Pyrosequencing reveals the predominance of Pseudomonadaceae in gut microbiome of a gall midge

Pathogens

Volumn 3, Issue 2, 2014, Pages 459-472

  Bansal, Raman ^a   Hulbert, Scot H ^b   Reese, John C ^a   Whitworth, Robert J ^a   Stuart, Jeffrey J ^c   Chen, Ming Shun ^a,d  

^a KANSAS STATE UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c Purdue University ^*  (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Gut; Hessian fly; Mayetiola destructor; Microbe; Symbiosis

Indexed keywords

DNA 16S; RNA 16S;

ACHROMOBACTER; ACIDOBACTERIA; ACTINOBACTERIA; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BACTEROIDETES; BUTTIAUXELLA; CHEMOTAXONOMY; DIPTERA; DNA EXTRACTION; DNA TEMPLATE; ENTEROBACTERIACEAE; FEMALE; GENE SEQUENCE; HESSIAN FLY; INFESTATION; LARVA; MICROBIAL POPULATION DYNAMICS; MICROBIOME; NONHUMAN; PHYLOGENETIC TREE; PLANT INSECT INTERACTION; POLYMERASE CHAIN REACTION; PROTEOBACTERIA; PSEUDOMONADACEAE; PSEUDOMONAS; PYROSEQUENCING; SEQUENCE ANALYSIS; UNDIBACTERIUM; XANTHOMONADACEAE;

EID: 84924754974     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens3020459     Document Type: Article

References (51)

1. Dillon, R.; Dillon, V. The gut bacteria of insects: nonpathogenic interactions. Annual Reviews in Entomology 2004, 49, 71-92.
2. Engel, P.; Moran, N.A. The gut microbiota of insects-diversity in structure and function. FEMS Microbiol. Rev. 2013, 37, 699-735.
3. Holmes, E.; Nicholson, J. Variation in gut microbiota strogly influences individual rodent phenotypes. Toxicological Sciences 2005, 87, 1-2.
4. Chapman, R.F. The Insects: Structure And Function; Cambridge University press: Cambridge, UK, 1998.
5. Buchner, P. Endosymbiosis of Animals with Plant Microorganims; John Wiley & Sons: Chichester, UK, 1965.
6. Hansen, A.K.; Moran, N.A. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol. Ecol. 2013, 23, 1473-1496.
7. Gagne, R.; Hatchett, J. Instars of the Hessian fly (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 1989, 82, 73-79.
8. Ananthakrishnan, T.N. Biology of gall insects; Oxford and IBH: New Delhi, India, 1984.
9. Pauly, P.J. Fighting the Hessian fly: American and British responses to insect invasion 1776-1789. Environ. Hist. 2002, 7, 485-507.
10. Harris, M.; Stuart, J.; Mohan, M.; Nair, S.; Lamb, R.; Rohfritsch, O. Grasses and gall midges: plant defense and insect adaptation. Annu. Rev. Entomol. 2003, 48, 549-577.
11. Harris, M.; Freeman, T.; Rohfritsch, O.; Anderson, K.; Payne, S.; Moore, J. Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Ann. Entomol. Soc. Am. 2006, 99, 305-316.
12. Boosalis, G. Hessian fly in relation to the development of crown and basal stem rot of wheat. Phytopathology 1954, 44, 224-229.
13. Mittapalli, O.; Shukle, R.H.; Sardesai, N.; Giovanini, M.P.; Williams, C.E. Expression patterns of antibacterial genes in the Hessian fly. J. Insect Physiol. 2006, 52, 1143-1152.
14. Bansal, R. Hessian Fly Associated Microbes: Dynamics, Transmission And Essentiality; ProQuest, UMI Dissertation Publishing: Ann Arbor, MI, USA, 2010.
15. Bansal, R.; Hulbert, S.; Schemerhorn, B.; Reese, J.C.; Whitworth, R.J.; Stuart, J.J.; Chen, M. Hessian fly-associated bacteria: transmission, essentiality, and composition. PloS One 2011, 6, e23170.
16. Warnecke, F.; Luginbühl, P.; Ivanova, N.; Ghassemian, M.; Richardson, T.H.; Stege, J.T.; Cayouette, M.; McHardy, A.C.; Djordjevic, G.; Aboushadi, N. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450, 560-565.
17. Cox-Foster, D.L.; Conlan, S.; Holmes, E.C.; Palacios, G.; Evans, J.D.; Moran, N.A.; Quan, P.; Briese, T.; Hornig, M.; Geiser, D.M. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007, 318, 283-287.
18. Moran, N.A.; Hansen, A.K.; Powell, J.E.; Sabree, Z.L. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 2012, 7, e36393.
19. Neefs, J.; Van de Peer, Y.; De Rijk, P.; Goris, A.; De Wachter, R. Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 1991, 19, 1987-2015.
20. Fox, G.E.; Stackebrandt, E.; Hespell, R.B.; Gibson, J.; Maniloff, J.; Dyer, T.A.; Wolfe, R.S.; Balch, W.E.; Tanner, R.S.; Magrum, L.J. et al. The phylogeny of prokaryotes. Science 1980, 209, 457-463.
21. Huse, S.M.; Dethlefsen, L.; Huber, J.A.; Welch, D.M.; Relman, D.A.; Sogin, M.L. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS genetics 2008, 4, e1000255.
22. Schloss, P.D.; Westcott, S.L.; Ryabin, T.; Hall, J.R.; Hartmann, M.; Hollister, E.B.; Lesniewski, R.A.; Oakley, B.B.; Parks, D.H.; Robinson, C.J. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75, 7537-7541.
23. Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512-526.
24. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731-2739.
25. Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39, 783-791.
26. Byers, R.A.; Gallun, R.L. Ability of the Hessian fly to stunt winter wheat: effect of larval feeding on elongation of leaves. J. Econ. Entomol. 1972, 65, 955-958.
27. Rohfritsch, O. Patterns in gall development. In Biology of insect-induced galls; Shorthouse, J.D., Rohfritsch, O., Eds.; Oxford University Press: Oxford, UK, 1992; pp. 60-86.
28. Prabhakar, C.S.; Sood, P.; Kanwar, S.S.; Sharma, P.N.; Kumar, A.; Mehta, P.K. Isolation and characterization of gut bacteria of fruit fly, Bactrocera tau (Walker). Phytoparasitica 2013, 41, 193-201.
29. Jing, X.; Wong, A.C.; Chaston, J.M.; Colvin, J.; McKenzie, C.L.; Douglas, A.E. The bacterial communities in plant phloem-sap-feeding insects. Mol. Ecol. 2014, 23, 1433-1444.
30. Wei, T.; Ishida, R.; Miyanaga, K.; Tanji, Y. Seasonal variations in bacterial communities and antibiotic-resistant strains associated with green bottle flies (Diptera: Calliphoridae). Appl. Microbiol. Biotechnol. 2014, 98, 4197-4208.
31. Broderick, N.A.; Robinson, C.J.; McMahon, M.D.; Holt, J.; Handelsman, J.; Raffa, K.F. Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biology 2009, 7, 11.
32. Stavrinides, J.; McCloskey, J.K.; Ochman, H. Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl. Environ. Microbiol. 2009, 75, 2230-2235.
33. Zhang, F.; Huang, Y.H.; Liu, S.Z.; Zhang, L.; Li, B.T.; Zhao, X.X.; Fu, Y.; Liu, J.J.; Zhang, X.X. Pseudomonas reactans, a bacterial strain isolated from the intestinal flora of Blattella germanica with anti-Beauveria bassiana activity. Environ. Entomol. 2013, 42, 453-459.
34. Morales-Jiménez, J.; de León, A.V.; García-Domínguez, A.; Martínez-Romero, E.; Zúñiga, G.; Hernández-Rodríguez, C. Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microb. Ecol. 2013, 66, 200-210.
35. Hagen, K.S. Dependence of the olive fly, Dacus oleae, larvae on symbiosis with Pseudomonas savastanoi for the utilization of olive. 1966, 209, 423-424.
36. Harris, M.; Rose, S. Temporal changes in the egglaying behaviour of the Hessian fly. Entomol. Exp. Appl. 1989, 53, 17-29.
37. Chen, M.; Echegaray, E.; Whitworth, R.J.; Wang, H.; Sloderbeck, P.E.; Knutson, A.; Giles, K.L.; Royer, T.A. Virulence analysis of Hessian fly populations from Texas, Oklahoma, and Kansas. J. Econ. Entomol. 2009, 102, 774-780.
38. Stuart, J.; Hatchett, J. Morphogenesis and cytology of the salivary gland of the Hessian fly, Mayetiola destructor (Diptera: Cecidomyiidae). Ann. Entomol. Soc. Am. 1987, 80, 475-482.
39. Doyle, J.J. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull 1987, 19, 11-15.
40. Sambrook, J.; Fritsch, E.F.; Maniatis, T. Molecular cloning; Cold spring harbor laboratory press: New York, NY, USA, 1989; Volume 2.
41. Bansal, R.; Mian, M.; Michel, A.P. Microbiome diversity of Aphis glycines with extensive superinfection in native and invasive populations. Env. Microbiol. Rep. 2014, 6, 57-69.
42. Schloss, P.D.; Gevers, D.; Westcott, S.L. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PloS One 2011, 6, e27310.
43. Pruesse, E.; Quast, C.; Knittel, K.; Fuchs, B.M.; Ludwig, W.; Peplies, J.; Glöckner, F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35, 7188-7196.
44. Pruesse, E.; Peplies, J.; Glöckner, F.O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012, 28, 1823-1829.
45. Huse, S.M.; Welch, D.M.; Morrison, H.G.; Sogin, M.L. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 2010, 12, 1889-1898.
46. Quince, C.; Lanzen, A.; Davenport, R.J.; Turnbaugh, P.J. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 2011, 12, 38.
47. Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261-5267.
48. Pruesse, E.; Peplies, J.; Glöckner, F.O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012, 28, 1823-1829.
49. Chao, A.; Lee, S. Estimating the number of classes via sample coverage. Journal of the American Statistical Association 1992, 87, 210-217.
50. Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 1984, 265-270.
51. Giovanini, M.P.; Puthoff, D.P.; Nemacheck, J.A.; Mittapalli, O.; Saltzmann, K.D.; Ohm, H.W.; Shukle, R.H.; Williams, C.E. Gene-for-gene defense of wheat against the Hessian fly lacks a classical oxidative burst. Mol. Plant Microbe Interact. 2006, 19, 1023-1033.