Systematics and phylogeny of the entomopathogenic nematobacterial complexes Steinernema-Xenorhabdus and Heterorhabditis-Photorhabdus.
Beneficial microorganisms
Biological control agents
Entomopathogens
Phylogeny
Systematics
Taxonomy
Journal
Zoological letters
ISSN: 2056-306X
Titre abrégé: Zoological Lett
Pays: England
ID NLM: 101664800
Informations de publication
Date de publication:
17 Jul 2024
17 Jul 2024
Historique:
received:
16
02
2024
accepted:
08
06
2024
medline:
18
7
2024
pubmed:
18
7
2024
entrez:
17
7
2024
Statut:
epublish
Résumé
Entomopathogenic nematodes of the genera Steinernema and Heterorhabditis, along with their bacterial symbionts from the genera Xenorhabdus and Photorhabdus, respectively, are important biological control agents against agricultural pests. Rapid progress in the development of genomic tools has catalyzed a transformation of the systematics of these organisms, reshaping our understanding of their phylogenetic and cophlylogenetic relationships. In this review, we discuss the major historical events in the taxonomy and systematics of this group of organisms, highlighting the latest advancements in these fields. Additionally, we synthesize information on nematode-bacteria associations and assess the existing evidence regarding their cophylogenetic relationships.
Identifiants
pubmed: 39020388
doi: 10.1186/s40851-024-00235-y
pii: 10.1186/s40851-024-00235-y
doi:
Types de publication
Journal Article
Review
Langues
eng
Pagination
13Subventions
Organisme : Swiss National Science Foundation
ID : 186094
Pays : Switzerland
Organisme : Grantová Agentura České Republiky
ID : 23-06457S
Informations de copyright
© 2024. The Author(s).
Références
Poinar G. Nematodes for Biological Control of insects. Fla: CRCPress. Inc Boca Raton; 1979. p. 277.
Boemare N, Akhurst R, Mourant R. DNA relatedness between Xenorhabdus spp.(Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. Nov. Int J Syst Bacteriol. 1993;43:249–55.
doi: 10.1099/00207713-43-2-249
Bovien P. Some types of association between nematodes and insects. 1937.
Khan A, Brooks W, Hirschmann H. Chromonema heliothidis n. gen., n. sp. (Steinernematidae, Nematoda), a parasite of Heliothis Zea (Noctuidae, Lepidoptera), and other insects. J Nematology. 1976;8:159.
Dutky SR. Investigation of the diseases of the immature stages of the Japanese beetle. 1937.
Ogier J-C, Akhurst R, Boemare N, Gaudriault S. The endosymbiont and the second bacterial circle of entomopathogenic nematodes. Trends Microbiol. 2023;31:629–43.
pubmed: 36801155
doi: 10.1016/j.tim.2023.01.004
Ogier J-C, Pagès S, Frayssinet M, Gaudriault S. Entomopathogenic nematode-associated microbiota: from monoxenic paradigm to pathobiome. Microbiome. 2020;8:1–17.
doi: 10.1186/s40168-020-00800-5
Ruiu L, Marche MG, Mura ME, Tarasco E. Involvement of a novel Pseudomonas protegens strain associated with entomopathogenic nematode infective juveniles in insect pathogenesis. Pest Manag Sci. 2022;78:5437–43.
pubmed: 36057860
pmcid: 9826039
doi: 10.1002/ps.7166
Zwyssig M, Spescha A, Patt T, Belosevic A, Machado RA, Regaiolo A et al. Entomopathogenic pseudomonads can share an insect host with entomopathogenic nematodes and their mutualistic bacteria. ISME J. 2024;wrae028.
Akhurst R, Boemare N. Biology and taxonomy of Xenorhabdus. Entomopathogenic nematodes in biological control. CRC; 1990. pp. 75–90.
Stock SP. Partners in crime: symbiont-assisted resource acquisition in Steinernema entomopathogenic nematodes. Curr Opin Insect Sci. 2019;32:22–7.
pubmed: 31113627
doi: 10.1016/j.cois.2018.10.006
Griffin C, Boemare N, Lewis E. Biology and behaviour. Nematodes as Biocontrol Agents. 2005;47–64.
Dowds BC, Peters A. Virulence mechanisms. Entomopathogenic nematology. CABI publishing Wallingford UK; 2002. pp. 79–98.
Půža V. Control of insect pests by entomopathogenic nematodes. Principles of plant-microbe interactions. Springer; 2015. pp. 175–83.
Somvanshi VS, Sloup RE, Crawford JM, Martin AR, Heidt AJ, Kim K, et al. A single promoter inversion switches Photorhabdus between pathogenic and mutualistic states. Science. 2012;337:88–93.
pubmed: 22767929
pmcid: 4006969
doi: 10.1126/science.1216641
Haag ES, Fitch DH, Delattre M. From the worm to the worms and back again: the evolutionary developmental biology of nematodes. Genetics. 2018;210:397–433.
pubmed: 30287515
pmcid: 6216592
doi: 10.1534/genetics.118.300243
Laumond C, Mauleon H, Kermarrec A. [New data on the host spectrum and the parasitism of the entomophagous nematode, Neoaplectana carpocapsae [biological control]].[French]. Entomophaga. 1979;24:13–27.
doi: 10.1007/BF02377505
Woodring JL, Kaya HK. Steinernematid and heterorhabditid nematodes: a handbook of biology and techniques. Southern cooperative series bulletin (USA), Arkansas Agricultural Experiment Station. 1988.
Bathon H. Impact of entomopathogenic nematodes on non-target hosts. Biocontrol Sci Technol. 1996;6:421–34.
doi: 10.1080/09583159631398
Piedra-Buena A, López-Cepero J, Campos-Herrera R. Entomopathogenic nematode production and application: regulation, ecological impact and non–target effects. Nematode pathogenesis of insects and other pests: Ecology and Applied technologies for sustainable plant and Crop Protection. Springer; 2015. pp. 255–82.
Ehlers R-U, Hokkanen H. Insect biocontrol with non-endemic entomopathogenic nematodes (Steinernema and Heterorhabditis spp.): conclusions and recommendations of a combined OECD and COST workshop on scientific and regulatory policy issues. Biocontrol Sci Technol. 1996;6:295–302.
doi: 10.1080/09583159631280
Kaya HK, Gaugler R. Entomopathogenic nematodes. Ann Rev Entomol. 1993;38:181–206.
doi: 10.1146/annurev.en.38.010193.001145
Bruno P, Machado RA, Glauser G, Köhler A, Campos-Herrera R, Bernal J, et al. Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Sci Rep. 2020;10:8257.
pubmed: 32427834
pmcid: 7237494
doi: 10.1038/s41598-020-64945-x
Machado RA, Thönen L, Arce CC, Theepan V, Prada F, Wüthrich D, et al. Engineering bacterial symbionts of nematodes improves their biocontrol potential to counter the western corn rootworm. Nat Biotechnol. 2020;38:600–8.
pubmed: 32066956
doi: 10.1038/s41587-020-0419-1
Daborn P, Waterfield N, Silva C, Au C, Sharma S, Ffrench-Constant R. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci. 2002;99:10742–7.
pubmed: 12136122
pmcid: 125031
doi: 10.1073/pnas.102068099
Bode HB. Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol. 2009;13:224–30.
pubmed: 19345136
doi: 10.1016/j.cbpa.2009.02.037
Fujdiarová E, Houser J, Dobeš P, Paulíková G, Kondakov N, Kononov L, et al. Heptabladed β-propeller lectins PLL2 and PHL from Photorhabdus spp. recognize O‐methylated sugars and influence the host immune system. FEBS J. 2021;288:1343–65.
pubmed: 32559333
doi: 10.1111/febs.15457
Cimen H, Touray M, Gulsen SH, Hazir S. Natural products from Photorhabdus and Xenorhabdus: mechanisms and impacts. Appl Microbiol Biotechnol. 2022;106:4387–99.
pubmed: 35723692
doi: 10.1007/s00253-022-12023-9
Půža V, Tarasco E. Interactions between entomopathogenic fungi and entomopathogenic nematodes. Microorganisms. 2023;11:163.
pubmed: 36677455
pmcid: 9864569
doi: 10.3390/microorganisms11010163
Wollenberg AC, Jagdish T, Slough G, Hoinville ME, Wollenberg MS. Death becomes them: bacterial community dynamics and stilbene antibiotic production in cadavers of Galleria mellonella killed by Heterorhabditis and Photorhabdus spp. Applied and environmental microbiology. 2016;82:5824–37.
Baur M, Kaya H, Strong D. Foraging ants as scavengers on entomopathogenic nematode-killed insects. Biol Control. 1998;12:231–6.
doi: 10.1006/bcon.1998.0635
Foltan P, Puza V. To complete their life cycle, pathogenic nematode–bacteria complexes deter scavengers from feeding on their host cadaver. Behav Process. 2009;80:76–9.
doi: 10.1016/j.beproc.2008.09.012
Gulcu B, Hazir S, Kaya HK. Scavenger deterrent factor (SDF) from symbiotic bacteria of entomopathogenic nematodes. J Invertebr Pathol. 2012;110:326–33.
pubmed: 22446508
doi: 10.1016/j.jip.2012.03.014
Hunt DJ, Subbotin SA. Taxonomy and systematics. Advances in entomopathogenic nematode taxonomy and phylogeny. Brill; 2016. pp. 13–58.
Nemys eds. Nemys: World Database of Nematodes. Accessed at https://nemys.ugent.be on 2023-12-13. 2023.
Adams BJ. Species concepts and the evolutionary paradigm in modem nematology. J Nematology. 1998;30:1.
Spiridonov SE, Reid AP, Podrucka K, Subbotin SA, Moens M. Phylogenetic relationships within the genus Steinernema (Nematoda: Rhabditida) as inferred from analyses of sequences of the ITS1-5.8 S-ITS2 region of rDNA and morphological features. Nematology. 2004;6:547–66.
doi: 10.1163/1568541042665304
Adams BJ, Peat SM, Dillman AR. Phylogeny and evolution. Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts. Brill; 2007. pp. 693–733.
Půža V, Chundelová D, Nermuť J, Žurovcová M, Mráček Z. Intra-individual variability of ITS regions in entomopathogenic nematodes (Steinernematidae: Nematoda): implications for their taxonomy. Biocontrol. 2015;60:547–54.
doi: 10.1007/s10526-015-9664-5
Nguyen KB. Methodology, morphology and identification. Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts. Brill; 2007. pp. 59–119.
Lis M, Sajnaga E, Skowronek M, Wiater A, Rachwał K, Kazimierczak W. Steinernema sandneri n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from Poland. J Nematology. 2021;53:1–24.
doi: 10.21307/jofnem-2021-051
Bhat AH, Machado RA, Abolafia J, Askary TH, Půža V, Ruiz-Cuenca AN et al. Multigene sequence-based and phenotypic characterization reveals the occurrence of a Novel Entomopathogenic Nematode species, Steinernema anantnagense n. sp. J Nematology. 2023;55.
Dhakal M, Nguyen KB, Hunt DJ, Ehlers RU, Spiridonov SE, Subbotin SA. Molecular identification, phylogeny and phylogeography of the entomopathogenic nematodes of the genus Heterorhabditis Poinar, 1976: a multigene approach. Nematology. 2020;23:451–66.
doi: 10.1163/15685411-bja10052
Machado RA, Bhat AH, Abolafia J, Muller A, Bruno P, Fallet P, et al. Multi-locus phylogenetic analyses uncover species boundaries and reveal the occurrence of two new entomopathogenic nematode species, Heterorhabditis ruandica n. sp. and Heterorhabditis zacatecana n. sp. J Nematology. 2021;53:1–42.
doi: 10.21307/jofnem-2021-089
Bhat AH, Machado RA, Abolafia J, Ruiz-Cuenca AN, Askary TH, Ameen F, et al. Taxonomic and molecular characterization of a new entomopathogenic nematode species, Heterorhabditis casmirica n. sp., and whole genome sequencing of its associated bacterial symbiont. Parasites Vectors. 2023;16:383.
pubmed: 37880744
pmcid: 10598981
doi: 10.1186/s13071-023-05990-z
Spiridonov SE. Entomopathogenic nematodes of the families Steinernematidae and Heterorhabditidae: morphology and taxonomy. Biocontrol agents: entomopathogenic and slug parasitic nematodes. Wallingford UK: CABI; 2017. pp. 45–62.
doi: 10.1079/9781786390004.0045
Smythe AB, Holovachov O, Kocot KM. Improved phylogenomic sampling of free-living nematodes enhances resolution of higher-level nematode phylogeny. BMC Evol Biol. 2019;19:1–15.
doi: 10.1186/s12862-019-1444-x
Ahmed M, Holovachov O. Twenty years after De Ley and Blaxter—How far did we progress in understanding the phylogeny of the phylum Nematoda? Animals. 2021;11:3479.
pubmed: 34944255
pmcid: 8697950
doi: 10.3390/ani11123479
Ahmed M, Roberts NG, Adediran F, Smythe AB, Kocot KM, Holovachov O. Phylogenomic analysis of the phylum Nematoda: conflicts and congruences with morphology, 18S rRNA, and mitogenomes. Front Ecol Evol. 2022;9:769565.
doi: 10.3389/fevo.2021.769565
Nguyen KB, Shapiro-Ilan DI, Mbata GN. Heterorhabditis georgiana n. sp. (Rhabditida: Heterorhabditidae) from Georgia. USA Nematology. 2008;10:433–48.
doi: 10.1163/156854108783900276
Spiridonov SE, Subbotin SA. Phylogeny and phylogeography of Heterorhabditis and Steinernema. Advances in entomopathogenic nematode taxonomy and phylogeny. Brill; 2016. pp. 413–27.
Patricia Stock S, Campbell JF, Nadler SA. Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. J Parasitol. 2001;87:877–89.
doi: 10.1645/0022-3395(2001)087[0877:POSTCS]2.0.CO;2
Weiser J. Neoaplectana carpocapsae n. sp. (Anguillulata, Steinernematinae), novy cizopasník housenek obalece jablecného, Carpocapsa pomonella L.[Czech]. Vestnik Ceskoslovenske Spolecnosti Zoologicke. 1955;19:44–52.
Poinar GO, Thomas GM. Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 (Neoaplectana sp. Steinernematidae). Parasitology. 1966;56:385–90.
pubmed: 4960247
doi: 10.1017/S0031182000070980
Dutky S, Hough W. Note on a parasitic nematode from codling moth larvae. Carpocapsa pamonetta. Lepidoptera, Olethreutidae; 1955.
Anonymous. Nematode-borne disease that attacks insects is discovered by USDA scientist. USDA Press Release; 1955.
Poinar GO. The presence of Achromobacter nematophilus in the infective stage of a Neoaplectana sp. (Steinernematidae: Nematoda). Nematologica. 1966;12:105–8.
doi: 10.1163/187529266X00068
Poinar GO Jr, Himsworth PT. Neoaplectana parasitism of larvae of the greater wax moth, Galleria mellonella. J Invertebr Pathol. 1967;9:241–6.
doi: 10.1016/0022-2011(67)90012-2
Khan A, Brooks W. A chromogenic bioluminescent bacterium associated with the entomophilic nematode Chromonema heliothidis. J Invertebr Pathol. 1977;29:253–61.
doi: 10.1016/S0022-2011(77)80030-X
Poinar GO, Thomas GM, Hess R. Characteristics of the specific bacterium associated with Heterorhabditis Bacteriophora (Heterorhabditidae: Rhabditida). Nematologica. 1977;23:97–102.
doi: 10.1163/187529277X00273
Milstead JE. Heterorhabditis bacteriophora as a vector for introducing its associated bacterium into the hemocoel of Galleria mellonella larvae. J Invertebr Pathol. 1979;33:324–7.
doi: 10.1016/0022-2011(79)90033-8
Castellani A, Chalmers AJ. Manual of tropical medicine. Baillière, Tindall and Cox; 1919.
Hendrie MS, Holding A, Shewan JM. Emended descriptions of the genus Alcaligenes and of Alcaligenes faecalis and proposal that the generic name Achromobacter be rejected: status of the named species of Alcaligenes and Achromobacter: request for an opinion. Int J Syst Evol MicroBiol. 1974;24:534–50.
Thomas GM, Poinar JRGO. Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic bacteria of the family Enterobacteriaceae. International Journal of Systematic and Evolutionary Microbiology. 1979;29:352–60.
Burnell A, Stock SP, Heterorhabditis. Steinernema and their bacterial symbionts—lethal pathogens of insects. Nematology. 2000;2:31–42.
doi: 10.1163/156854100508872
Wee KE, Yonan CR, Chang F. A new broad-spectrum protease inhibitor from the entomopathogenic bacterium Photorhabdus luminescens. Microbiology. 2000;146:3141–7.
pubmed: 11101672
doi: 10.1099/00221287-146-12-3141
Akhurst R. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. Microbiology. 1980;121:303–9.
doi: 10.1099/00221287-121-2-303
Akhurst R. Neoaplectana species: specificity of association with bacteria of the genus Xenorhabdus. Exp Parasitol. 1983;55:258–63.
pubmed: 6832284
doi: 10.1016/0014-4894(83)90020-6
Thomas G, Poinar G Jr. Amended description of the genus Xenorhabdus Thomas and Poinar. Int J Syst Evol MicroBiol. 1983;33:878–9.
Akhurst R, Brooks W. The distribution of entomophilic nematodes (Heterorhabditidae and Steinernematidae) in North Carolina. J Invertebr Pathol. 1984;44:140–5.
doi: 10.1016/0022-2011(84)90004-1
Grimont PA, Steigerwalt A, Boemare N, Hickman-Brenner F, Deval C, Grimont F, et al. Deoxyribonucleic acid relatedness and phenotypic study of the genus Xenorhabdus. Int J Syst Evol MicroBiol. 1984;34:378–88.
Hotchkin PG, Kaya HK. Electrophoresis of Soluble Proteins from two species of Xenorhabdus, Bacteria Mutualistically Associated with the nematodes Steinernema spp. and Heterohabditis spp. Microbiology. 1984;130:2725–31.
doi: 10.1099/00221287-130-10-2725
Akhurst RJ. Xenorhabdus nematophilus subsp. beddingii (Enterobacteriaceae): a new subspecies of bacteria mutualistically associated with entomopathogenic nematodes. Int J Syst Evol MicroBiol. 1986;36:454–7.
Akhurst RJ. Xenorhabdus nematophilus subsp. poinarii: its interaction with insect pathogenic nematodes. Syst Appl Microbiol. 1986;8:142–7.
doi: 10.1016/S0723-2020(86)80162-X
Akhurst R, Boemare N. A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of X. nematophilus to species. Microbiology. 1988;134:1835–45.
doi: 10.1099/00221287-134-7-1835
Yamanaka S, Hagiwara A, Nishimura Y, Tanabe H, Ishibashi N. Biochemical and physiological characteristics of Xenorhabdus species, symbiotically associated with entomopathogenic nematodes including Steinernema kushidai and their pathogenicity against Spodoptera litura (Lepidoptera: Noctuidae). Arch Microbiol. 1992;158:387–93.
doi: 10.1007/BF00276297
Nishimura Y, Hagiwara A, Suzuki T, Yamanaka S. Xenorhabdus japonicus sp. nov. associated with the nematode Steinernema kushidai. World J Microbiol Biotechnol. 1994;10:207–10.
pubmed: 24420949
doi: 10.1007/BF00360889
Ehlers R-U, Wyss U, Stackebrandt E. 16S rRNA cataloguing and the phylogenetic position of the genus Xenorhabdus. Syst Appl Microbiol. 1988;10:121–5.
doi: 10.1016/S0723-2020(88)80025-0
Farmer J 3rd, Jorgensen J, Grimont P, Akhurst R, Poinar G Jr, Ageron E, et al. Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens. J Clin Microbiol. 1989;27:1594–600.
pubmed: 2768446
pmcid: 267621
doi: 10.1128/jcm.27.7.1594-1600.1989
Pütz J, Meinert F, Wyss U, Ehlers R, Stackebrandt E. Development and application of oligonucleotide probes for molecular identification of Xenorhabdus species. Appl Environ Microbiol. 1990;56:181–6.
pubmed: 2310180
pmcid: 183270
doi: 10.1128/aem.56.1.181-186.1990
Suzuki T, Yamanaka S, Nishimura Y. Chemotaxonomic study of Xenorhabdus species-cellular fatty acids, ubiquinone and DNA-DNA hybridization. J Gen Appl Microbiol. 1990;36:393–401.
doi: 10.2323/jgam.36.393
Aguillera MM, Hodge NC, Stall RE, Smart GC Jr. Bacterial symbionts of Steinernema scapterisci. J Invertebr Pathol. 1993;62:68–72.
doi: 10.1006/jipa.1993.1076
Akhurst RJ. Taxonomic study of Xenorhabdus, a genus of bacteria symbiotically associated with insect pathogenic nematodes. Int J Syst Evol MicroBiol. 1983;33:38–45.
Rainey F, Ehlers R-U, Stackebrandt E. Inability of the polyphasic approach to systematics to determine the relatedness of the genera Xenorhabdus and Photorhabdus. Int J Syst Evol MicroBiol. 1995;45:379–81.
Suzuki T, Yabusaki H, Nishimura Y. Phylogenetic relationships of entomopathogenic nematophilic bacteria: Xenorhabdus spp. and Photorhabdus sp. J Basic Microbiol. 1996;36:351–4.
pubmed: 8914266
doi: 10.1002/jobm.3620360509
Brunel B, Givaudan A, Lanois A, Akhurst R, Boemare N. Fast and accurate identification of Xenorhabdus and Photorhabdus species by restriction analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol. 1997;63:574–80.
pubmed: 9023937
pmcid: 168349
doi: 10.1128/aem.63.2.574-580.1997
Liu J, Berry R, Poinar G, Moldenke A. Phylogeny of Photorhabdus and Xenorhabdus species and strains as determined by comparison of partial 16S rRNA gene sequences. Int J Syst Evol MicroBiol. 1997;47:948–51.
Szállás E, Koch C, Fodor A, Burghardt J, Buss O, Szentirmai A, et al. Phylogenetic evidence for the taxonomic heterogeneity of Photorhabdus luminescens. Int J Syst Evol MicroBiol. 1997;47:402–7.
Fischer-Le Saux M, Mauléon H, Constant P, Brunel B, Boemare N. PCR-ribotyping of Xenorhabdus and Photorhabdus isolates from the Caribbean region in relation to the taxonomy and geographic distribution of their nematode hosts. Appl Environ Microbiol. 1998;64:4246–54.
pubmed: 9797272
pmcid: 106634
doi: 10.1128/AEM.64.11.4246-4254.1998
Fischer-Le Saux M, Viallard V, Brunel B, Normand P, Boemare NE. Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp. temperata subsp. nov. and P. asymbiotica sp. nov. Int J Syst Evol MicroBiol. 1999;49:1645–56.
doi: 10.1099/00207713-49-4-1645
Liu J, Berry RE, Blouin MS. Identification of symbiotic bacteria (Photorhabdus and Xenorhabdus) from the entomopathogenic nematodes Heterorhabditis marelatus and Steinernema oregonense based on 16S rDNA sequence. J Invertebr Pathol. 2001;77:87–91.
pubmed: 11273687
doi: 10.1006/jipa.2001.5007
Lengyel K, Lang E, Fodor A, Szállás E, Schumann P, Stackebrandt E. Description of four novel species of Xenorhabdus, family Enterobacteriaceae: Xenorhabdus budapestensis sp. nov., Xenorhabdus ehlersii sp. nov., Xenorhabdus innexi sp. nov., and Xenorhabdus szentirmaii sp. nov. Syst Appl Microbiol. 2005;28:115–22.
pubmed: 15830803
doi: 10.1016/j.syapm.2004.10.004
Somvanshi VS, Lang E, Ganguly S, Swiderski J, Saxena AK, Stackebrandt E. A novel species of Xenorhabdus, family Enterobacteriaceae: Xenorhabdus indica sp. nov., symbiotically associated with entomopathogenic nematode Steinernema thermophilum Ganguly and Singh, 2000. Syst Appl Microbiol. 2006;29:519–25.
pubmed: 16459045
doi: 10.1016/j.syapm.2006.01.004
Tailliez P, Pages S, Ginibre N, Boemare N. New insight into diversity in the genus Xenorhabdus, including the description of ten novel species. Int J Syst Evol MicroBiol. 2006;56:2805–18.
pubmed: 17158981
doi: 10.1099/ijs.0.64287-0
Tailliez P, Laroui C, Ginibre N, Paule A, Pagès S, Boemare N. Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. luminescens subsp. thracensis as P. temperata subsp. thracensis comb. nov. Int J Syst Evol MicroBiol. 2010;60:1921–37.
pubmed: 19783607
doi: 10.1099/ijs.0.014308-0
Tailliez P, Pagès S, Edgington S, Tymo LM, Buddie AG. Description of Xenorhabdus magdalenensis sp. nov., the symbiotic bacterium associated with Steinernema australe. Int J Syst Evol MicroBiol. 2012;62:1761–5.
pubmed: 21948091
doi: 10.1099/ijs.0.034322-0
Ferreira T, Van Reenen CA, Endo A, Spröer C, Malan AP, Dicks LM. Description of Xenorhabdus khoisanae sp. nov., the symbiont of the entomopathogenic nematode Steinernema khoisanae. Int J Syst Evol MicroBiol. 2013;63:3220–4.
pubmed: 23456807
doi: 10.1099/ijs.0.049049-0
Kuwata R, Qiu L, Wang W, Harada Y, Yoshida M, Kondo E, et al. Xenorhabdus ishibashii sp. nov., isolated from the entomopathogenic nematode Steinernema aciari. Int J Syst Evol MicroBiol. 2013;63:1690–5.
pubmed: 22922533
doi: 10.1099/ijs.0.041145-0
Kämpfer P, Tobias NJ, Ke LP, Bode HB, Glaeser SP. Xenorhabdus thuongxuanensis sp. nov. and Xenorhabdus eapokensis sp. nov., isolated from Steinernema species. Int J Syst Evol MicroBiol. 2017;67:1107–14.
pubmed: 28056225
doi: 10.1099/ijsem.0.001770
Castaneda-Alvarez C, Prodan S, Zamorano A, San-Blas E, Aballay E. Xenorhabdus lircayensis sp. nov., the symbiotic bacterium associated with the entomopathogenic nematode Steinernema unicornum. Int J Syst Evol MicroBiol. 2021;71:005151.
doi: 10.1099/ijsem.0.005151
Machado RA, Bhat AH, Castaneda-Alvarez C, Askary TH, Půža V, Pagès S, et al. Xenorhabdus aichiensis sp. nov., Xenorhabdus anantnagensis sp. nov., and Xenorhabdus yunnanensis sp. nov., isolated from Steinernema Entomopathogenic Nematodes. Curr Microbiol. 2023;80:300.
pubmed: 37493817
pmcid: 10371910
doi: 10.1007/s00284-023-03373-2
Machado RA, Bhat AH, Fallet P, Turlings TC, Kajuga J, Yan X, et al. Xenorhabdus bovienii subsp. africana subsp. nov., isolated from Steinernema africanum entomopathogenic nematodes. Int J Syst Evol MicroBiol. 2023;73:005795.
doi: 10.1099/ijsem.0.005795
Ritter CL, Malan AP, Dicks LM. Xenorhabdus bakwenae sp. n., associated with the entomopathogenic nematode Steinernema bakwenae. Nematology. 2023;25:1169–79.
doi: 10.1163/15685411-bja10284
Ehlers R-U, Niemann I. Molecular identification of Photorhabdus luminescens strains by amplification of specific fragments of the 16S ribosomal DNA. Syst Appl Microbiol. 1998;21:509–19.
pubmed: 9924819
doi: 10.1016/S0723-2020(98)80063-5
Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev. 1996;60:407–38.
pubmed: 8801440
pmcid: 239450
doi: 10.1128/mr.60.2.407-438.1996
Wayne L, Brenner D, Colwell R, Grimont P, Kandler O, Krichevsky M, et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol MicroBiol. 1987;37:463–4.
doi: 10.1099/00207713-37-4-463
Hazir S, Stackebrandt E, Lang E, Schumann P, Ehlers R-U, Keskin N. Two new subspecies of Photorhabdus luminescens, isolated from Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae): Photorhabdus luminescens subsp. kayaii subsp. nov. and Photorhabdus luminescens subsp. thracensis subsp. nov. Syst Appl Microbiol. 2004;27:36–42.
pubmed: 15053319
doi: 10.1078/0723-2020-00255
Toth T, Lakatos T. Photorhabdus temperata subsp. cinerea subsp. nov., isolated from Heterorhabditis nematodes. Int J Syst Evol MicroBiol. 2008;58:2579–81.
pubmed: 18984696
doi: 10.1099/ijs.0.2008/000273-0
An R, Grewal PS. Photorhabdus temperata subsp. stackebrandtii subsp. nov.(Enterobacteriales: Enterobacteriaceae). Curr Microbiol. 2010;61:291–7.
pubmed: 20852981
doi: 10.1007/s00284-010-9610-9
An R, Grewal PS. Photorhabdus luminescens subsp. kleinii subsp. nov.(Enterobacteriales: Enterobacteriaceae). Curr Microbiol. 2011;62:539–43.
pubmed: 20717672
doi: 10.1007/s00284-010-9741-z
Ferreira T, Van Reenen C, Pages S, Tailliez P, Malan AP, Dicks LM. Photorhabdus luminescens subsp. noenieputensis subsp. nov., a symbiotic bacterium associated with a novel Heterorhabditis species related to Heterorhabditis indica. Int J Syst Evol MicroBiol. 2013;63:1853–8.
pubmed: 22984141
doi: 10.1099/ijs.0.044388-0
Ferreira T, van Reenen CA, Endo A, Tailliez P, Pages S, Spröer C, et al. Photorhabdus heterorhabditis sp. nov., a symbiont of the entomopathogenic nematode Heterorhabditis zealandica. Int J Syst Evol MicroBiol. 2014;64:1540–5.
pubmed: 24478206
doi: 10.1099/ijs.0.059840-0
Glaeser SP, Tobias NJ, Thanwisai A, Chantratita N, Bode HB, Kämpfer P. Photorhabdus luminescens subsp. namnaonensis subsp. nov., isolated from Heterorhabditis baujardi nematodes. International Journal of Systematic and Evolutionary Microbiology. 2017;67:1046–51.
Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, et al. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol MicroBiol. 2009;59:102–11.
pubmed: 19126732
doi: 10.1099/ijs.0.001123-0
Glaeser SP, Kämpfer P. Multilocus sequence analysis (MLSA) in prokaryotic taxonomy. Syst Appl Microbiol. 2015;38:237–45.
pubmed: 25959541
doi: 10.1016/j.syapm.2015.03.007
López-Hermoso C, de la Haba RR, Sánchez-Porro C, Papke RT, Ventosa A. Assessment of multilocus sequence analysis as a valuable tool for the classification of the genus Salinivibrio. Front Microbiol. 2017;8:1107.
pubmed: 28690592
pmcid: 5479898
doi: 10.3389/fmicb.2017.01107
Machado RA, Wüthrich D, Kuhnert P, Arce CC, Thönen L, Ruiz C et al. Whole-genome-based revisit of Photorhabdus phylogeny: proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov. International journal of systematic and evolutionary microbiology. 2018;68:2664–81.
Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci. 2009;106:19126–31.
pubmed: 19855009
pmcid: 2776425
doi: 10.1073/pnas.0906412106
Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci. 2010;2:117–34.
pubmed: 21304684
pmcid: 3035253
doi: 10.4056/sigs.531120
Auch AF, Klenk H-P, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci. 2010;2:142–8.
pubmed: 21304686
pmcid: 3035261
doi: 10.4056/sigs.541628
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics. 2013;14:1–14.
doi: 10.1186/1471-2105-14-60
Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V, Fiebig A, et al. Complete genome sequence of DSM 30083 T, the type strain (U5/41 T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci. 2014;9:1–19.
doi: 10.1186/1944-3277-9-2
Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol MicroBiol. 2016;66:1100–3.
pubmed: 26585518
doi: 10.1099/ijsem.0.000760
Machado RA, Bruno P, Arce CC, Liechti N, Köhler A, Bernal J et al. Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminescens subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. International journal of systematic and evolutionary microbiology. 2019;69:652–61.
Machado RA, Muller A, Ghazal SM, Thanwisai A, Pagès S, Bode HB et al. Photorhabdus heterorhabditis subsp. aluminescens subsp. nov., Photorhabdus heterorhabditis subsp. heterorhabditis subsp. nov., Photorhabdus australis subsp. thailandensis subsp. nov., Photorhabdus australis subsp. australis subsp. nov., and Photorhabdus aegyptia sp. nov. isolated from Heterorhabditis entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology. 2021;71:004610.
Castaneda-Alvarez C, Machado RA, Morales-Montero P, Boss A, Muller A, Prodan S, et al. Photorhabdus antumapuensis sp. nov., a novel symbiotic bacterial species associated with Heterorhabditis atacamensis entomopathogenic nematodes. Int J Syst Evol MicroBiol. 2022;72:005525.
doi: 10.1099/ijsem.0.005525
Machado RA, Bhat AH, Castaneda-Alvarez C, Půža V, San-Blas E. Photorhabdus aballayi sp. nov. and Photorhabdus luminescens subsp. venezuelensis subsp. nov., isolated from Heterorhabditis amazonensis entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology. 2023;73:005872.
Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3.
pubmed: 26198102
pmcid: 4817141
doi: 10.1093/bioinformatics/btv421
Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641–50.
pubmed: 19377059
pmcid: 2693737
doi: 10.1093/molbev/msp077
Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun. 2019;10:2182.
pubmed: 31097708
pmcid: 6522516
doi: 10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res. 2022;50:D801–7.
pubmed: 34634793
doi: 10.1093/nar/gkab902
Riesco R, Trujillo ME. Update on the proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol MicroBiol. 2024;74:006300.
pubmed: 38512750
pmcid: 10963913
doi: 10.1099/ijsem.0.006300
Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol MicroBiol. 2014;64:316–24.
pubmed: 24505069
doi: 10.1099/ijs.0.054171-0
Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proceedings of the National Academy of Sciences. 2005;102:2567–72.
Emelianoff V, Le Brun N, Pages S, Stock SP, Tailliez P, Moulia C, et al. Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Hérault and Gard (Southern France). J Invertebr Pathol. 2008;98:211–7.
pubmed: 18353356
doi: 10.1016/j.jip.2008.01.006
Sajnaga E, Kazimierczak W, Skowronek M, Lis M, Skrzypek T, Waśko A. Steinernema poinari (Nematoda: Steinernematidae): a new symbiotic host of entomopathogenic bacteria Xenorhabdus bovienii. Arch Microbiol. 2018;200:1307–16.
pubmed: 29946739
pmcid: 6182613
doi: 10.1007/s00203-018-1544-9
Gorgadze O, Lortkhipanidze M, Ogier J-C, Tailliez P, Burjanadze M. Steinernema tbilisiensis sp. n. (Nematoda: Steinernematidae) — a new species of entomopathogenic nematode from Georgia. J Agricultural Sci Technol (JAST). 2015;264–76.
Fischer-Le Saux M, Arteaga-Hernandez E, Mracek Z, Boemare N. The bacterial symbiont Xenorhabdus poinarii (Enterobacteriaceae) is harbored by two phylogenetic related host nematodes: the entomopathogenic species Steinernema cubanum and Steinernema glaseri (Nematoda: Steinernematidae). FEMS Microbiol Ecol. 1999;29:149–57.
doi: 10.1111/j.1574-6941.1999.tb00606.x
Cimen H, Půža V, Nermuť J, Hatting J, Ramakuwela T, Hazir S. Steinernema biddulphi n. sp., a new Entomopathogenic Nematode (Nematoda: Steinernematidae) from South Africa. J Nematology. 2017;48:148–58.
doi: 10.21307/jofnem-2017-022
Fayyaz S, Yan X, Qiu L, Han R, Gulsher M, Khanum TA, et al. A new entomopathogenic nematode, Steinernema bifurcatum n. sp. (Rhabditida: Steinernematidae) from Punjab, Pakistan. Nematology. 2014;16:821–36.
doi: 10.1163/15685411-00002811
Půža V, Campos-Herrera R, Blanco-Pérez R, Jakubíková H, Vicente-Díez I, Nermuť J. Steinernema riojaense n. sp., a new entomopathogenic nematode (Nematoda: Steinernematidae) from Spain. Nematology. 2020;22:825–41.
doi: 10.1163/15685411-00003343
Godjo A, Afouda L, Baimey H, Decraemer W, Willems A. Molecular diversity of Photorhabdus and Xenorhabdus bacteria, symbionts of Heterorhabditis and Steinernema nematodes retrieved from soil in Benin. Archives of Microbiology. 2018;200:589–601.
Clausi M, Longo A, Rappazzo G, Tarasco E, Vinciguerra MT. Steinernema vulcanicum n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode species from Sicily (Italy). Nematology. 2011;13:409–23.
doi: 10.1163/138855410X526868
Bhat AH, Chaubey AK, Půža V. The first report of Xenorhabdus indica from Steinernema pakistanense: co-phylogenetic study suggests co-speciation between X. indica and its steinernematid nematodes. J Helminthol. 2019;93:81–90.
pubmed: 29338795
doi: 10.1017/S0022149X17001171
Patil J, Linga V, Mhatre PH, Gowda MT, Rangasamy V, Půža V. Steinernema indicum n. sp., a new entomopathogenic nematode (Nematoda: Steinernematidae) from India. Nematology. 2023;1:1–19.
Soni S, Patil J, Linga V, Mhatre P, Gowda M, Ganguli J, et al. Steinernema shori n. sp., a new entomopathogenic nematode (Nematoda: Steinernematidae) from India. J Helminthol. 2023;97:e72.
pubmed: 37681419
doi: 10.1017/S0022149X23000536
Dreyer J, Malan AP, Dicks LM. First report of a symbiotic relationship between Xenorhabdus griffiniae and an unknown Steinernema from South Africa. Arch Microbiol. 2018;200:349–53.
pubmed: 29170804
doi: 10.1007/s00203-017-1452-4
Ferreira T, Van Reenen C, Tailliez P, Pagès S, Malan A, Dicks L. First report of the symbiotic bacterium Xenorhabdus indica associated with the entomopathogenic nematode Steinernema yirgalemense. J Helminthol. 2016;90:108–12.
pubmed: 25119819
doi: 10.1017/S0022149X14000583
Cimen H, Půža V, Nermuť J, Hatting J, Ramakuwela T, Faktorova L, et al. Steinernema beitlechemi n. sp., a new entomopathogenic nematode (Nematoda: Steinernematidae) from South Africa. Nematology. 2016;18:439–53.
doi: 10.1163/15685411-00002968
Půža V, Nermut J, Mráček Z, Gengler S, Haukeland S. Steinernema pwaniensis n. sp., a new entomopathogenic nematode (Nematoda: Steinernematidae) from Tanzania. J Helminthol. 2017;91:20–34.
pubmed: 26765335
doi: 10.1017/S0022149X15001157
Kanga FN, Ivanova ES, Shepeleva NS, Spiridonov SE. Additional data on Steinernema cameroonense Ngo Kanga, Phap Quang Trinh, Wayenberge, Spiridonov, Hauser & Moens, 2012. Russian J Nematology. 2014;22:67–76.
Abate BA, Slippers B, Wingfield MJ, Malan AP, Hurley BP. Diversity of entomopathogenic nematodes and their symbiotic bacteria in South African plantations and indigenous forests. Nematology. 2018;20:355–71.
doi: 10.1163/15685411-00003144
Dreyer J, Malan AP, Dicks LM. Three novel Xenorhabdus–Steinernema associations and evidence of strains of X. khoisanae switching between different clades. Curr Microbiol. 2017;74:938–42.
pubmed: 28526895
doi: 10.1007/s00284-017-1266-2
Phan KL, Mráček Z, Půža V, Nermut J, Jarošová A. Steinernema huense sp. n., a new entomopathogenic nematode (Nematoda: Steinernematidae) from Vietnam. Nematology. 2014;16:761–75.
doi: 10.1163/15685411-00002806
Maneesakorn P, Grewal P, Chandrapatya A. Steinernema minutum sp. nov.(Rhabditida: Steinernematidae): a new entomopathogenic nematode from Thailand. Int J Nematology. 2010;20:27–42.
Kuwata R, Shigematsu M, Yoshiga T, Yoshida M, Kondo E. Phylogenetic analyses of Japanese steinernematid nematodes and their associating Xenorhabdus bacteria. Jpn J Nematol. 2006;36:75–85.
doi: 10.3725/jjn.36.75
Bhat AH, Chaubey AK, Puža V, San-Blas E. First report and comparative study of Steinernema surkhetense (Rhabditida: Steinernematidae) and its symbiont bacteria from subcontinental India. J Nematology. 2017;49:92–102.
doi: 10.21307/jofnem-2017-049
Londoño-Caicedo JM, Uribe-Londoño M, Buitrago-Bitar MA, Cortés AJ, Muñoz-Flórez JE. Molecular identification and Phylogenetic Diversity of Native Entomopathogenic Nematodes, and their bacterial endosymbionts, isolated from Banana and Plantain crops in Western Colombia. Agronomy. 2023;13:1373.
doi: 10.3390/agronomy13051373
Spiridonov SE, Waeyenberge L, Moens M. Steinernema Schliemanni sp. n. (Steinernematidae; Rhabditida) – a new species of steinernematids of the ‘monticolum’group from Europe. Russian J Nematology. 2010;18:175–90.
Machado RA, Bhat AH, Abolafia J, Shokoohi E, Fallet P, Turlings TC et al. Steinernema africanum n. sp. (Rhabditida, Steinernematidae), a new entomopathogenic nematode species isolated in the Republic of Rwanda. J Nematology. 2022;54.
Tarasco E, Santiago Alvarez C, Triggiani O, Quesada Moraga E. Laboratory studies on the competition for insect haemocoel between Beauveria bassiana and Steinernema ichnusae recovered in the same ecological niche. Biocontrol Sci Technol. 2011;21:693–704.
doi: 10.1080/09583157.2011.570428
Sugar DR, Murfin KE, Chaston JM, Andersen AW, Richards GR, deLéon L, et al. Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes. Environ Microbiol. 2012;14:924–39.
pubmed: 22151385
doi: 10.1111/j.1462-2920.2011.02663.x
Lee M-M, Stock SP. A multilocus approach to assessing co-evolutionary relationships between Steinernema spp.(Nematoda: Steinernematidae) and their bacterial symbionts Xenorhabdus spp.(γ-Proteobacteria: Enterobacteriaceae). Syst Parasitol. 2010;77:1–12.
pubmed: 20700692
doi: 10.1007/s11230-010-9256-9
Kazimierczak W, Sajnaga E, Skowronek M, Kreft AM, Skrzypek HW, Wiater A. Molecular and phenotypic characterization of Xenorhabdus bovienii symbiotically associated with Steinernema silvaticum. Arch Microbiol. 2016;198:995–1003.
pubmed: 27342112
doi: 10.1007/s00203-016-1261-1
Mamiya Y, Akiba M, Ekino T, Kanzaki N. Morphology, molecular profiles and distribution of Japanese populations of Steinernema tielingense Ma, Chen, Li, Han, Khatri-Chhetri, De Clercq & Moens, 2012 (Rhabditida: Steinernematidae). Nematology. 2021;23:909–28.
doi: 10.1163/15685411-bja10085
Shapiro-Ilan DI, Blackburn D, Duncan L, El-Borai FE, Koppenhöfer H, Tailliez P, et al. Characterization of biocontrol traits in Heterorhabditis floridensis: a species with broad temperature tolerance. J Nematology. 2014;46:336.
Orozco RA, Hill T, Stock SP. Characterization and phylogenetic relationships of Photorhabdus luminescens subsp. sonorensis (γ-Proteobacteria: Enterobacteriaceae), the bacterial symbiont of the entomopathogenic nematode Heterorhabditis sonorensis (Nematoda: Heterorhabditidae). Current microbiology. 2013;66:30–9.
Geldenhuys J, Malan A, Dicks L. First Report of the isolation of the Symbiotic Bacterium Photorhabdus luminescens subsp. laumondii Associated with Heterorhabditis safricana from South Africa. Curr Microbiol. 2016;73:790–5.
pubmed: 27567899
doi: 10.1007/s00284-016-1116-7
Machado RA, Somvanshi VS, Muller A, Kushwah J, Bhat CG. Photorhabdus hindustanensis sp. nov., Photorhabdus akhurstii subsp. akhurstii subsp. nov., and Photorhabdus akhurstii subsp. bharatensis subsp. nov., isolated from Heterorhabditis entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology. 2021;71:004998.
Page RD, Charleston MA. Trees within trees: phylogeny and historical associations. Trends Ecol Evol. 1998;13:356–9.
pubmed: 21238340
doi: 10.1016/S0169-5347(98)01438-4
Stock SP. Diversity, biology and evolutionary relationships. Nematode pathogenesis of insects and other pests: Ecology and applied technologies for sustainable plant and crop protection. Springer; 2015. pp. 3–27.
Lalramnghaki H, Vanlalhlimpuia, Vanramliana L. Characterization of a new isolate of entomopathogenic nematode, Steinernema sangi (Rhabditida, Steinernematidae), and its symbiotic bacteria Xenorhabdus vietnamensis (γ-Proteobacteria) from Mizoram, northeastern India. J Parasitic Dis. 2017;41:1123–31.
doi: 10.1007/s12639-017-0945-z
Maher AM, Asaiyah MA, Brophy C, Griffin CT. An entomopathogenic nematode extends its niche by associating with different symbionts. Microb Ecol. 2017;73:211–23.
pubmed: 27543560
doi: 10.1007/s00248-016-0829-2
Maneesakorn P, An R, Daneshvar H, Taylor K, Bai X, Adams BJ, et al. Phylogenetic and cophylogenetic relationships of entomopathogenic nematodes (Heterorhabditis: Rhabditida) and their symbiotic bacteria (Photorhabdus: Enterobacteriaceae. Mol Phylogenet Evol. 2011;59:271–80.
pubmed: 21335093
doi: 10.1016/j.ympev.2011.02.012
Funk DJ, Helbling L, Wernegreen JJ, Moran NA. Intraspecific phylogenetic congruence among multiple symbiont genomes. Proceedings of the Royal Society of London Series B: Biological Sciences. 2000;267:2517–21.
Wernegreen J, Riley M. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol Biol Evol. 1999;16:98–113.
pubmed: 10331255
doi: 10.1093/oxfordjournals.molbev.a026041
Peccoud J, Simon J-C, McLaughlin HJ, Moran NA. Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proceedings of the National Academy of Sciences. 2009;106:16315–20.
Liu L, Huang X, Zhang R, Jiang L, Qiao G. Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect–bacteria parallel evolution. Syst Entomol. 2013;38:81–92.
doi: 10.1111/j.1365-3113.2012.00647.x
Murfin K, Lee M, Klassen J, McDonald B, Larget B, Forst S et al. Xenorhabdus bovienii strain diversity impacts coevolution and symbiotic maintenance with. Steinernema spp. 2015;00076–15.