo as many as five longitudinal divi- sporozoan. The idea that these organisms sions at the same time, giving it a character- were sporozoan parasites remained in the istic fan shape" (Sayre, 1993). Metchnikoff literature for nearly 70 years. Micoletzky (1888) also tried to culture the bacterium (1925) suggested their placement in Dubo- but was unsuccessful. scqia Perez, 1908. In 1940, a parasite from Metchnikoff's paper, with its concept of Pratylenchus pratensis (de Man) Filipjev was longitudinal division of a microorganism named Duboscqia penetrans on the assump- and the accompanying drawings that tion that it was similar to the nematode para- showed "stalked" spores, intrigued other in- site described by Micoletzky (Thorne, 1940). vestigators. The bacterium, however, was not It was not until the mid-1970s, when the found again; consequently, Metchnikoff's nematode parasite was examined with elec- work was considered erroneous until the tron microscopy, that its relatedness to bac- 1970s (Hirsh, 1972; Migula, 1900), when teria rather than protozoa was recognized, Sayre et al. (1977, 1979) reported its redis- and it was named Bacillus penetrans (Mankau 1975a, 1975b). However, B. penetrans was not included in the approved lists of bacterial Received for publication 5 August 1997. 1 Florida Agricultural Experiment Station Journal Series No. names (Skerman et al., 1980). R-05899. Supported in part by a grant from the Southern Re- Sayre and Start (1985) drew attention to gion IPM Grant No. 93-34103-8396. 2 Post-Doctoral Research Associate and Professor, Entomol- the fact that B. penetrans resembled the acti- ogy and Nematology Department, Institute of Food and Agri- nomycete Pasteuria ramosa (Metchnikoff, cultural Sciences, University of Florida, Gainesville, FL 32611- 0620. 1888; Sayre et al., 1979) and renamed the E-mail: [email protected] organism Pasteuria penetrans. Recently, Ebert 313 314 Journal of Nematology, Volume 30, No. 3, September 1998 et al. (1996) rediscovered P. ramosa infecting genus (Ebert et al., 1996). The other three Daphnia magvm, the organism with which species of Pasteuria are parasites of plant- Metchnikoff originally worked, and the evi- parasitic nematodes: P. penetrans on Meloido- dence presented suggested that the parasite gyne spp., P. tho~vzei on Pratylenchus spp., and infecting Moina rectirostris (Sayre et al., 1977, P. nishizawae on cyst nematodes of the gen- 1979) was not the type species of Pasteuria era Heterodera and Globodera (Sayre and and belonged to another species. The genus Starr, 1989). Two undescribed species of Pasteuria as described by Metchnikoff has Pasteuria have been reported, one from Het- been conserved (Judicial Commission of the Erodera goettingiana Liebscher in Germany International Committee on Systematic Bac- (Sturhan et al., 1994) and the other from teriology, 1986; Starr et al., 1983). Current Belonolaimus longicaudatus Rau in Florida research emphasis is mostly on species of (Giblin-Davis et al., 1990, 1995). Pasteuria that parasitize plant-parasitic The taxon Pasteuria penetrans is often mis- nematodes. takenly used to represent other Pasteuria members (Ciancio, 1995b; Ciancio et al., MEMBERS OF PASTEURIA 1992; Fattah et al., 1989; Singh and Dhawan, 1994; Vovlas et al., 1993). Pasteuria penetrans Pasteuria species are gram-positive, di- originally was suggested to mean 'members chotomously branched, endospore-forming of P. penetrans group' (Sayre and Starr, bacteria with septate mycelium (Mankau 1985), but the species was later delineated to and Imbriani, 1975). Endospores are a non- P. penetrans sensu stricto, which infects M. in- motile form of the organism that lie in the cognita, and P. thornei, which infects Prat- soil matrix. When a suitable nematode host ylenchus spp. (Starr and Sayre, 1988). Pasteu- enters its domain, the endospore attaches to ria penetrans now is a valid taxon (Sayre and the nematode's cuticle. One to several hun- Starr, 1989), which according to the nomen- dred endospores may attach per nematode; clatural code (Lapage et al., 1975) must re- however, a single endospore is sufficient to fer only to the parasite of M. incognita. We infect the nematode host. The infection pro- suggest that other indefinitive isolate (s) be cess involves the formation of a germ tube addressed as Pasteuria sp. (spp.), or Pasteuria that penetrates the nematode body wall. Pri- member(s). mary colonies are formed from the germi- There is still considerable confusion nating tube after it penetrates inside the about the taxonomy of Pasteuria spp. be- nematode pseudocoelom. These colonies cause of the criteria currently used for dif- are shaped like cauliflower florets or clusters ferentiating species within the genus. These of elongated grapes. Daughter colonies are criteria (ultrastructure, morphology, life formed by fragmentation of the mother cycle, and host preference), once seemingly colonies, and the daughter colonies in turn explicit, are challenged by the numerous produce clusters of sporangia. The terminal new isolates of Pasteuria spp. collected from hyphae of the mycelium elongate to form plant and soil nematodes. Some isolates of sporangia, and these give rise to endospores. Pasteuria spp. display cross-generic parasit- Endospores are resistant to desiccation. ism of nematodes. Also, isolates from differ- Pasteuria spp. have not been grown suc- ent nematode genera often appear superfi- cessfully in pure culture. Species of the ge- cially similar under light microscopy in re- nus must be cultured on a nematode or wa- gard to development within the nematode's ter-flea host. Four species of Pasteuria have pseudocoelom and endospore morphology. been described; they are differentiated by Furthermore, recent evidence indicates that their host preference, developmental char- morphology of sporangia and endospores of acterisfics, and size and shape of sporangia 69 Pasteuria members were correlated with and endospores (Sayre and Starr, 1989). Pas- some host characters (Ciancio, 1995a). Di- teuria ramosa, which parasitizes water fleas of ameter of sporangia varied from 1.5 pm for the genus Daphnia, is the type species of the an isolate from Criconemella sp. in Florida Review of P. penetrans: Chen, Dickson 315 (Z. X. Chen, pers. obs.) to 8 pm for an iso- Tylenchulus semipenetrans, appeared to be late from Axonchium valvulatum in Sri Lanka host-specific (Kaplan, 1994). Endospores of (Ciancio et al., 1994). Distinct groupings of the isolate did not attach to the body of M. Pasteuria spp. by sizing sporangia and endo- incognita, M. javanica, Radopholus citrophilus, spores were not obtainable. It is apparent or R. similis, whereas several T. semipenetrans that the taxonomy of Pasteuria spp. will re- J2 and males were observed with endospores main unclear until more efforts are allo- developing inside their bodies after 20 days' cated to the problem. incubation. Some isolates of Pasteuria spp. display Pasteuria spp. are reported to selectively cross-generic
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