Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Mattila, Heather R ^a   Rios, Daniela ^a   Walker Sperling, Victoria E ^a   Roeselers, Guus ^b   Newton, Irene L G ^c  

^a WELLESLEY COLLEGE   (United States)

^b TNO   (Netherlands)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; COMPLEMENTARY DNA;

ANAEROBIC BACTERIUM; ANAEROBIC FERMENTATION; ARTICLE; BIFIDOBACTERIUM; CONTROLLED STUDY; GENETIC VARIABILITY; HONEYBEE; HOST PATHOGEN INTERACTION; MATING; MICROFLORA; NONHUMAN; NUTRITION; ORGANISM COLONY; PATHOGEN LOAD; PYROSEQUENCING; QUEEN (INSECT); WORKER (INSECT); ANIMAL; BACTERIUM; BEE; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; MICROBIOLOGY; NONPARAMETRIC TEST; PHYSIOLOGY; SPECIES DIFFERENCE; UNITED STATES;

APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM;

ANIMALS; BACTERIA; BEES; BIFIDOBACTERIUM; DNA, COMPLEMENTARY; GASTROINTESTINAL TRACT; GENETIC VARIATION; MASSACHUSETTS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; STATISTICS, NONPARAMETRIC;

EID: 84858039964     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032962     Document Type: Article

References (128)

1. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, et al. (2010) Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research 49: 15-22.
2. vanEngelsdorp D, Hayes J, Underwood RM, Caron D, Pettis J, (2011) A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010. Journal of Apicultural Research 50: 1-10.
3. Oldroyd BP, (2007) What's killing American honey Bees? Plos Biology 5: 1195-1199.
4. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287.
5. Vanengelsdorp D, Evans JD, Donovall L, Mullin C, Frazier M, et al. (2009) "Entombed Pollen": A new condition in honey bee colonies associated with increased risk of colony mortality. Journal of Invertebrate Pathology 101: 147-149.
6. Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, et al. (2010) Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. Plos One 5:-.
7. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, et al. (2009) Colony Collapse Disorder: A Descriptive Study. Plos One 4:-.
8. Vanengelsdorp D, Hayes J, Underwood RM, Pettis J, (2008) A Survey of Honey Bee Colony Losses in the US, Fall 2007 to Spring 2008. Plos One 3:-.
9. vanEngelsdorp D, Hayes J, Underwood RM, Pettis JS, (2010) A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. Journal of Apicultural Research 49: 7-14.
10. vanEngelsdorp D, Meixner MD, (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103: S80-S95.
11. vanEngelsdorp D, Speybroeck N, Evans JD, Nguyen BK, Mullin C, et al. (2010) Weighing Risk Factors Associated With Bee Colony Collapse Disorder by Classification and Regression Tree Analysis. Journal of Economic Entomology 103: 1517-1523.
12. Meixner MD, Costa C, Kryger P, Hatjina F, Bouga M, et al. (2010) Conserving diversity and vitality for honey bee breeding. Journal of Apicultural Research 49: 85-92.
13. Naug D, (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation 142: 2369-2372.
14. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B, (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5: 200-211.
15. Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A, (2011) Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet 7: e1002272.
16. Dillon RJ, Dillon VM, (2004) The gut bacteria of insects: Nonpathogenic interactions. Annual Review of Entomology 49: 71-92.
17. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL, (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
18. Ley R, Turnbaugh P, Klein S, Gordon J, (2006) Microbial ecology: Human gut microbes associated with obesity. Nature 444: 1022-1023.
19. Martin FPJ, Wang Y, Sprenger N, Yap IKS, Lundstedt T, et al. (2008) Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Molecular Systems Biology 4:-.
20. Moran NA, Telang A, (1998) Bacteriocyte-associated symbionts of insects- A variety of insect groups harbor ancient prokaryotic endosymbionts. Bioscience 48: 295-304.
21. Mueller UG, Schultz TR, Currie CR, Adams RMM, Malloch D, (2001) The origin of the attine ant-fungus mutualism. Quarterly Review of Biology 76: 169-197.
22. Gokarn RR, Eiteman MA, Martin SA, Eriksson KEL, (1997) Production of succinate from glucose, cellobiose, and various cellulosic materials by the ruminal anaerobic bacteria Fibrobacter succinogenes and Ruminococcus flavefaciens. Applied Biochemistry and Biotechnology 68: 69-80.
23. Lednicka D, Mergaert J, Cnockaert MC, Swings J, (2000) Isolation and identification of cellulolytic bacteria involved in the degradation of natural cellulosic fibres. Systematic and Applied Microbiology 23: 292-299.
24. Han YJ, Chen HZ, (2007) Plant cell wall proteins & enzymatic hydrolysis of lignocellulose. Progress in Chemistry 19: 1153-1158.
25. Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG, et al. (2010) An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity. Plos Genetics 6:-.
26. Gheldof N, Wang XH, Engeseth NJ, (2002) Identification and quantification of antioxidant components of honeys from various floral sources. Journal of Agricultural and Food Chemistry 50: 5870-5877.
27. Roulston TH, Cane JH, (2002) The effect of pollen protein concentration on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera: Apiformes). Evolutionary Ecology 16: 49-65.
28. Haydak M, (1970) Honey bee nutrition. Annual Reviews of Entomology 15: 143-156.
29. Herbert E, eds. (1992) Honey bee nutrition. 5th ed Hamilton, IL Dadant and Sons pp. 197-233.
30. Herbert E, eds. (1992) Hone bee nutrition. pp. 197-233 Hamilton, IL.
31. Roulston TH, Cane JH, (2000) Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution 222: 187-209.
32. Kunieda T, Fujiyuki T, Kucharski R, Foret S, Ament SA, et al. (2006) Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Molecular Biology 15: 563-576.
33. Crailsheim K, Schneider LHW, Hrassnigg N, Buhlmann G, Brosch U, et al. (1992) Pollen Consumption and Utilization in Worker Honeybees (Apis-Mellifera-Carnica)- Dependence on Individual Age and Function. Journal of Insect Physiology 38: 409-419.
34. Cook SM, Awmack CS, Murray DA, Williams IH, (2003) Are honey bees' foraging preferences affected by pollen amino acid composition? Ecological Entomology 28: 622-627.
35. Day S, Beyer R, Mercer A, Ogden S, (1990) The nutrient composition of honeybee-collected pollen in Otago, New Zealand. Journal of Apicultural Research 29: 138-146.
36. Human H, Nicolson S, (2006) Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheidii var. davyana (Aspholdelaceae). Phyotchemistry 67: 1486-1492.
37. Gilliam M, (1979) Microbiology of Pollen and Bee Bread- the Yeasts. Apidologie 10: 43-53.
38. Vasquez A, Olofsson TC, (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research 48: 189-195.
39. Haydak M, Vivino A, (1950) The changes in the thiamine, riboflavin, niacin, and pantothenic acid content in the food of female honeybees during growth with a note on the vitamin K activity of royal jelly and bee bread. Annals of the Entomological Society of America 43: 361-367.
40. Standifer L, McCaughey W, Dixon S, Gilliam M, (1980) Biochemistry and microbiology of pollen collected by honey bees (Apis mellifera L.) from almond, Prunis dulcis. II Protein, amino acids, and enzymes. Apidologie 11: 163-171.
41. Herbert E, Shimanuki H, (1978) Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9: 33-40.
42. Loper G, Standifer L, Thompson M, Gilliam M, (1980) Biochemistry and microbiology of bee-collected almond (Prunis dulcis) pollen and bee bread. I. Fatty-acids, sterols, vitamins and minerals. Apidologie 11: 63-73.
43. Gilliam M, (1979) Microbiology of Pollen and Bee Bread- Genus Bacillus. Apidologie 10: 269-274.
44. Gilliam M, (1997) Identification and roles of non-pathogenic microflora associated with honey bees (vol 155, pg 1, 1997). Fems Microbiology Letters 157: 219-219.
45. Gilliam M, Roubik DW, Lorenz BJ, (1990) Microorganisms Associated with Pollen, Honey, and Brood Provisions in the Nest of a Stingless Bee, Melipona-Fasciata. Apidologie 21: 89-97.
46. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F, (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. Fems Microbiology Ecology 59: 600-610.
47. Jeyaprakash A, Hoy MA, Allsopp MH, (2003) Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. Journal of Invertebrate Pathology 84: 96-103.
48. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, et al. (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20: 619-628.
49. Beutler R, Opfinger E, (1949) Pollenernährung und Nosemabefall der Honigbiene (Apis mellifica) [Pollen feeding and Nosema infection of the honey bee (Apis mellifica)]. Zeitschrift für Vergleichende Physiologie 32: 383-421.
50. Janmaat AF, Winston ML, (2000) The influence of pollen storage area and Varroa jacobsoni Oudemans parasitism on temporal caste structure in honey bees (Apis mellifera L.). Insectes Sociaux 47: 177-182.
51. Tarpy DR, Nielsen R, Nielsen DI, (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Sociaux 51: 203-204.
52. Moritz RFA, Kryger P, Allsopp MH, (1996) Competition for royalty in bees. Nature 384: 31-31.
53. Tarpy DR, Nielsen DI, (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera: Apidae). Annals of the Entomological Society of America 95: 513-528.
54. Kronauer D, Johnson R, Boomsma J, (2007) The evolution of multiple mating in army ants. Evolution 61: 413-422.
55. Villesen P, Murakami T, Schultz TR, Boomsma JJ, (2002) Identifying the transition between single and multiple mating of queens in fungus-growing ants. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 1541-1548.
56. Palmer KA, Oldroyd BP, (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90: 265-268.
57. Seeley TD, Tarpy DR, (2007) Queen promiscuity lowers disease within honeybee colonies. Proceedings of the Royal Society B-Biological Sciences 274: 67-72.
58. Tarpy DR, Seeley TD, (2006) Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93: 195-199.
59. Jones JC, Myerscough MR, Graham S, Oldroyd BP, (2004) Honey bee nest thermoregulation: Diversity promotes stability. Science 305: 402-404.
60. Girard MB, Mattila HR, Seeley TD, (2011) Recruitment-dance signals draw larger audiences when honey bee colonies have multiple patrilines. Insectes Sociaux 58: 77-86.
61. Oldroyd BP, Rinderer TE, Harbo JR, Buco SM, (1992) Effects of Intracolonial Genetic Diversity on Honey-Bee (Hymenoptera, Apidae) Colony Performance. Annals of the Entomological Society of America 85: 335-343.
62. Mattila HR, Burke KM, Seeley TD, (2008) Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers. Proceedings of the Royal Society B-Biological Sciences 275: 809-816.
63. Mattila HR, Seeley TD, (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364.
64. Mattila HR, Seeley TD, (2010) Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers. Behavioral Ecology and Sociobiology 64: 875-889.
65. Mattila HR, Seeley TD, (2011) Does a polyandrous honeybee queen improve through patriline diversity the activity of her colony's scouting foragers? Behavioral Ecology and Sociobiology 65: 799-811.
66. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science 312: 1355-1359.
67. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, et al. (2008) Evolution of mammals and their gut microbes. Science 320: 1647-1651.
68. Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang TY, et al. (2011) Disease Phenotype and Genotype Are Associated with Shifts in Intestinal-associated Microbiota in Inflammatory Bowel Diseases. Inflammatory Bowel Diseases 17: 179-184.
69. Kovacs A, Ben-Jacob N, Tayem H, Halperin E, Iraqi FA, et al. (2011) Genotype Is a Stronger Determinant than Sex of the Mouse Gut Microbiota. Microbial Ecology 61: 423-428.
70. Roeselers G, Mittge E, Stephens W, Parichy D, Cavanaugh C, et al. (2011) Evidence for a core gut microbiota in the zebrafish. The ISME Journal doi:10.1038/ismej.2011.38.
71. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW, (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213-1216.
72. Michener C, (1974) The social behavior of the bees Cambridge, MA Harvard University Press.
73. Stackebrandt E, Hespell R, eds. (2006) pp. 419-429 The Family Succinivibrionaceae: Springer-Verlag.
74. Bjorkroth, Holzapfel, eds. (2006) Genera Leuconostoc, Oenoccocus, and Weissella Berlin Springer-Verlag pp. 267-319.
75. Hammes W, Hertel C, eds. (2006) pp. 320-403 The Genera Lactobacillus and Carnobacterium: Springer-Verlag.
76. Biavati B, Mattarelli P, eds. (2006) pp. 322-382 The Family Bifidobacteriaceae: Springer-Verlag.
77. Sanz Y, Sanchez E, Marzotto M, Calabuig M, Torriani S, et al. (2007) Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol 51: 562-568.
78. Henderson AR, (2005) The bootstrap: a technique for data-driven statistics. Using computer-intensive analyses to explore experimental data. Clin Chim Acta 359: 1-26.
79. Kacaniova M, Chlebo R, Kopernicky M, Trakovicka A, (2004) Microflora of the honeybee gastrointestinal tract. Folia Microbiologica 49: 169-171.
80. Mohr KI, Tebbe CC, (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environmental Microbiology 8: 258-272.
81. Lennon JT, Jones SE, (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9: 119-130.
82. Jones SE, Lennon JT, (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci U S A 107: 5881-5886.
83. Fierer N, Lennon JT, (2011) The generation and maintenance of diversity in microbial communities. Am J Bot 98: 439-448.
84. Rodriguez-Blanco A, Ghiglione JF, Catala P, Casamayor EO, Lebaron P, (2009) Spatial comparison of total vs. active bacterial populations by coupling genetic fingerprinting and clone library analyses in the NW Mediterranean Sea. FEMS Microbiol Ecol 67: 30-42.
85. McCarren J, Becker JW, Repeta DJ, Shi YM, Young CR, et al. (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proceedings of the National Academy of Sciences of the United States of America 107: 16420-16427.
86. Lanzen A, Jorgensen SL, Bengtsson MM, Jonassen I, Ovreas L, et al. (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiol Ecol 77: 577-589.
87. Jones SE, Lennon JT, (2010) Dormancy contributes to the maintenance of microbial diversity. Proceedings of the National Academy of Sciences of the United States of America 107: 5881-5886.
88. Schloss PD, Westcott SL, (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 77: 3219-3226.
89. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, et al. (2010) Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2: 53-66.
90. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108 (Suppl 1): 4578-4585.
91. Ochman H, Worobey M, Kuo CH, Ndjango JB, Peeters M, et al. (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8: e1000546.
92. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, et al. (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5: 1595-1608.
93. Koch H, Schmid-Hempel P, (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci U S A 108: 19288-19292.
94. O'Herrin S, Kenealy W, (1993) Glucose and carbon dioxide metabolism by Succinivibrio dextrinosolvens. Applied Environmental Microbiology 59: 748-755.
95. Mills DA, Marcobal A, (2006) Genomic analysis of Oenococcus oeni. American Journal of Enology and Viticulture 57: 390A-390A.
96. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, et al. (2010) Acetic Acid Bacteria, Newly Emerging Symbionts of Insects. Applied and Environmental Microbiology 76: 6963-6970.
97. Brown MV, Schwalbach MS, Hewson I, Fuhrman JA, (2005) Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environmental Microbiology 7: 1466-1479.
98. Zourari A, Accolas J, Desmazeaud M, (1992) Metabolism and biochemical characteristics of yogurt bacteria: a review. Lait 72: 1-34.
99. Kopecny J, Mrazek J, Killer J, (2010) The presence of bifidobacteria in social insects, fish and reptiles. Folia Microbiol (Praha) 55: 336-339.
100. Olofsson TC, Vasquez A, (2009) Phylogenetic comparison of bacteria isolated from the honey stomachs of honey bees Apis mellifera and bumble bees Bombus spp. Journal of Apicultural Research 48: 233-237.
101. Olofsson T, Vasquez A, (2010) Novel bacteria isolated from fresh honey or the honey producing tract of honey bees. USA.
102. Evans JD, Lopez DL, (2004) Bacterial Probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97: 752-756.
103. Kaznowski A, Szymas B, Jazdzinska E, Kazimierczak M, Paetz H, et al. (2005) The effects of probiotic supplementation on the content of intestinal microflora and chemical composition of worker honey bees (Apis mellifera). Journal of Apicultural Research 44: 10-14.
104. Johnson M, Agrawal A, (2007) Covariation and composition of arthropod species across plant genotypes of evening primrose (Oenothera biennis). Oikos 116: 941-956.
105. Crutsinger G, Collins M, Fordyce J, Sanders N, (2008) Temporal dynamics in non-additive responses of arthropods to host-plant genotypic diversity. Oikos 117: 255-264.
106. Crutsinger G, Reynolds W, Classen A, Sanders N, (2008) Disparate effects of plant genotypic diversity on foliage and litter arthropod communities. Oecologia 158: 65-75.
107. Schweitzer J, Fischer D, Rehill B, Wooley S, Woolbright S, et al. (2011) Forest gene diversity is correlated with the composition and function of soil microbial communities. Population Ecology 53: 35-46.
108. Berg RD, (1996) The indigenous gastrointestinal microflora. Trends in Microbiology 4: 430-435.
109. Dillon R, Charnley K, (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Research in Microbiology 153: 503-509.
110. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology 15: 645-656.
111. vanEngelsdorp D, Hayes J, Underwood R, Pettis J, (2010) A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. Journal of apicultural research 49: 7-14.
112. Mullin C, Frazier M, Frazier J, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5: e9754.
113. Camazine S, Cakmak I, Cramp K, Finley J, Fisher J, et al. (1998) How healthy are commercially-produced US honey bee queens? American Bee Journal 138: 677-680.
114. Lane D, eds. (1991) 16S/23S rRNA sequencing New York, NY John Wiley and Sons pp. 115-175.
115. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M, (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology 22: 434-444.
116. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology 75: 7537-7541.
117. Huse SM, Welch DM, Morrison HG, Sogin ML, (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environmental Microbiology 12: 1889-1898.
118. Haas B, Grevers D, Earl A, Feldgarden M, Ward D, et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research 21: 494-504.
119. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied Environmental Microbiology 71: 8228-8235.
120. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261-5267.
121. Hurst MRH, Glare TR, Jackson TA, (2004) Cloning Serratia entomophila antifeeding genes- A putative defective prophage active against the grass grub Costelytra zealandica (vol 186, pg 5116, 2004). Journal of Bacteriology 186: 7023-7024.
122. Flyg C, Kenne K, Boman HG, (1980) Insect Pathogenic Properties of Serratia-Marcescens- Phage-Resistant Mutants with a Decreased Resistance to Cecropia Immunity and a Decreased Virulence to Drosophila. Journal of General Microbiology 120: 173-181.
123. Dodd SJ, Hurst MRH, Glare TR, O'Callaghan M, Ronson CW, (2006) Occurrence of sep insecticidal toxin complex genes in Serratia spp. and Yersinia frederiksenii. Applied and Environmental Microbiology 72: 6584-6592.
124. Biosca EG, Gonzalez R, Lopez-Lopez MJ, Soria S, Monton C, et al. (2003) Isolation and characterization of Brenneria quercina, causal agent for bark canker and drippy nut of Quercus spp. in Spain. Phytopathology 93: 485-492.
125. Turyanitsa A, Boiko N, (1996) Pathogenic effect of bacteria of Klebsiella genus on Lepinotarsa decemlineata. Mikrobiologichnyi Zhurnal 58: 73-80.
126. Yamamoto T, Ota E, (1989) An outbreak of European foulbrood disease associated with Melissoccoccus pluton. Journal of the Japan veterinary medical association 42: 249-254.
127. Belloy L, Imdorf A, Fries I, Forsgren E, Berthoud H, et al. (2007) Spatial distribution of Melissococcus plutonis in adult honey bees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie 38: 136-140.
128. Forsgren E, Olofsson TC, Vasquez A, Fries I, (2010) Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108.