Abstract
The genus Pasteuria comprises a truly extraordinary group of unculturable bacteria that are obligate parasites of either water fleas or plant parasitic nematodes. They have an astonishing vegetative morphology that, through an intricate process of differentiation, leads to a structurally unique endospore form. Remarkably, phylogenetic studies indicate that this genus is ancestral to the genus Bacillus. P. penetrans is the most studied species and is a highly specific internal parasite of phytoparasitic nematodes, several hundred species of which are infected. This chapter reviews this parasitic interaction and the concomitant development and multiplication of P. penetrans. The problems encountered and solutions found in carrying out molecular and ecological studies of this organism are also explored. The major goal in studying this bacterium is to exploit its ability to decrease nematode damage to crops and ecosystems. Evidence is presented of experiments demonstrating its ability to cause economically and ecologically valuable suppression of plant parasitic nematodes.
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References
Aktar M, Malik A (2000) Roles of organic amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour Technol 74:35–47
Andersen GL, Simchock JM, Wilson KH (1996) Identification of a region of genetic variability among Bacillus anthracis strains and related species. J Bacteriol 177:377–384
Anderson JM, Preston JF, Dickson DW, Hewlett TE, Williams NH, Maruniak JE (1999) Phylogenetic analysis of Pasteuria penetrans by 16S rRNA gene cloning and sequencing. J Nematol 31:319–325
Atibalentja N, Noel GR (1997) Life cycle and host specificity of Pasteuria sp. parasitizing Heterodera glycines. J Nematol 29:568 (Abstr)
Atibalentja N, Noel GR, Liao TF, Dormier LL (2000) Phylogenetic position of the American isolate of Pasteuria that parasitizes the soybean cyst nematode, Heterodera glycines, as inferred from 16S rRNA sequence analysis. Int J Syst Evol Microbiol 50:605–613
Atibalentja N, Noel GR, Ciancio A (2004) A simple method for the extraction, PCR-amplification, cloning, and sequencing of Pasteuria 16S rDNA from small numbers of endospores. J Nematol 36:100–105
Bekal S, Giblin-Davis RM, Becker JO (1999) Gnotobiotic culture of Pasteuria sp. on Belonolaimus longicaudatus. J Nematol 31:522
Bekal S, Borneman J, Springer MS, Giblin-Davis RM, Becker JO (2001) Phenotypic and molecular analysis of a Pasteuria strain parasitic to the sting nematode. J Nematol 33:110–115
Bhattacharya D, Swarup G (1988) Pasteuria penetrans, a pathogen of the genus Heterodera, its effect on nematode biology and control. Indian J Nematol 18:61–70
Bird AF, Brisbane PG (1988) The influence of Pasteuria penetrans in field soils on the reproduction of root-knot nematodes. Rev Nématol 11:75–81
Bird D, Opperaman CH, Davies KG (2003) Interactions between bacteria and plant parasitic nematodes: now and then. Int J Parasitol 33:1269–1276
Bishop AH (2002) The insecticidal proteins of Bacillus thuringiensis. In: Berkeley R, Heyndrickx M, Logan NA, De Vos P (eds) Applications and systematics of the genus Bacillus and related organisms. Blackwell, Oxford, pp 160–175
Bishop AH, Ellar DJ (1991) Attempts to culture Pasteuria penetrans. Biocontrol Sci Technol 1:101–114
Bishop AH, Gowen SR, Pembroke B, Trotter JR (2007) Morphological and molecular characteristics of a new species of Pasteuria parasitic on Meloidogyne ardenensis. J Invertebr Pathol 96:28–33
Brown SM, Smart GC (1985) Root penetration by Meloidogyne incognita juveniles infected with Bacillus penetrans. J Nematol 17:123–125
Charles L, Carbone I, Davies KG, Bird D, Burke M, Kerry BR, Opperman CH (2005) Phylogenetic analysis of Pasteuria penetrans by use of multiple genetic loci. J Bacteriol 187:5700–5708
Charnecki JH, Rice JD, Dickson DW, Preston JF (1998) Determinants for attachment of endospores of Pasteuria penetrans to phytopathogenic nematodes. In: 98th Annual Meeting of American Society of Microbiology. Abstr Q-171, p 449
Chen ZX, Dickson DW (1998) Review of Pasteuria penetrans: biology, ecology and biological control potential. J Nematol 30:313–340
Chen ZX, Dickson DW, Hewlett TE (1996a) Quantification of the endospore concentrations of Pasteuria penetrans in tomato root material. J Nematol 28:50–55
Chen ZX, Dickson DW, Freitas, LG Preston JF (1996b) Suppression of Meloidogyne arenaria race 1 by soil application of endospores of Pasteuria penetrans. J Nematol 28:159–168
Chen ZX, Dickson DW, McSorley R, Mitchell DJ, Hewlett TE (1997) Suppression of Meloidogyne arenaria race 1 by soil application of endospores of Pasteuria penetrans. J Nematol 28:159–168
Ciancio A, Bonsignore R, Vovlas N, Lamberi F (1994) Host records and spore morphometrics of Pasteuria penetrans group parasites of nematodes. J Invertebr Pathol 63:260–267
Cobb NA (1906) Fungus maladies of the sugar cane, with notes on associated insects and nematodes, 2nd edn. Hawai Sugar Planters Assoc Exp Stat Div Pathol Physiol Bull 19:342–348
Davies KG, Kerry BR, Flynn CA (1988) Observations on the pathogenicity of Pasteuria penetrans, a parasite of root-knot nematodes. Ann Appl Biol 112:491–501
Davies KG, Flynn CA, Laird V, Kerry BR (1990) The life-cycle, population dynamics, and host specificity of a parasite of Heterodera avenae, similar to Pasteuria penetrans. Rev Nématol 13:303–309
Davies KG, Afolabi P, O’Shea P (1996) Adhesion of Pasteuria penetrans to the cuticle of root-knot nematodes (Meloidogyne spp.) inhibited by fibronectin: a study of electrostatic and hydrophobic interactions. Parasitology 112:553–559
Dean FB, Nelson JR, Gielse TL, Lasken RS (2001) Rapid amplification of plasmid and phage DNA using Phi29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11:1095–1099
Duan YP, Castro HF, Hewlett TE, White JH, Ogram AV (2003) Detection and characterization of Pasteuria 16S rRNA gene sequences from nematodes and soils. Int J Syst Evol Microbiol 53:105–112
Dutky EM, Sayre RM (1978) Some factors affecting infection of nematodes by the bacterial spore parasite Bacillus penetrans. J Nematol 10:285 (Abstr)
Ebert D, Rainey P, Embley TM, Scholz D (1996) Development, life cycle, ultrastructure, and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Strauss. Philos Trans R Soc Lond Ser B 351:1689–1701
Ellis RJ, Morgan P, Weightman PAJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microbiol 69:3223–3230
Esnard J, McClure MA, Dickson DW, Hewlett TE, Zuckerman BM (1997) Effects of monoclonal antibodies, cationized ferritin, and other organic molecules on adhesion of Pasteuria penetrans endospores to Meloidogyne incognita. J Nematol 29:556–564
Fould S, Dieng AL, Davies KG, Normand P, Matielle T (2001) Immunological quantification of the nematode parasitic bacterium Pasteuria penetrans in soil. FEMS Microbiol Ecol 37:187–195
Giannakou IO, Pembroke B, Gowen SR Davies KG (1997) Effects of long-term storage and above-normal temperatures on spore adhesion of Pasteuria penetrans and infection of the root-knot nematode Meloidogyne javanica. Nematologica 43:185–192
Giblin-Davis RM, McDaniel LL, Bilz FG (1990) Isolates of the Pasteuria penetrans group from phytoparasitic nematodes in bermudagrass turf. J Nematol 22:750–762
Giblin-Davis RM, Williams DS, Bekal S, Dickson DW, Brito JA, Becker JO, Preston JF (2003) ‘Candidatus Pasteuria usgae’ sp.nov., an obligate endoparasite of the phytoparasitic nematode, Belonolaimus longicaudatus. Int J Syst Evol Microbiol 53:197–200
Hatz B, Dickson DW (1992) Effect of temperature on attachment, development, and interactions of Pasteuria penetrans on Meloidogyne arenaria. J Nematol 24:512–521
Hewlett TE, Dickson DW (1994) Endospore attachment specificity of Pasteuria penetrans from a peanut field in Florida. J Nematol 26:103–104 (Abstr)
Kaplan DT (1994) Partial characterisation of a Pasteuria sp. attacking the citrus nematode, Tylenchulus semipenetrans, in Florida. Fundam Appl Nematol 17:509–512
Kariuki GM, Dickson DW (2007) Transfer and development of Pasteuria penetrans. J Nematol 39:55–61
Kariuki GM, Brito JA, Dickson DW (2006) Effects of Pasteuria penetrans endospores rate of attachment on root penetration and fecundity of Meloidogyne arenaria race 1. Nematropica 36:261–267
Kerry BR (1988) Fungal parasites of cyst nematodes. Agric Ecol Environ 24:293–305
Mankau R (1975) Bacillus penetrans n. comb. causing a virulent disease of plant parasitic nemtodes. J Invertebr Pathol 26:333–339
Mankau R, Prasad N (1972) Possibilities and problems in the use of a sporozoan endoparasite for biological control of plant-parasitic nematodes. Nematropica 2:7–8
Melki KC, Giannokou IO, Pembroke B, Gowen SR (1998) The cumulative build up of Pasteuria penetrans spores in root-knot nematodes infested soil and the effect of soil applied fungicide on its infectivity. Fundam Appl Nematol 21:679–683
Metchnikoff ME (1888) Pasteuria ramose un representant des bacteries a division longitudinale. Annales de L’Institut Pasteur (Paris) 2:165–170
Mohan S, Fould S, Davies KG (2001) The interaction between the gelatin-binding domain of fibronectin and the attachment of Pasteuria penetrans endospores to nematode cuticle. Parasitology 123:271–276
Mouton L, Ebert D (2008) Variable number of tandem repeats analysis of genetic diversity in Pasteuria ramosa. Curr Microbiol 56:447–452
Mouton L, Nong G, Preston JF, Ebert D (2007) Variable-number tandem repeats as molecular markers for biotypes for Pasteuria ramosa in Daphnia spp. Appl Environ Microbiol 73:3715–3718
Nannipieri C, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Noel GR, Stanger BA (1994) First report of Pasteuria sp.attacking Heterodera glycines in North America. Suppl J Nematol 26:612–615
Nong G, Chow V, Schmidt LM, Dickson DW, Preston JF (2007) Multiple strand displacement and identification of single nucleotide polymorphisms as markers of genetic variation of Pasteuria penetrans biotypes infecting biotypes infecting root-knot nematodes. FEMS Microbiol Ecol 61:327–336
Oka Y, Koltai H, Bar-Eyal M, Mor M, Sharon E, Chet I, Spiegel Y (2000) New strategies for the control of plant-parasitic nematodes. Pest Manag Sci 56:983–988
Oostendorp M, Dickson DW, Mitchell DJ (1990) Host range and ecology of isolates of Pasteuria spp. from the southeastern United States. J Nematol 22:525–531
Pan C, Lin J, Ni Z, Wang S (1993) Study on the pathogenic bacteria parsitizing root-knot nematodes discovered in China and their application to biological control. Acta Microbiol Sin 33:313–316
Persidis A, Lay JG, Manousis T, Bishop AH, Ellar DJ (1991) Characterization of potential adhesions of the bacterium Pasteuria penetrans, and of putative receptors on the cuticle of Meloidogyne incognita, a nematode host. J Cell Sci 100:613–622
Preston JF, Dickson DW, Maruniak JE, Nong G, Brito JA, Schmidt LM, Giblin-Davis RM (2003) Pasteuria spp.: systematics and phylogeny of these bacterial parasites of phytopathogenic nematodes. J Nematol 35:198–207
Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: genomic analysis of microbial communities. Ann Rev Genet 38:525–552
Sayre RM, Starr MP (1985) Pasteuria penetrans (ex Thorne 1940) nom. rev. comb. n., sp., n., a mycelial and endospores-forming bacterium parasitic in plant-parasitic nematodes. Proc Helminthol Soc Washington 52:149–165
Sayre RM, Wergin WP (1977) Bacterial parasite of a plant nematode: morphology and ultrastructure. J Bacteriol 129:1091–1101
Sayre RM, Starr MP, Golden MA, Wergin WP, Endo BY (1988) Comparison of Pasteuria penetrans from Meloidogyne incognita with a related mycelial and endospore-forming bacterial parasite from Pratylenchus brachyurus. Proc Helminthol Washington 55:28–49
Sayre RM, Wergin WP, Schmidt JM, Starr MP (1991) Pasteuria nishizawae sp. nov., a mycelial and endospore-forming bacterium parasitic on cyst nematodes of genera Heterodera and Globodera. Res Microbiol 142:551–564
Schmidt LM, Preston JF, Rice JD, Hewlett TE (2003) Environmental quantification of Pasteuria penetrans endospores using in situ antien extraction and immunodetection with monoclonal antibody. FEMS Microbiol Ecol 44:17–26
Schmidt LM, Preston JF, Nong G, Dickson DW, Aldrich HC (2004) Detection of Pasteuria penetrans infection in Meloidogyne arenaria race 1 in planta by polymerase chain reaction. FEMS Microbiol Ecol 48:457–464
Schmidt LM, Mouton L, Nong G, Ebert D, Preston JF (2008) Genetic and immunological comparison of the cladoceran parasite Pasteuria ramosa with the nematode parasite Pasteuria penetrans. Appl Environ Microbiol 74:259–264
Sharma SB, Davies KG (1996) Characterisation of Pasteuria isolated from Heterodera cajani using morphology, pathology and serology of endospores. Syst Appl Microbiol 19:106–112
Sharma R, Ranjan R, Kapardar RK, Grover A (2005) Unculturable bacterial diversity: an untapped resource. Curr Sci 89:72–77
Siddiqui ZA, Mahmood I (1999) Role of bacteria in the management of plant parasitic nematodes: a review. Bioresour Technol 69:167–179
Starr MP, Sayre RM (1988) Pasteuria thornei sp. nov. and Pasteuria penetrans sensu stricto emend., mycelial and endospore-forming bacteria parasitic, respectively, on plant-parasitic nematodes of the genera Pratylenchus and Meloidogyne. Ann Inst Pasteur Microbiol 139:11–31
Stirling GR (1984) Biological control of Meloidogyne javanica with Bacillus penetrans. Phytopathology 74:55–60
Stirling GR, Bird AF, Cakurs AB (1986) Attachment of Pasteuria penetrans spores to the cuticle of root knot nematodes. Rev Nematol 9:251–260
Sturhan D (1988) New host and geographical records of nematode-parasitic bacteria on the Pasteuria penetrans group. Nematologica 34:35–356
Sturhan D, Winkelheide R, Sayre RM, Wergin WP (1994) Light and electron microscopical studies of the life cycle and developmental stages of a Pasteuria isolate parasitizing the pea cyst nematode, Heterodera goettingiana. Fundam Appl Nematol 17:29–42
Sturhan D, Shutova TS, Akimov VN, Subbotin SA (2005) Occurrence, hosts, morphology, and molecular characterization of Pasteuria bacteria parasitic to nematodes in the family Plectidae. J Invertbr Pathol 88:17–26
Thorne G (1940) Duboscquia penetrans n. sp. (Sporozoa, Microsporidia Nosematidae), a parasite of the nematode Pratylenchus pratensis (de Man) Filipjev. Proc Helminthol Soc Washington 7:51–53
Tian B, Yang J, Zang K-Q (2007) Bacteria in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61:197–213
Trotter JR, Bishop AH (2003) Phylogenetic analysis and confirmation of the endospore-forming nature of Pasteuria penetrans based in the spo0A gene. FEMS Microbiol Lett 225:249–256
Trotter JR, Darban DA, Gowen SR, Bishop AH, Pembroke B (2004) The isolation of a single spore isolate of Pasteuria penetrans and its pathogenicity on Meloidogyne javanica. Nematology 6:463–472
Tzortzakakis EA, Gowen SR (1994) Evaluation of Pasteuria penetrans alone and in combination with oxamyl, plant resistance and solarization from control of Meloidogyne spp. on vegetables grown in greenhouses in Crete. Crop Prot 13:455–462
Vaid A, Bishop AH, Davies KG (2002) The polypeptide components of the parasporal fibres of Pasteuria penetrans. World J Microbiol Biotechnol 18:151–157
Waterman JT, Bird DM, Opperman CH (2006) A method for isolation of Pasteuria penetrans endospores for bioassay and genomic studies. J Nematol 38:165–167
Westphal A, Becker JO (1999) Transfer of biological soil suppressiveness against Heterodera schachtii. Phytopathology 90:401–406
Williams AR, Stirling GR, Hayward AC, Perry J (1989) Properties and attempted culture of Pasteuria penetrans, a bacterial parasite of root-knot nematode (Meloidogyne javanica). J Appl Bacteriol 67:145–156
Winkelheide R, Sturhan D (1996) Studies on host specificity of Pasteuria isolate from Heterodera goettingiana. Mitteilungen der Biologischen Bundesanstalt für Land-Forstwirtschaft 317:46–53
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Bishop, A.H. (2011). Pasteuria penetrans and Its Parasitic Interaction with Plant Parasitic Nematodes. In: Logan, N., Vos, P. (eds) Endospore-forming Soil Bacteria. Soil Biology, vol 27. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19577-8_9
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