Phylogenetic, metabolic, and taxonomic diversities shape mediterranean fruit fly microbiotas during ontogeny

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 303-313

  Aharon, Yael ^a   Pasternak, Zohar ^a   Yosef, Michael Ben ^a   Behar, Adi ^a,c   Lauzon, Carol ^b   Yuval, Boaz ^a   Jurkevitch, Edouard ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL COMMUNITY; CERATITIS CAPITATA; DIGESTIVE TRACT; DIVERSE COMMUNITY; FLUORESCENT IN SITU HYBRIDIZATION; HOST BEHAVIORS; MEDITERRANEAN FRUIT FLY; METABOLIC CAPABILITIES; METABOLIC PROFILING; MICROBIOTAS; MULTIPLE STRAINS; PYROSEQUENCING; STOCHASTIC EFFECTS; TAXONOMIC DIVERSITY;

BACTERIA; DIGESTIVE SYSTEM; DYNAMICS;

METABOLISM;

BACTERIAL DNA; PECTIN; RIBOSOME DNA; RNA 16S;

FLY; FRUIT; METABOLISM; MICROBIAL COMMUNITY; ONTOGENY; PHYLOGENETICS; STOCHASTICITY; TAXONOMY;

ANIMAL; ARTICLE; BACTERIUM; BIOTA; CLASSIFICATION; GASTROINTESTINAL TRACT; GENETICS; MEDITERRANEAN FRUIT FLY; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; POPULATION DYNAMICS;

ANIMALS; BACTERIA; BIOTA; CERATITIS CAPITATA; DNA, BACTERIAL; DNA, RIBOSOMAL; GASTROINTESTINAL TRACT; NITROGEN FIXATION; PECTINS; POPULATION DYNAMICS; RNA, RIBOSOMAL, 16S;

BACTERIA (MICROORGANISMS); CERATITIS CAPITATA; ENTEROBACTERIACEAE;

EID: 84871863418     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02761-12     Document Type: Article

References (72)

1. Weinert LA, Tinsley MC, Temperley M, Jiggins FM. 2007. Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol. Lett. 3:678-681.
2. Baumann P, Moran NA, Baumann L. 2006. Bacteriocyte-associated endosymbionts of insects, p 403-438. In Dworkin M, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The prokaryotes. Springer, New York, NY.
3. Behar A, Jurkevitch E, Yuval B. 2008. Bringing back the fruit into fruit fly-bacteria interactions. Mol. Ecol. 17:1375-1386.
4. Ben Yosef M, Jurkevitch E, Yuval B. 2008. Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol. Entomol. 33:145-154.
5. Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N, Ito M, Fukatsu T. 2010. Primary gut symbiont and secondary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. Appl. Environ. Microbiol. 76:3486-3494.
6. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T. 23 April 2012, posting date. Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. U. S. A. doi:10.1073/pnas.1200231109.
7. Feldhaar H. 2011. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36:533-543.
8. Mouton L, Henri H, Bouletreau M, Vavre F. 2003. Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 12:3459-3465.
9. Yuval B, Hendrichs J. 2000. Behavior of flies in the genus Ceratitis (Dacinae: Ceratidini), p 429-457. In Aluja M, Norrbom AL (ed), Fruit flies Tehpritidae: phylogeny and evolution of behaviour. CRC Press, Boca Raton, FL.
10. Liquido N, Shinoda LA, Cunningham RT. 1991. Host plants of the Mediterranean fruit fly (Diptera: Tephritidae): an annotated world review, p 52. Entomological Society of America, Madison, WI.
11. Behar A, Yuval B, Jurkevitch E. 2005. Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol. Ecol. 14:2637-2643.
12. Behar A, Yuval B, Jurkevitch E. 2008. Community structure of the Mediterranean fruit fly microbiota: seasonal and spatial sources of variation. Isr. J. Ecol. Evol. 54:181-191.
13. Ben Ami E, Yuval B, Jurkevitch E. 2010. Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J. 4:28-37.
14. Marchini D, Dallai RMR, Marri L. 2002. Bacteria associated with the oesophageal bulb of the medfly Ceratitis capitata (Diptera: Tephritidae). Curr. Microbiol. 44:120-124.
15. Lauzon C. 2003. Symbiotic relationships of tephritids, p 115-129. In Bourtzis K, Miller TA (ed), Insect symbiosis. CRC Press, Boca Raton, FL.
16. Lauzon CR, McCombs SD, Potter SE, Peabody NC. 2009. Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 102:85-95.
17. Behar A, Ben-Yosef M, Lauzon CR, Yuval B, Jurkevitch E. 2008. Structure and function of the bacterial community associated with the Mediterranean fruit fly, p 251-271. In Bourtzis K, Miller T (ed), Insect symbiosis. CRC Press, Boca Raton, FL.
18. Ben-Yosef M, Aharon Y, Jurkevitch E, Yuval B. 2010. Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a dietdependent fashion. Proc. Biol. Sci. 277:1545-1552.
19. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
20. Kloep F, Manz W, Röske I. 2006. Multivariate analysis of microbial communities in the River Elbe (Germany) on different phylogenetic and spatial levels of resolution. FEMS Microbiol. Ecol. 56:79-94.
21. Ootsubo M, Shimizu T, Tanaka R, Sawabe T, Tajima K, Yoshimizu M, Ezura Y, Ezaki T, Oyaizu H. 2002. Oligonucleotide probe for detecting Enterobacteriaceae by in situ hybridization. J. Appl. Microbiol. 93:60-68.
22. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
23. Ludwig W, Klenk H-P. 2005. Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics, p 49-65. In BrennerDJ, Krieg NR, Staley JT, Garrity GM (ed), Bergey's manual of systematic bacteriology. Springer, New York, NY.
24. Hugenholtz P, Tyson GW, Blackall LL. 2002. Design and evaluation of 16S rRNA-targeted oligonucleotide probes for fluorescence in situ hybridization. Methods Mol. Biol. 179:29-42.
25. Behrens S, Fuchs BM, Mueller F, Amann R. 2003. Is the in situ accessibility of the 16S rRNA of Escherichia coli for Cy3-labeled oligonucleotide probes predicted by a three-dimensional structure model of the 30S ribosomal subunit? Appl. Environ. Microbiol. 69:4935-4941.
26. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed- Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145. doi:10.1093/nar/gkn879.
27. Manz W, Ludwig ARW, Wagner M, Schleiffer KH. 1992. Phylogenetic oligonucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15:593-600.
28. Fukatsu T, Koga R, Smith WA, Tanaka K, Nikoh N, Sasaki-Fukatsu K, Yoshizawa K, Dale C, Clayton DH. 2007. Bacterial endosymbiont of the slender pigeonlouse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl. Environ. Microbiol. 73:6660-6668.
29. Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E. 2006. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl. Environ. Microbiol. 72:3646-3652.
30. Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer K-H. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter- Bacteroides in the natural environment. Microbiology 142:1097-1106.
31. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS. 2008. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8:125. doi:10.1186/1471-2180-8-125.
32. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
33. Quince C, Lanzen A, Davenport R, Turnbaugh P. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38. doi:10.1186/ 1471-2105-12-38.
34. Huse SM, Welch DM, Morrison HG, Sogin ML. 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 12:1889-1898.
35. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
37. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
38. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
39. Ruimy R, Breittmayer V, Boivin V, Christen R. 1994. Assessment of the state of activity of individual bacterial cells by hybridization with a ribosomal RNA targeted fluorescently labelled oligonucleotidic probe. FEMS Microbiol. Ecol. 15:207-213.
40. Behar A, Yuval B, Jurkevitch E. 2008. Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J. Insect Physiol. 54:1377-1383.
41. Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:17-37.
42. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T. 2006. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4:e337. doi:10.1371/journal.pbio.0040337.
43. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165-190.
44. Kikuchi Y, Hosokawa T, Fukatsu T. 2011. An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 5:446-460.
45. Conn KE, Ogawa JM, Manji BT, Adaskaveg JE. 1995. Leuconostoc mesenteroides subsp mesenteroides, the first report of a coccoid bacterium causing a plant disease. Phytopathology 85:593-599.
46. Naum M, Brown E, Mason-Gamer R. 2008. Is 16S rDNA a reliable phylogenetic marker to characterize relationships below the family level in the Enterobacteriaceae? J. Mol. Evol. 66:630-642.
47. Naum M, Brown EW, Mason-Gamer RJ. 2011. Is a robust phylogeny of the enterobacterial plant pathogens attainable? Cladistics 27:80-93. 48. Treangen TJ, Rocha EPC. 2011. Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet. 7:e1001284. doi:10.1371/journal.pgen.1001284.
48. Stecher B, Denzler R, Maier L, Bernet F, Sanders MJ, Pickard DJ, Barthel M, Westendorf AM, Krogfelt KA, Walker AW, Ackermann M, Dobrindt U, Thomson NR, Hardt W-D. 2012. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl. Acad. Sci. U. S. A. 109:1269-1274.
49. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:723-735.
50. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS. 2011. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254-256.
51. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 107:20051-20056.
52. Christenson LD, Foote RH. 1960. Biology of fruit flies. Annu. Rev. Entomol. 5:171-192.
53. Munguira ML, Muniz SFM. 1983. Estudio morfológico del aparato reproductor femenino de Ceratitis capitata Wied (Dipt: Trypetidae). Bol. Serv. Plagas 9:31-43.
54. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336:1255-1262.
55. McDonald PT, McInnis DO. 1985. Ceratitis capitata: effect of host fruit size on the number of eggs per clutch. Entomol. Exp. Appl. 37:207-211.
56. Papaj DR, Roitberg BD, Opp SB, Aluja M, Prokopy RJ, Wong TTY. 1990. Effect of marking pheromone on clutch size in the Mediterranean fruit fly. Physiol. Entomol. 15:463-468.
57. Mira A, Moran NA. 2002. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44:137-143.
58. Vautrin E, Vavre F. 2009. Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol. 17:95-99.
59. Hosokawa T, Kikuchi Y, Fukatsu T. 2007. How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect-bacterium mutualism? Mol. Ecol. 16:5316-5325.
60. Ferrari J, Vavre F. 2011. Bacterial symbionts in insects or the story of communities affecting communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366:1389-1400.
61. Sela S, Nestel D, Pinto R, Nemny-Lavy E, Bar-Joseph M. 2005. Mediterranean fruit fly as a potential vector of bacterial pathogens. Appl. Environ. Microbiol. 71:4052-4056.
62. Marchini D, Manetti AGO, Rosetto M, Bernini LF, Telford JL, Baldari CT, Dallai R. 1995. cDNA sequence and expression of the ceratotoxin gene encoding an antibacterial sex-specific peptide from the medfly Ceratitis capitata (Diptera). J. Biol. Chem. 270:6199-6204.
63. Marri L, Dallai R, Marchini D. 1996. The novel antibacterial peptide ceratotoxin A alters permeability of the inner and outer membrane of Escherichia coli K-12. Curr. Microbiol. 33:40-43.
64. Friedrich MW, Schmitt-Wagner D, Lueders T, Brune A. 2001. Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil-feeding termite Cubitermes orthognathus. Appl. Environ. Microbiol. 67:4880-4890.
65. Li M, Yang H, Gu J-D. 2009. Phylogenetic diversity and axial distribution of microbes in the intestinal tract of the polychaete Neanthes glandici. Microb. Ecol. 58:892-902.
66. Nakajima H, Hongoh Y, Usami R, Kudo T, Ohkuma M. 2005. Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiol. Ecol. 54:247-255.
67. Kuraishi T, Binggeli O, Opota O, Buchon N, Lemaitre B. 2011. Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 108:15966-15971.
68. Lauzon CR, Potter SE. 2012. Description of the irradiated and nonirradiated midgut of Ceratitis capitata Wiedemann (Diptera: Tephritidae) used for sterile insect technique. J. Pest Sci. 85(2):217-226.
69. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25:697-743.
70. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. 2009. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 23:2333-2344.
71. Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N, Kudo T. 2006. Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol. Ecol. 15:505-516.
72. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, Stanton C, van Sinderen D, O'Connor M, Harnedy N, O'Connor K, Henry C, O'Mahony D, Fitzgerald AP, Shanahan F, Twomey C, Hill C, Ross RP, O'Toole PW. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl 1):4586-4591.