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Diversity of entomopathogenic bacteria associated with the white grub, Brahmina coriacea

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Abstract

A survey of potato fields located in the south-eastern region of Himachal Pradesh (India) was carried out in order to find out the natural pathogens infecting the white grub, Brahmina coriacea. About 88 % population of the infected grubs were found to exhibit symptoms of natural bacterial infection during the years 2007–2008. Hence, we attempted to isolate and characterize the most potent bacteria for the management of B. coriacea and tested their insecticidal activity. In this study, ten different bacterial isolates belonging to genera Bacillus, Psychrobacter, Paracoccus, Paenibacillus, Mycobacterium, Staphylococcus and Novosphingobium were isolated from B. coriacea. Bacterial species were identified based on morphology, biochemical tests and homologies of 16S rRNA gene sequences. Pathogenicity tests for all isolated bacteria at 1.0 × 108 cfu/ml of broth were performed on late first instar grubs. Among the bacteria tested, Bacillus cereus induced highest mortality level of 51.85 % within 7 days of treatment followed by Psychrobacter pulmonis (33.33 %), Bacillus psychrodurans (25.93 %), Bacillus pumilus (25.93 %), Paenibacillus tylopili (22.22 %) and Novosphingobium capsulatum (18.52 %). Mortality levels were further increased up to 100 % by B. cereus followed by 88.89 % by P. pulmonis after 30 days of treatment. Our results indicate that B. cereus, P. pulmonis, B. psychrodurans, B. pumilus, P. tylopili and N. capsulatum may be valuable biological control agents for white grubs, B. coriacea.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Google Scholar 

  • Abd El-Rahman HA, Fritze D, Sproer C, Claus D (2002) Two novel psychrotolerant species, Bacillus psychrotolerans sp. nov. and Bacillus psychrodurans sp. nov., which contain ornithine in their cell walls. Int J Syst Evol Microbiol 52:2127–2133

    Article  PubMed  Google Scholar 

  • Abi Khattar Z, Rejasse A, Destoumieux GD, Scoubas JM, Sanchis V, Lereclus DA, Givaudan M, Kallassy C, Nielsen L, Gaudriault S (2009) The dlt operon of Bacillus cereus is required for resistance to cationic antimicrobial peptides and for virulence in insects. J Bacteriol 191(22):7063–7073

    Article  PubMed  CAS  Google Scholar 

  • Adekambi T, Reynaud-Gaubert M, Greub G, Gevaudan MJ, La Scola B, Raoult D, Drancourt M (2004) Amoebal coculture of Mycobacterium massiliense sp. nov. from the sputum of a patient with hemoptoic pneumonia. J Clin Microbiol 42:5493–5501

    Article  PubMed  CAS  Google Scholar 

  • Alm S, Villani M, Yeh T, Shutter R (1997) Bacillus thuringiensis serovar japonensis strain Buibui for control of Japanese and Oriental beetle larvae (Coleoptera: Scarabaeidae). Appl Entomol Zool 32:477–484

    Google Scholar 

  • Bahar AA, Demirbag Z (2007) Isolation of pathogenic bacteria from Oberea linearis (Coleptera: Cerambycidae). Biologia 62:13–18

    Article  CAS  Google Scholar 

  • Bentur HN, Dalzell AM, Riordan FAI (2007) Central venous catheter infection with Bacillus pumilus in an immunocompetent child: a case report. Ann Clin Microbiol Antimicrob 6:12

    Article  PubMed  CAS  Google Scholar 

  • Bottone EJ, Peluso RW (2003) Production by Bacillus pumilus (MSH) of an antifungal compound that is active against Mucoraceae and Aspergillus species: preliminary report. J Med Microbiol 52:69–74

    Article  PubMed  CAS  Google Scholar 

  • Bowman JP, Cavanagh J, Austin JJ, Sanderson K (1996) Novel Psychrobacter species from Antarctic ornithogenic soils. Int J Syst Bacteriol 46:841–848

    Article  PubMed  CAS  Google Scholar 

  • Broderick NA, Goodman RM, Raffa KF, Handelsman JO (2000) Synergy between zwittermicin A and Bacillus thuringiensis subsp. kurstaki against gypsy moth (Lepidoptera: Lymantridae). Environ Entomol 29:101–107

    Article  CAS  Google Scholar 

  • Cano RJ, Borucki MK, Higby-Schweitzer M, Poinar HN, George O, Poinar JR, Kerri JP (1994) Bacillus DNA in fossil bees: an ancient symbiosis? Appl Environ Microbiol 60:2164–2167

    PubMed  CAS  Google Scholar 

  • Chandel RS, Chander R, Gupta PR (1993) Toxicity of some soil insecticides to immature stages of Brahmina coriacea (Hope). J Soil Biol Ecol 13(2):103–107

    Google Scholar 

  • Chandla VK, Raj D, Sharma A, Garg ID, Verma KD, Raman R (2001) Serious attack of white grub in potato fields at Shimla. J Indian Potato Assoc 28(1):125–126

    Google Scholar 

  • Chiba M, Kono M, Hoshina S, Komatsu M, Kitagawa Y, Iizuka M, Watanabe S (2000) Presence of bacterial 16S ribosomal RNA gene segments in human intestinal lymph follicles. Scand J Gastroenterol 35:824–831

    PubMed  CAS  Google Scholar 

  • Coppel CH, Martins JW (1977) Biological insect pest suppression. Springer, Berlin

    Book  Google Scholar 

  • Davidson EW, Rosell RC, Hendrix DL (2000) Culturable bacteria associated with the whitefly, Bemisia argentifolii (Homoptera: Aleyrodidae). Florida Entomol 83:159–171

    Article  Google Scholar 

  • Demir I, Sezen K, Demirbag Z (2002) The first study on bacterial flora and biological control agent of Anoplus roboris (Sufr., Coleoptera). J Microbiol 40:104–108

    Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Erturk O, Yaman M, Irfan A (2008) Effects of four Bacillus spp. of soil origin on the Colorado potato beetle Leptinotarsa decemlineata (Say). Entomol Res 38:135–138

    Article  Google Scholar 

  • Euzeby JP (2007) List of bacterial names with standing in nomenclature. Society for systematic and veterinary bacteriology, Toulouse, France. http://www.bacterio.cict.fr/m/mycobacterium.html. Accessed 4 Oct 2011

  • Ezekiel R, Sukumaran NP, Shekhawat GS (1999) Potato: a wholesome food. In: Technical Bulletin, vol 49. Central Potato Research Institute, Shimla, p 132

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • French JRJ, Robinson PJ, Minko G, Pahl P (1984) Response of the European elm bark beetle, Scolytus multistriatus, to host bacterial isolates. J Chem Ecol 10:1133–1149

    Article  Google Scholar 

  • Fuxa JR, Kunimi Y, Nakai M (1997) Research methods for microorganisms interacting with arthropods in soil. In: Hurst CJ, Kundsen GR, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology, vol 2. ASM Press, Washington, DC, p 894

    Google Scholar 

  • Groudieva T, Grote R, Antranikian G (2003) Psychromonas arctica sp. nov., a novel psychrotolerant, biofilm-forming bacterium isolated from Spitzbergen. Int J Syst Evol Microbiol 53:539–545

    Article  PubMed  CAS  Google Scholar 

  • Guttigoli A, Zaman MM (2000) Bacteremia and possible endocarditis caused by Moraxella phenylpyruvica. South Med J 93:708–709

    PubMed  CAS  Google Scholar 

  • Handelsman J, Raffel J, Mester EH, Wunderlich L, Grau CR (1996) Biological control of damping off of alfalfa seedlings with Bacillus cereus UW 85. Appl Environ Microbiol 56:713–718

    Google Scholar 

  • Harke M, Hirschberg J, Oren A (1998) Paracoccus marcusii sp. nov., an orange Gram-negative coccus. Int J Syst Evol Microbiol 48:543–548

    Google Scholar 

  • Heuchert A, Glockner FO, Amann R, Fischer U (2004) Psychrobacter nivimaris sp. nov., a heterotrophic bacterium attached to organic particles isolated from the South Atlantic (Antarctica). Syst Appl Microbiol 27:399–406

    Article  PubMed  CAS  Google Scholar 

  • Hori H, Suzuki N, Ogiwara K, Himejima M, Indrasith LS, Minami S, Sato R, Ohba M, Iwahana H (1994) Characterization of larvicidal toxin protein from Bacillus thuringiensis serovar Japonensis strain Buibui specific for scarabaeidae beetles. J Appl Bacteriol 76:307–313

    Article  PubMed  CAS  Google Scholar 

  • Hurst MR, Glare TR, Jackson TA, Ronson C (2000) Plasmid located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J Bacteriol 182:5127–5138

    Article  PubMed  CAS  Google Scholar 

  • Jackson TA, Saville DJ (2000) Bioassays of replicating bacteria against soil-dwelling pests. In: Navon A, Ascher KRS (eds) Bioassays of entomopathogenic microbes and nematodes. CABI, Wallingford, pp 73–94

    Chapter  Google Scholar 

  • Jackson TA, Pearson JF, O’Callaghan MO, Mahanty HK, Willocks MJ (1992) Pathogen to product-development of Serratia entomophila (Enterobacteriaceae) as a commercial biological control agent for the New Zealand grass grub (Costelytra zealandica). In: Jackson TA, Glare TR (eds) Use of pathogens in scarab pest management. Intercept, Andover, pp 191–198

    Google Scholar 

  • Joo GJ, Kim YM, Lee IJ, Song KS, Rhee IK (2004) Growth promotion of red pepper plug seedlings and the production of gibberellins by Bacillus cereus, Bacillus macroides and Bacillus pumilus. Biotechnol Lett 26:487–491

    Article  PubMed  CAS  Google Scholar 

  • Juni E (2005) Genus Psychrobacter, Juni and Heym 1986, 389VP. In: Boone DR, Brenner DJ, Castenholz RW, Garrity GM, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, Part A, vol 2, 2nd edn. Springer, New York, pp 437–441

    Google Scholar 

  • Kawamura Y, Hou XG, Ferdousi S, Hirose K, Miyake M, Shu SE, Ezaki T (1998) Distribution of Staphylococcus species among human clinical specimens and emended description of Staphylococcus caprae. J Clin Microbiol 36(7):2038–2042

    PubMed  CAS  Google Scholar 

  • Kim HY, Yun YJ, Park CG, Lee DH, Cho YK, Park BJ, Joo SI, Kim EC, Hur YJ, Kim BJ, Kook YH (2007) Outbreak of Mycobacterium massiliense infection associated with intramuscular injections. J Clin Microbiol 45:3127–3130

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kocur M (1984) Genus Paracoccus, Davis 1969, 384AL. In: Krig NR, Hold JG (eds) Bergey’s manual of systematic bacteriology, Section-4, vol 1. Williams & Wilkins, Baltimore, pp 399–402

  • Koppenhofer AM, Wilson M, Brown I, Kaya HK, Gaugler R (2000) Biological control agents for white grubs (Coleoptera: Scarabaeidae) in anticipation of the establishment of the Japanese beetle in California. J Econ Entomol 93:71–80

    Article  PubMed  CAS  Google Scholar 

  • Kuisiene N, Raugalas J, Sproer C, Kroppenstedt RM, Stuknyte M, Chitavichius D (2008) Paenibacillus tylopili sp. nov., a chitinolytic bacterium isolated from the mycorhizosphere of Tylopilus felleus. Folia Microbiol 53(3):433–437

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lacey LA, Unruh TR, Simkins H, Thomsen-Archer K (2007) Gut bacteria associated with the pacific coast wireworm, Limonius canus, inferred from 16S rDNA sequences and their Implications for Control. Phytoparasitica 35(5):479–489

    Article  Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959

    Article  PubMed  CAS  Google Scholar 

  • Leao SC, Tortoli E, Viana-Niero C, Ueki SYM, Lima KVB, Lopes ML, Yubero JM, Maria C, Garcia MJ (2009) Characterization of mycobacteria from a major Brazilian outbreak suggests that revision of the taxonomic status of members of the Mycobacterium chelonae-M. abscessus group is needed. J Clin Microbiol 47(9):2691–2698

    Article  PubMed  CAS  Google Scholar 

  • Link L, Sawyer J, Venkateswaran K, Nicholson W (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47:159–163

    Article  PubMed  CAS  Google Scholar 

  • Logan AN, De Vos P (2009) Genus Bacillus Cohn De Vos 1872, 174AL. In: De Vos P, Garrity GM, Krieg NR, Ludwid W, Rainey FA, Schleifer KH, Whileman WB (eds) Bergey’s manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, pp 21–128

    Google Scholar 

  • Lysenko O (1972a) Pathogenicity of Bacillus cereus for insects. I. Production of phospholipase C. Folia Microbiol 17:221–227

    Article  CAS  Google Scholar 

  • Lysenko O (1972b) Pathogenicity of Bacillus cereus for insects. II. Toxicity of phospholipase C for Galleria mellonella. Folia Microbiol 17:228–231

    Article  CAS  Google Scholar 

  • Mashtoly TA, EL-Zemaity MS, Hussien MI, Alm SR (2009) LC and LD50 values of Bacillus thuringiensis Serovar japonensis strain buibui toxin to oriental beetle and northern masked chafer larvae (Coleoptera: Scarabaeidae). J Econ Entomol 102(5):1891–1895

    Article  PubMed  CAS  Google Scholar 

  • Misra SS, Chandel RS (2003) Potato white grubs in India. In: Technical Bulletin, vol 60. Central Potato Research Institute, Shimla, p 8

  • Muratoglu H, Kati H, Demirbag Z, Sezen K (2009) High insecticidal activity of Leclercia adecarboxylata isolated from Leptinotarsa decemlineata (Col.: Chrysomelidae). Afr J Biotechnol 8(24):7115

    Google Scholar 

  • Needham AJ, Kibart M, Crossley H, Ingham PW, Foster SJ (2004) Drosophila melanogaster as a model host for Staphylococcus aureus infection. Microbiology 150:2347–2355

    Article  PubMed  CAS  Google Scholar 

  • Nelson A, Hultenby K, Hell E, Riedel HM, Brismar H, Flock JI, Lundahl J, Giske CG, Marchini G (2009) Staphylococcus epidermidis isolated from newborn infants express pilus-like structures and are inhibited by the cathelicidin-derived antimicrobial peptide LL37. Pediatr Res 66(2):174–178

    Article  PubMed  CAS  Google Scholar 

  • Nishiwaki H, Ito K, Otsuki K, Yamamoto H, Komai K (2004) Purification and functional characterization of insecticidal sphingomyelinase C produced by Bacillus cereus. Eur J Biochem 271:601–606

    Article  PubMed  CAS  Google Scholar 

  • Olayide AJ, Bamidele AA (2008) Transmission of bacterial isolates through all the developmental stages of dog ticks (bacteriological evidence). J Anim Vet Adv 7(8):959–962

    Google Scholar 

  • Priest FG (2009) Genus Paenibacillus Ash Priest & Collins, 1994, 852VL. In: De Vos P, Garrity GM, Krieg NR, Ludwid W, Rainey FA, Schleifer KH, Whileman WB (eds) Bergey’s manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, pp 269–295

    Google Scholar 

  • Ray JL, Helga KA, Sandra Y, Nielsen KM, O’Callaghan M (2007) An assessment of the potential of herbivorous insect gut bacteria to develop competence for natural transformation. Environ Biosafety Res 6:135–147

    Article  PubMed  CAS  Google Scholar 

  • Roth RR, James WD (1988) Microbial ecology of the skin. Annu Rev Microbiol 42:441–464

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Schleifer KH, Bell JH (2009) Genus Staphylococcus, Rosenberg 1884, 18L. In: De Vos P, Garrity GM, Krieg NR, Ludwid W, Rainey FA, Schleifer KH, Whileman WB (eds) Bergey’s manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, pp 392–421

    Google Scholar 

  • Selvakumar G, Sushil SN, Bhatt JC, Singh RD (2003) Isolation of Yersinia sp. from diseased white grub larvae. Indian. J Microbiol 43(3):211–212

    Google Scholar 

  • Selvakumar G, Mohan M, Sushil SN, Kundu S, Bhatt JC, Gupta HS (2007) Characterization and phylogenetic analysis of an entomopathogenic Bacillus cereus strain WGPSB-2 (MTCC 7182) isolated from white grub Anomala dimidiata (Coleoptera: Scarabaeidae). Biocontrol Sci Technol 17:525–534

    Article  Google Scholar 

  • Sevim A, Demirbag Z, Demir I (2010) New study on the bacteria of Agrotis segetum Schiff. (Lepidoptera: Noctuidae) and their insecticidal activities. Turk J Agric For 34. doi:10.3906/tar-0902-9

  • Sezen K, Demir I, Kati H, Demirbag Z (2005) Investigations on bacteria as a potential biological control agent of summer chafer, Amphimallon solstitiale L. (Coleoptera: Scarabaeidae). J Microbiol 43:463–468

    PubMed  CAS  Google Scholar 

  • Simmon KE, Pounder JI, Greene JN, Walsh F, Anderson CM, Cohen S, Petti CA (2007) Identification of an emerging pathogen, Mycobacterium massiliense, by rpoB sequencing of clinical isolates collected in the United States. J Clin Microbiol 45:1978–1980

    Article  PubMed  CAS  Google Scholar 

  • Sushil SN, Mohan M, Selvakumar G, Bhatt JC, Gupta HS (2008) Isolation and toxicity evaluation of bacterial entomopathogens against phytophagous white grubs (Coleoptera: Scarabaeidae) in Indian Himalayan hills. Int J Pest Manag 54(4):301–307

    Article  CAS  Google Scholar 

  • Suzuki N, Hori H, Ogiwara K, Asano S, Sato R, Ohba M, Iwahana H (1992) Insecticidal spectrum of a novel isolate of Bacillus thuringiensis serovar Japonensis. Biol Control 2:136–142

    Article  Google Scholar 

  • Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417

    PubMed  CAS  Google Scholar 

  • Tan B, Jackson TA, Hurst MR (2006) Virulen1ce of Serratia strains against Costelytra zealandica. Appl Environ Microbiol 72:6417–6418

    Article  PubMed  CAS  Google Scholar 

  • Thiery I, Frachon E (1997) Identification, isolation, culture and preservation of entomopathogenic bacteria. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, London, pp 55–77

  • Travers RS, Martin AWP, Reichelderfer CF (1987) Selective process for efficient isolation of soil Bacillus spp. Appl Environ Microbiol 53:1263–1266

    PubMed  CAS  Google Scholar 

  • US Environmental Protection Agency Office of Pesticide Programs (2004) Biopesticides registration action document, Bacillus pumilus strain QST 2808 (PC Code 006485)

  • Valiente MC, Thioulouse J, Chauve C, Normand P, Zenner L (2009) Bacterial taxa associated with the hematophagous mite Dermanyssus gallinae detected by 16S rRNA PCR amplification and TTGE fingerprinting. Res Microbiol 160:63–70

    Article  Google Scholar 

  • Wayne LG, Kubica GP (1986) Genus Mycobacterium Lehman & Neuman 1896, 363AL. In: Peter HA, Mair NS, Sharpe ME, Hold JG (eds) Bergey’s manual of systematic bacteriology, vol 2, Section-16. Williams & Wilkins, Baltimore, pp 1436–1457

  • Yabuuchi E, Kosako Y (2005) Genus Novosphingobium Yabuuchi, Yanno, Oaizu, Hashimoto, Ezaki, Yamamoto 1990, 321VP. In: Boone DR, Castenholz RW, Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s Manual of systematic Bacteriology, Part C, vol 2, 2nd edn. Springer, New York, pp 234–258

    Chapter  Google Scholar 

  • Yaman M, Erturk O, Aslan I (2010) Isolation of some pathogenic bacteria from the great spruce bark beetle, Dendroctonus micansand its specific predator Rhizophagus grandis. Folia Microbiol 55(1):35–38

    Article  CAS  Google Scholar 

  • Yilmaz H, Sezen K, Katil H, Demirbag Z (2006) The first study on the bacterial flora of the European spruce bark beetle, Dendroctonus micans (Coleoptera: Scolytidae). Biologia (Bratisl) 61(6):679–686

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

    Article  PubMed  CAS  Google Scholar 

  • Zouache K, Tran-Van V, Voronin D, Mavingui P (2009) Composition of bacterial communities associated with natural and laboratory populations of Asobara tabida infected with Wolbachia. Appl Environ Microbiol 75(11):3755–3764

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Indian Council of Agricultural Research, New Delhi, for funding this project. A.S. gratefully acknowledges the Senior Research Fellowship awarded by the Indian Council of Agricultural Research.

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Sharma, A., Thakur, D.R., Kanwar, S. et al. Diversity of entomopathogenic bacteria associated with the white grub, Brahmina coriacea . J Pest Sci 86, 261–273 (2013). https://doi.org/10.1007/s10340-012-0459-5

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