Providencia entomophila sp. nov., a new bacterial species associated with major olive pests in Tunisia

Autoři: Ines Ksentini aff001;  Houda Gharsallah aff001;  Maryam Sahnoun aff001;  Christina Schuster aff002;  Sirine Hamli Amri aff001;  Rim Gargouri aff001;  Mohamed Ali Triki aff001;  Mohieddine Ksantini aff001;  Andreas Leclerque aff002
Působiště autorů: Tunisian Olive Institute, University of Sfax, Sfax, Tunisia aff001;  Institute for Microbiology and Biochemistry, Hochschule Geisenheim University, Geisenheim, Germany aff002;  Institute for Sustainable Plant Protection (IPSP), National Research Council (CNR), Portici, Italy aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Bioprospection for potential microbial biocontrol agents associated with three major insect pests of economic relevance for olive cultivation in the Mediterranean area, namely the olive fly, Bactrocera oleae, the olive moth, Prays oleae, and the olive psyllid, Euphyllura olivina, led to the isolation of several strains of readily cultivable Gram-negative, rod-shaped bacteria from Tunisian olive orchards. Determination of 16S ribosomal RNA encoding sequences identified the bacteria as members of the taxonomic genus Providencia (Enterobacterales; Morganellaceae). A more detailed molecular taxonomic analysis based on a previously established set of protein-encoding marker genes together with DNA-DNA hybridization and metabolic profiling studies led to the conclusion that the new isolates should be organized in a new species within this genus. With reference to their original insect association, the designation “Providencia entomophila” is proposed here for this hypothetical new taxon.

Klíčová slova:

Death rates – Olive trees – Phylogenetic analysis – Phylogenetics – Ribosomal RNA – Sequence databases – Sequence similarity searching – Insect pests


1. Chermiti B. Approche d’évaluation de la nocivité du psylle de l’Olivier Euphllura olivina (Costa) (Homoptera. Aphalaridae). Olivae 1992;43: 34–42.

2. Hiskia AE, Atmajidou ME, Tsipi DF. Determination of Organophosphorus Pesticide Residues in Greek Virgin Olive Oil by Capillary Gas Chromatographie. J Agric Food Chem. 1998;46: 570−574. doi: 10.1021/jf970427y 10554279

3. Bajwa U, Sandhu KS. Effect of handling and processing on pesticide residues in food—a review. J Food Sci Technol. 2014;51: 201–220. doi: 10.1007/s13197-011-0499-5 24493878

4. Gharsallah H, Ksentini I, Abdelhedi N, Naayma S, Hadj Taieb K, Sahnoun M, et al. Screening of bacterial isolates related to olive orchard pests in Tunisia and evaluation of their biotechnological potential. J Appl Microbiol. 2018;126: 489–502. doi: 10.1111/jam.14159 30451348

5. Adeolu M, Alnajar S, Naushad S, Gupta R. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov.. Int J Syst Evol Microbiol. 2016;66: 5575–5599. doi: 10.1099/ijsem.0.001485 27620848

6. Penner JL, Hennessy JN. Application of O-serotyping in a study of Providencia rettgeri (Proteus rettgeri) isolated from human and nonhuman sources. J Clin Microbiol. 1979;10: 834–840. 521481

7. Hickman-Brenner FW, Farmer JJ III, Steigerwalt AG, Brenner DJ. Providencia rustigianii: a new species in the family Enterobacteriaceae formerly known as Providencia alcalifaciens biogroup 3. J Clin Microbiol. 1983;17: 1057–1060. 6874899

8. Müller HE, O’Hara CM, Fanning GR, Hickman-Brenner FW, Swenson JM, Brenner DJ. Providencia heimbachae,a new species of Enterobacteriaceae isolated from animals. Int J Syst Bacteriol. 1986;36: 252–256.

9. Yoh M, Matsuyama J, Ohnishi M, Takagi K, Miyagi H, Mori K, et al. Importance of Providencia species as a major cause of travellers’ diarrhoea. J Med Microbiol. 2005;54: 1077–1108. doi: 10.1099/jmm.0.45846-0 16192440

10. Somvanshi VS, Lang E, Sträubler B, Spröer C, Schumann P, Ganguly S, et al. Providencia vermicola sp. nov., isolated from infective juveniles of the entomopathogenic nematode Steinernema thermophilum. Int J Syst Evol Microbiol. 2006;56: 629–633. doi: 10.1099/ijs.0.63973-0 16514040

11. Juneja P, Lazzaro BP. Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. Int J Syst Evol Microbiol. 2009;59: 1108–1111. doi: 10.1099/ijs.0.000117-0 19406801

12. Khunthongpan S, Sumpavapol P, Tanasupawat S, Benjakul S, H-Kittikun A. Providencia thailandensis sp. nov., isolated from seafood processing wastewater. J Gen Appl Microbiol. 2013;59: 185–190. 23863288

13. Hu Y, Feng Y, Zhang X, Zong Z. Providencia huaxiensis sp. nov., recovered from a human rectal swab. Int J Syst Evol Microbiol. 2019;69: 2638–2643. doi: 10.1099/ijsem.0.003502 31162027

14. O’Hara CM, Brenner FW, Miller JM. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev. 2000;13: 534–546. doi: 10.1128/cmr.13.4.534-546.2000 11023955

15. Kuzina LV, Peloquin JJ, Vacek DC, Miller TA. Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Curr Microbiol. 2001;42: 290–294. 11178731

16. Msaad Guerfali M, Djobbi W, Charaabi K, Hamden H, Fadhl S, Marzouki W, et al. Evaluation of Providencia rettgeri pathogenicity against laboratory Mediterranean fruit fly strain (Ceratitis capitata). PLoS One 2018;13: e0196343. doi: 10.1371/journal.pone.0196343 29734397

17. Galac MR, Lazzaro BP. Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes Infect. 2011;13: 673–683. doi: 10.1016/j.micinf.2011.02.005 21354324

18. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA 6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

19. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25: 3389–3402. doi: 10.1093/nar/25.17.3389 9254694

20. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol. 2000;7: 203–214. doi: 10.1089/10665270050081478 10890397

21. Thompson JD, Higgins DG, Gibson TJ. ClustalW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 7984417

22. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. Tree-Puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002;18: 502–504. doi: 10.1093/bioinformatics/18.3.502 11934758

23. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52: 696–704. doi: 10.1080/10635150390235520 14530136

24. Hasegawa M, Kishino H, Yano TA. Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22: 160–174. doi: 10.1007/bf02101694 3934395

25. Yang Z. Maximum-Likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol Biol Evol. 1993;10: 1396–1401. doi: 10.1093/oxfordjournals.molbev.a040082 8277861

26. Cashion P, Hodler-Franklin MA, McCully J, Franklin M. A rapid method for base ratio determination of bacterial DNA. Anal Biochem. 1977;81: 461–466. doi: 10.1016/0003-2697(77)90720-5 907108

27. De Ley J, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem. 1970;12: 133–142. doi: 10.1111/j.1432-1033.1970.tb00830.x 4984993

28. Huss VAR, Festl H, Schleifer KH. Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol. 1983;4: 184–192. doi: 10.1016/S0723-2020(83)80048-4 23194591

29. Yi YK, Park HW, Shrestha S, Seo J, Kim YO, Shin CS, et al. Identification of two entomopathogenic bacteria from a nematode pathogenic to the Oriental beetle, Blitopertha orientalis. J Microbiol Biotechnol. 2007;17: 968–978. 18050915

30. Park HW, Kim YO, Ha JS, Youn SH, Kim HH, Bilgrami AL, et al. Effects of associated bacteria on the pathogenicity and reproduction of the insect-parasitic nematode Rhabditis blumi (Nematoda: Rhabditida). Can J Microbiol. 2011;57: 750–758. doi: 10.1139/w11-067 21867444

31. Marquez-Ortiz RA, Haggerty L, Sim EM, Duarte C, Castro-Cardozo BE, Beltran M, et al. First complete Providencia rettgeri genome sequence, the NDM-1-producing clinical strain RB151. Genome Announc. 2017;5: e01472–16. doi: 10.1128/genomeA.01472-16 28104655

32. Olaitan AO, Diene SM, Assous MV, Rolain JM. Genomic Plasticity of Multidrug-Resistant NDM-1 Positive Clinical Isolate of Providencia rettgeri. Genome Biol Evol. 2016;8: 723–728. doi: 10.1093/gbe/evv195 27386606

33. Pereira PS, Albano RM, Asensi MD, Carvalho-Assef AP. Draft genome sequences of three NDM-1-producing Enterobacteriaceae species isolated from Brazil. Mem Inst Oswaldo Cruz. 2015;110: 580–582. doi: 10.1590/0074-02760150081 26061151

34. Farmer JJ III, Davis BR, Hickman-Brenner FW, McWhorter A, Huntley-Carter GP, Asbury MA, et al. Biochemical identification of new species and biogroups of Enterobacteriaceae isolated from clinical specimens. J Clin Microbiol. 1985;21: 46–76. 3881471

35. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, et al. International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol. 1987;37: 463–464.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden