Abstract
Soil contains a diverse range of fungi that are parasites on nematodes. These fungi include the nematode-trapping fungi that are dependent on specific hyphal structures on or in which nematodes can be trapped mechanically or by adhesion. The interests of studying these fungi come from their potential use as biological control agents against plant- and animal-parasitic nematodes. Studies on the molecular mechanisms of the interaction between nematode-trapping fungi and nematodes were initiated already in the 1950s. Recently, the infection process, including the differentiation of trap cells and the penetration and digestion of nematodes, has been examined using tools of genomics and functional genomics. The results from these studies are reviewed. We discuss how genomic approaches can provide insights into the infection process, the environmental factors that influence survival and activity in soils, and the mechanisms that could account for the variation in parasitic activity within and between species of nematode-trapping fungi.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Åhman J, Ek B, Rask L et al (1996) Sequence analysis and regulation of a gene encoding a cuticle-degrading serine protease from the nematophagous fungus Arthrobotrys oligospora. Microbiology 142:1605–1616
Åhman J, Johansson T, Olsson M et al (2002) Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl Environ Microbiol 68:3408–3415
Ahrén D, Ursing BM, Tunlid A (1998) Phylogeny of nematode-trapping fungi based on 18 S rDNA sequences. FEMS Microbiol Lett 158:179–184
Ahrén D, Tholander M, Fekete C et al (2005) Comparison of gene expression in trap cells and vegetative hyphae of the nematophagous fungus Monacrosporium haptotylum. Microbiology 151:789–803
Anderson IC, Cairney JW (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6:769–779
Bagga S, Hu G, Screen SE et al (2004) Reconstructing the diversification of subtilisins in the pathogenic fungus Metarhizium anisopliae. Gene 324:159–169
Balogh J, Tunlid A, Rosen S (2003) Deletion of a lectin gene does not affect the phenotype of the nematode-trapping fungus Arthrobotrys oligospora. Fungal Genet Biol 39:128–135
Barron GL (1977) The nematode-destroying fungi. Lancester Press, Guelph
Barron GL (1992) Lignolytic and cellulolytic fungi as predators and parasites. In: Carroll GC, Wicklow DT (eds) The fungal community. Marcel Dekker, New York, pp 311–326
Birck C, Damian L, Marty-Detraves C et al (2004) A new lectin family with structure similarity to actinoporins revealed by the crystal structure of Xerocomus chrysenteron lectin XCL. J Mol Biol 344:1409–1420
Blackwood CB, Waldrop MP, Zak DR et al (2007) Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition. Environ Microbiol 9:1306–1316
Bordallo JJ, Lopez-Llorca LV, Jansson H-B et al (2002) Colonization of plant roots by egg-parasitic and nematode-trapping fungi. New Phytol 154:491–499
Borrebaeck CA, Mattiasson B, Nordbring-Hertz B (1984) Isolation and partial characterization of a carbohydrate-binding protein from a nematode-trapping fungus. J Bacteriol 159:53–56
Breakspear A, Momany M (2007) The first fifty microarray studies in filamentous fungi. Microbiology 153:7–15
Carrizo ME, Capaldi S, Perduca M et al (2005) The antineoplastic lectin of the common edible mushroom (Agaricus bisporus) has two binding sites, each specific for a different configuration at a single epimeric hydroxyl. J Biol Chem 280:10614–10623
Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973–1983
Couillault C, Pujol N, Reboul J et al (2004) TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 5:488–494
Cox GN, Kusch M, Edgar RS (1981) Cuticle of Caenorhabditis elegans: its isolation and partial characterization. J Cell Biol 90:7–17
Dackman C, Nordbring-Hertz B (1992) Conidial traps: a new survival structure of the nematode-trapping fungus Arthrobotrys oligospora. Mycol Res 96:194–198
Davies KG (2005) Interactions between nematodes and microorganisms: bridging ecological and molecular approaches. Adv Appl Microbiol 57:53–78
DeZwaan TM, Carroll AM, Valent B et al (1999) Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11:2013–2030
Dijksterhuis J, Veenhuis M, Harder W et al (1994) Nematophagous fungi: physiological aspects and structure-function relationships. Adv Microb Physiol 36:111–143
Drechsler C (1941) Predacious fungi. Biol Rev Camb Philos Soc 16:265–290
Dudddington CL (1955) Fungi that attack microscopic animals. Bot Rev 7:377–439
Fekete C, Tholander M, Rajashekar B et al (2008) Paralysis of nematodes: shifts in the transcriptome of the nematode-trapping fungus Monacrosporium haptotylum during infection of Caenorhabditis elegans. Environ Microbiol 10:364–375
Ferea TL, Botstein D, Brown PO et al (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci USA 96:9721–9726
Friman E (1993) Isolation of trap cells from the nematode-trapping fungus Dactylaria candida. Exp Mycol 17:368–370
Friman E, Olsson S, Nordbring-Hertz B (1985) Heavy-trap formation by Arthrobotrys oligospora in liquid culture. FEMS Microbiol Ecol 31:17–21
Gaspard JT, Jaffe BA, Ferris H (1990) Meloidogyne incognita survival in soil infested with Paecilomyces lilacinus and Verticillium chlamydosporium. J Nematol 22:176–181
Gravato-Nobre MJ, Hodgkin J (2005) Caenorhabditis elegans as a model for innate immunity to pathogens. Cell Microbiol 7:741–751
Hagedorn G, Scholler M (1999) A reevaluation of predatory orbiliaceous fungi. I: Phylogentic analysis using rDNA sequence data. Sydowia 51:27–48
Hu G, Liu I, Sham A et al (2008) Comparative hybridization reveals extensive genome variation in the AIDS-associated pathogen Cryptococcus neoformans. Genome Biol 9:R41
Iijima N, Yoshino H, Ten LC et al (2002) Two genes encoding fruit body lectins of Pleurotus cornucopiae: sequence similarity with the lectin of a nematode-trapping fungus. Biosci Biotechnol Biochem 66:2083–2089
Jansson H-B, Lopez-Llorca LV (2004) Control of nematodes by fungi. In: Arora DK (ed) Fungal biotechnology in agricultural, food, and environmental applications. Marcel Dekker, New York, pp 205–215
Jin X, Ming-He M, Xiao-Wei H et al (2005) Improvement on genetic transformation in the nematode-trapping fungus Arthrobotrys oligospora and its quantification on dung samples. Mycopathologia 159:533–538
Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44:41–60
Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441
Kerry BR (2001) Exploitation of the nematophagous fungus Verticillium chlamydosporium Goddar for the biological control of root-knot nematodes (Meloidogyne spp.). In: Butt TM, Jackson C, Magan M (eds) Fungi as biocontrol agents; progress, problems and potential. CABI Publishing, Wallingford, pp 155–168
Khan A, Williams KL, Soon J et al (2008) Proteomic analysis of the knob-producing nematode-trapping fungus Monacrosporium lysipagum. Mycol Res 112:1447–1452
Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28:118–121
Larsen M (2000) Prospects for controlling animal parasitic nematodes by predacious micro fungi. Parasitology 120(Suppl):S121–S131
Le Quéré A, Schützendübel A, Rajashekar B et al (2004) Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus. Mol Ecol 13:3809–3819
Leonidas DD, Swamy BM, Hatzopoulos GN et al (2007) Structural basis for the carbohydrate recognition of the Sclerotium rolfsii lectin. J Mol Biol 368:1145–1161
Li Y, Hyde KD, Jeewon R et al (2005) Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia 97:1034–1046
Linford MB (1937) Stimulated activity of natural enemies of nematodes. Science 85:123–124
Liou GY, Tzean SS (1997) Phylogeny of the genus Arthrobotrys and allied nematode-trapping-fungi based on rDNA sequences. Mycologia 89:876–884
Mallo GV, Kurz CL, Couillault C et al (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12:1209–1214
McKew BA, Coulon F, Yakimov MM et al (2007) Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic bacteria. Environ Microbiol 9:1562–1571
Miura F, Kawaguchi N, Sese J et al (2006) A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc Natl Acad Sci USA 103:17846–17851
Morton CO, Hirsch PR, Kerry BR (2004) Infection of plant-parasitic nematodes by nematophagous fungi - a review of the application of molecular biology to understand infectionprocesses and to improve biological control. Nematology 6:161–170
Mylonakis E, Ausubel FM, Perfect JR et al (2002) Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci USA 99:15675–15680
Nicolaisen MH, Baelum J, Jacobsen CS et al (2008) Transcription dynamics of the functional tfdA gene during MCPA herbicide degradation by Cupriavidus necator AEO106 (pRO101) in agricultural soil. Environ Microbiol 10:571–579
Norbring-Hertz B, Jansson H-B, Persson Y et al (1995) Nematophagous fungi. Film C1851. Institut für den Wissenschafltichen Film, Göttingen
Nordbring-Hertz B (1973) Peptide induced morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. Physiol Plant 29:223–233
Nordbring-Hertz B (1977) Nematode-induced morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. Nematologica 23:443–451
Nordbring-Hertz B, Brinck B (1974) Quantitative characterization of some peptides inducing morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. Physiol Plant 31:59–63
Nordbring-Hertz B, Chet I (1988) Fungal lectins and agglutinins. In: Mirelman D (ed) Microbial lectins and agglutinins: properties and biological activity. Wiley, New York, pp 393–408
Nordbring-Hertz B, Mattiasson B (1979) Action of a nematode-trapping fungus shows lectin-mediated host-microorganism interaction. Nature 281:477–479
O’Rourke D, Baban D, Demidova M et al (2006) Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 16:1005–1016
Olthof THA, Estey RH (1963) A nemtatotoxin produced by the nematode-trapping fungus Arthrobotrys oligospora. Nature 197:514–525
Peay KG, Kennedy PG, Bruns T (2008) Fungal comminity ecology: a hybrid beast with a molecular master. BioScience 58:799–810
Peng T, Orsborn KI, Orbach MJ et al (1999) Proline-rich vaccine candidate antigen of Coccidioides immitis: conservation among isolates and differential expression with spherule maturation. J Infect Dis 179:518–521
Persmark L, Nordbring-Hertz B (1997) Conidial trap formation of nematode-trapping fungi in soil and soil extracts. FEMS Microbiol Ecol 22:313–323
Persson Y, Veenhuis M, Nordbring-Hertz B (1985) Morphogenesis and significance of hyphal coling by nemtaode-trapping fungi in mycoparasitic relationships. FEMS Microbiol Ecol 31:283–291
Pramer D, Kuyama S (1963) Symposium on biochemical bases of morphogenesis in fungi II: Nemin and the nematode-trapping fungi. Bacteriol Rev 27:282–292
Pramer D, Stoll NR (1959) Nemin: a morphogenetic substance causing trap formation by predaceous fungi. Science 129:966–967
Premachandran D, Pramer D (1984) Role of N-Acetylgalactosamine-specific protein in trapping of nematodes by Arthrobotrys oligospora. Appl Environ Microbiol 47:1358–1359
Rauyaree P, Choi W, Fang E et al (2004) Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Mol Plant Pathol 2:347–354
Rep M (2005) Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253:19–27
Rosén S, Ek B, Rask L et al (1992) Purification and characterization of a surface lectin from the nematode-trapping fungus Arthrobotrys oligospora. J Gen Microbiol 138:2663–2672
Rosén S, Bergstrom J, Karlsson KA et al (1996a) A multispecific saline-soluble lectin from the parasitic fungus Arthrobotrys oligospora. Similarities in the binding specificities compared with a lectin from the mushroom agaricus bisporus. Eur J Biochem 238:830–837
Rosén S, Kata M, Persson Y et al (1996b) Molecular characterization of a saline-soluble lectin from a parasitic fungus Extensive sequence similarities between fungal lectins. Eur J Biochem 238:822–829
Rosén S, Sjollema K, Veenhuis M et al (1997) A cytoplasmic lectin produced by the fungus Arthrobotrys oligospora functions as a storage protein during saprophytic and parasitic growth. Microbiology 143:2593–2604
Schenck S, Chase T, Rosenzweig WD et al (1980) Collagenase production by nematode-trapping fungi. Appl Environ Microbiol 40:567–570
Sharon N, Lis H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14:53R–62R
Siezen RJ, Leunissen JA (1997) Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci 6:501–523
Sifri CD, Begun J, Ausubel FM (2005) The worm has turned–microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13:119–127
Smith ME, Jaffee BA (2008) PCR Primers with Enhanced Specificity for Nematode-Trapping Fungi (Orbiliales). Microb Ecol 58:117–128
Smith CJ, Osborn AM (2009) Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol Ecol 67:6–20
Stadler M, Sterner O (1993) Linoleic acid - The nematicidal principle of several nematophagous fungi and its production in trap-forming submerged culture. Arch Microbiol 160:401–405
Stein LD, Bao Z, Blasiar D et al (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1:E45
Stirling GR, Smith LJ (1998) Filed tests of formulated products containing either Verticillium chlamydoposporium or Arthrobotrys dactyloides for biological control of root-knot nematodes. Biol Control 11:231–239
Swamy BM, Bhat AG, Hegde GV et al (2004) Immunolocalization and functional role of Sclerotium rolfsii lectin in development of fungus by interaction with its endogenous receptor. Glycobiology 14:951–957
Takano Y, Choi W, Mitchell TK et al (2004) Large scale parallel analysis of gene expression during infection-related morphogenesis of Magnaporthe grisea. Mol Plant Pathol 4:337–346
Thines E, Weber RW, Talbot NJ (2000) MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703–1718
Thomas SW, Glaring MA, Rasmussen SW et al (2002) Transcript profiling in the barley mildew pathogen Blumeria graminis by serial analysis of gene expression (SAGE). Mol Plant Microbe Interact 15:847–856
Tucker SL, Talbot NJ (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417
Tunlid A, Ahrén D (2001) Application of genomics to the improvement of nematode-trapping fungi. In: Vurro M, Gressel J, Butt T et al (eds) Enhancing biocontrol agents and handling risks. Ios Press, Amsterdam, pp 193–200
Tunlid A, Jansson S (1991) Proteases and their involvement in the infection and immobilization of nematodes by the nematophagous fungus Arthrobotrys oligospora. Appl Environ Microbiol 57:2868–2872
Tunlid A, Talbot NJ (2002) Genomics of parasitic and symbiotic fungi. Curr Opin Microbiol 5:513–519
Tunlid A, Rosen S, Ek B et al (1994) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys oligospora. Microbiology 140:1687–1695
Tunlid A, Åhman J, Oliver RP (1999) Transformation of the nematode-trapping fungus Arthrobotrys oligospora. FEMS Microbiol Lett 173:111–116
Wilhelm BT, Marguerat S, Watt S et al (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239–1243
Wright DP, Johansson T, Le Quéré A et al (2005) Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula Roth.) seedlings in soil microcosms. New Phytol 167:579–596
Yang J, Tian B, Liang L et al (2007a) Extracellular enzymes and the pathogenesis of nematophagous fungi. Appl Microbiol Biotechnol 75:21–31
Yang Y, Yang E, An Z et al (2007b) Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proc Natl Acad Sci USA 104:8379–8384
Yu LG, Andrews N, Weldon M et al (2002) An N-terminal truncated form of Orp150 is a cytoplasmic ligand for the anti-proliferative mushroom Agaricus bisporus lectin and is required for nuclear localization sequence-dependent nuclear protein import. J Biol Chem 277:24538–24545
Acknowledgments
Work done in the laboratory of the authors has been supported by grants from the Swedish Research Council (VR) and the Swedish Research Council for Agricultural Sciences and Spatial Planning (FORMAS).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Tunlid, A., Ahrén, D. (2011). Molecular Mechanisms of the Interaction Between Nematode-Trapping Fungi and Nematodes: Lessons From Genomics. In: Davies, K., Spiegel, Y. (eds) Biological Control of Plant-Parasitic Nematodes:. Progress in Biological Control, vol 11. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9648-8_6
Download citation
DOI: https://doi.org/10.1007/978-1-4020-9648-8_6
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-9647-1
Online ISBN: 978-1-4020-9648-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)