Biodiversity and systematics of nematode-bacterium entomopathogensIntroductionBacterial biodiversityPhylogenetic diversity and distribution of major bacterial lineagesDelimitation of bacterial speciesBiodiversity, phylogeny, and systematics of Xenorhabdus and PhotorhabdusThe life cycle of Xenorhabdus and PhotorhabdusTaxonomic characterizationPhenotypic characterizationMolecular characterizationPhylogenetic systematicsGnotobiologyAssociated microbial speciesSystematics, diversity, and biogeography of entomopathogenic nematodesDiversity and phylogenetic position of the NematodaEntomopathogenic nematode taxonomyMethodology: Species identification and diagnosisPhylogenetic systematicsBiodiversity and biogeographyPatterns of geographic distributionPatterns of habitat distributionConclusionsAcknowledgmentsReferencesBiological Control 38 (2006) 4–21www.elsevier.com/locate/ybcon1049-9644/$ - see front matter © 2005 Elsevier Inc. All rights reserved.doi:10.1016/S1049-9644(06)00126-5Reprint of “Biodiversity and systematics of nematode–bacterium entomopathogens” [Biol. Control 37 (2006) 32–49]夽Byron J. Adamsa,¤, Andras Fodorb, Heather S. Koppenhöferd, Erko Stackebrandte, S. Patricia Stockf, Michael G. Kleinca Microbiology and Molecular Biology Department, Evolutionary Ecology Laboratories, Brigham Young University, Provo, UT 84602-5253, USAb Department of Genetics, Eötvös University, H-1117 Budapest, Pàzmàny Peter sétány 1/C, Hungaryc The Ohio State University, USDA-ARS, 1680 Madison Ave., Wooster, OH 44691, USAd Entomology and Nematology Department, University of Florida, Gainesville, FL 32611-0620, USAe DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, 38124 Braunschweig, Germanyf Department of Entomology, University of Arizona, 410 Forbes Building, P.O. Box 210036, Tucson, AZ 85721-0036, USAReceived 9 June 2005; accepted 16 November 2005Available online 9 January 2006AbstractNematodes are one of the most abundant animals on earth, and bacteria comprise the most biologically and phylogenetically diversedomains of organisms. On at least two separate occasions a soil dwelling nematode and a bacterium have entered into a mutualistic, insec-ticidal association. From such origins arose two distinct lineages of nematode–bacterium entomopathogens, Steinernema–Xenorhabdusand Heterorhabditis–Photorhabdus. Herein, we present a summary and discussion of the known evolutionary diversity and systematics ofthese two groups relative to other nematodes and bacteria, and their shared evolutionary history.© 2005 Elsevier Inc. All rights reserved.Keywords: Biodiversity; Heterorhabditis; Steinernema; Photorhabdus; Xenorhabdus; Taxonomy; Systematics; Evolution; Entomopathogenic nematodes;Mutualism; Symbiosis1. IntroductionNematodes are the most abundant animals on earth, andbacteria are the most biologically and phylogeneticallydiverse (Bongers and Ferris, 1999; Curtis and Sloan, 2004;Curtis et al., 2002; Rappe and Giovannoni, 2003; Torsviket al., 2002). Cyanobacterial fossils date to 2.9 billion yearsago (NoVke et al., 2003), whereas nematodes most likelyarose slightly prior to or during the Cambrian explosion(Ayala and Rzhetsky, 1998; Rodriguez-Trelles et al., 2002;Wray et al., 1996). Discovering the full extent of biodiver-sity of these two clades is one of the greatest challenges fac-ing modern science. Technological and analyticalchallenges faced by nematode and bacterial systematists aresimilar, yet the greatest dilemma may be the overwhelmingdiscrepancy between the number of systematists workingon the problem and the estimated number of species need-ing description (Wheeler et al., 2004). The number of nema-tode taxonomists has diminished to critical levels, withextinction looming on the horizon (Ferris, 1994). Institu-tional support for bacterial culture collections is at presentincapable of accommodating even a small fraction of theyet to be catalogued specimens, and dollar estimates to seesuch projects to completion involve multiples of billions.But despite the unknown systematic status for the majority夽A publisher’s error resulted in this article appearing in the wrong issue.The article is reprinted here for the reader’s convenience and for the conti-nuity of this special issue. Anyone wishing to cite this article should use thedetails of the original publication [Adams, B.J., Fodor, A., Koppenhöfer,H.S., Stackebrandt, E., Stock, S.P., Klien, M.G., 2006. Biodiversity and sys-tematics of nematode–bacterium entomopathogens. Biol. Control 37, 32–49, doi:10.1016/j.biocontrol.2005.11.008].*Corresponding author. Fax: +1 801 422 0519.E-mail address: [email protected] (B.J. Adams).B.J. Adams et al. / Biological Control 38 (2006) 4–21 5of nematode and bacterial taxa, nematode–bacterium ento-mopathogens are some of the best-studied members ofthese tremendously diverse groups of organisms.It has been speculated that in the mid-Paleozoic (approxi-mately 350 million years ago) ancestors of the Heterorhab-ditidae and Steinernematidae began to independently exploremutualistic relationships with Gram-negative enteric bacteria(Enterobacteriaceae), the respective lineages of which wouldevolve to comprise Photorhabdus and Xenorhabdus (Poinar,1993). The resulting bacterium–nematode complex comprisesa formidable biological control weapon against insect pests,which probably best explains the accelerated pace of system-atic activity that has focused on these groups over the last 15years. Our knowledge of bacterial and nematode biodiversityat the present is so poor that even the most sophisticatedbootstrapping estimates are at best a modest grope towardsreality (Boucher and Lambshead, 1995; Lambshead, 1993).In sharp contrast are the entomopathogenic bacterium–nem-atode complexes, which have been the subject of substantialeVorts to reveal their true biological diversity and place themin a meaningful systematic framework. As dynamic processesof discovery, these research programs include samplingeVorts that extend to previously unexplored regions of theglobe, and evolutionary studies of their historical lineages,from their position within the tree of life, to populationgenetic structure. Acknowledging that the discovery of eachnew species renders previous statements of biodiversity obso-lete and that there are considerable technological and analyt-ical challenges and gaps that need further scrutiny, the goalof this paper is to summarize