Comparative Evaluation of the Gut Microbiota Associated with the Below- and Above-Ground Life Stages (Larvae and Beetles) of the Forest Cockchafer, Melolontha hippocastani

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Arias Cordero, Erika ^a   Ping, Liyan ^a   Reichwald, Kathrin ^b   Delb, Horst ^c   Platzer, Mathias ^b   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b FRITZ LIPMANN INSTITUTE   (Germany)

^c Württemberg Forest Research Institute of the state of Baden   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

AEROBIC BACTERIUM; ANIMAL TISSUE; ARTICLE; BACILLI; BACTERIAL TRANSLOCATION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BEETLE; BETAPROTEOBACTERIA; CLOSTRIDIUM; DELTAPROTEOBACTERIA; DIGESTION; ECOLOGICAL NICHE; ERYSIPELOTRICHACEAE; FEEDING BEHAVIOR; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENE LIBRARY; INTESTINE FLORA; LARVAL STAGE; MALE; MELOLONTHA HIPPOCASTANI; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PUPA (LIFE CYCLE STAGE); SPECIES COMPARISON; SPHINGOBACTERIA; UNINDEXED SEQUENCE;

ANIMALS; BACTERIA; BEETLES; FLUORESCENT DYES; GASTROINTESTINAL TRACT; GENE LIBRARY; HERBIVORY; LARVA; LIFE CYCLE STAGES; METAGENOME; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT ROOTS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; TREES;

BACILLI (CLASS); BACTERIA (MICROORGANISMS); CLOSTRIDIA; COLEOPTERA; GAMMAPROTEOBACTERIA; HEXAPODA; MELOLONTHA HIPPOCASTANI; MELOLONTHA MELOLONTHA; OTUS; SPHINGOBACTERIA;

EID: 84870950048     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051557     Document Type: Article

References (61)

1. Dillon RJ, Dillon VM, (2004) The gut bacteria of insects: Nonpathogenic interactions. Annu Rev Entomol 49: 71-92.
2. Douglas AE, (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23: 38-47.
3. Brune A (2005) Symbiotic associations between termites and prokaryotes. The Prokaryotes. http://www.springer.com/lifesciences/microbiology/book/978-0-387-30742-8: Springer-Verlag.
4. Breznak JA, Brune A, (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39: 453-487.
5. Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, et al. (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71: 6590-6599.
6. Richter P, (1958) Biology of Scarabeidae. Annu Rev Entomol 3: 311-334.
7. Jackson TA, (2006) Scarabs as pests: a continuing problem. Coleopts Mono Soc 5: 102-119.
8. Keller S, (1984) Das andere Gesicht des Maikäfers. Tages Anz Magazine 19: 27-34.
9. Wildbolz T, (1954) Beitrag zur Anatomie, Histologie und Physiologie des Darmkanals der Larve von Melolontha melolontha L. Mitt Schweiz Entomol Ges. 27: 14-239.
10. Terra WR, Ferreira C, (1994) Insect digestive enzymes- properties, compartmentalization and function. Comp Biochem Physiol B: Biochem Mol Biol 109: 1-62.
11. Lemke T, Stingl U, Egert M, Friedrich MW, Brune A, (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69: 6650-6658.
12. Terra WR, (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35: 181-200.
13. Broderick NA, Raffa KF, Goodman RM, Handelsman J, (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70: 293-300.
14. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J, (2010) Robustness of the Bacterial Community in the Cabbage White Butterfly Larval Midgut. Microb Ecol 59: 199-211.
15. Li X, Brune A, (2005) Digestion of microbial biomass, structural polysaccharides, and protein by the humivorous larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Soil Biol Biochem 37: 107-116.
16. Egert M, Stingl U, Bruun LD, Pommerenke B, Brune A, et al. (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Appl Environ Microbiol 71: 4556-4566.
17. Andert J, Geissinger O, Brune A, (2008) Peptidic soil components are a major dietary resource for the humivorous larvae of Pachnoda spp. (Coleoptera: Scarabaeidae). J Insect Physiol 54: 105-113.
18. Andert J, Marten A, Brandl R, Brune A, (2010) Inter- and intraspecific comparison of the bacterial assemblages in the hindgut of humivorous scarab beetle larvae (Pachnoda spp.). FEMS Microbiol Ecol 74: 439-449.
19. Cazemier AE, Verdoes CJ, Reubsaet FAG, Hackstein JHP, van der Drift C, et al. (2003) Promicronospora pachnodae sp. nov., a member of the (hemi)cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata. Antonie Van Leeuwenhoek 83: 135-148.
20. Park DS, Oh HW, Jeong WJ, Kim H, Park HY, et al. (2007) A culture-based study of the bacterial communities within the guts of nine longicorn beetle species and their exo-enzyme producing properties for degrading xylan and pectin. Journal of Microbiology 45: 394-401.
21. Anand AAP, Vennison SJ, Sankar SG, Prabhu DIG, Vasan PT, et al. (2010) Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J Insect Sci 10.
22. Egert M, Wagner B, Lemke T, Brune A, Friedrich MW, (2003) Microbial Community Structure in Midgut and Hindgut of the Humus-Feeding Larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69: 6659-6668.
23. Pittman GW, Brumbley SM, Allsopp PG, O'Neill SL, (2008) "Endomicrobia" and other bacteria associated with the hindgut of Dermolepida albohirtum larvae. Appl Environ Microbiol 74: 762-767.
24. Schloss PD, Delalibera I, Handelsman J, Raffa KF, (2006) Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environ Entomol 35: 625-629.
25. Vasanthakumar A, Handelsman J, Schloss PD, Bauer LS, Raffa K, (2008) Gut Microbiota of an Invasive Subcortical Beetle, Agrilus planipennis Fairmaire, Across Various Life Stages. Environ Entomol 37: 1344-1353.
26. Park D-S, Oh H-W, Jeong W-J, Kim H, Park H-Y, et al. (2007) A Culture-Based Study of the Bacterial Communites within the Guts of Nine Longicorn Beetle Species and their Exo-enzyme Producing Properties for Degrading Xylan and Pectin. J Microbiol 45: 394-401.
27. Jones SE, Lennon JT, (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci USA 107: 5881-5886.
28. Su Z, Zhang M, Liu X, Tong L, Huang Y, et al. (2010) Comparison of Bacterial Diversity in Wheat Bran and in the Gut of Larvae and Newly Emerged Adult of Musca domestica (Diptera: Muscidae) by Use of Ethidium Monoazide Reveals Bacterial Colonization. J Econ Entomol 103: 1832-1841.
29. Adams L, Boopathy R, (2005) Isolation and characterization of enteric bacteria from the hindgut of Formosan termite. Bioresour Technol 96: 1592-1598.
30. Khianngam S, Tanasupawat S, Akaracharanya A, Kim KK, Lee KC, et al. (2010) Cohnella thailandensis sp. nov., a xylanolytic bacterium from Thai soil. Int J Syst Evol Microbiol 60: 2284-2287.
31. Yoon M-H, Ten LN, Im W-T, (2007) Cohnella panacarvi sp nov., a xylanolytic bacterium isolated from ginseng cultivating soil. J Mol Microbiol Biotechnol 17: 913-918.
32. Leuschner C, Coners H, Icke R, Hartmann K, Effinger ND, et al. (2003) Chemical composition of the periderm in relation to in situ water absorption rates of oak, beech and spruce fine roots. Annals of Forest Science 60: 763-772.
33. Ammar H, Lopez S, Gonzalez JS, Ranilla MJ, (2004) Chemical composition and in vitro digestibility of some Spanish browse plant species. J Sci Food Agric 84: 197-204.
34. Kuhnigk T, Branke J, Krekeler D, Cypionka H, Konig H, (1996) A feasible role of sulfate-reducing bacteria in the termite gut. Syst Appl Microbiol 19: 139-149.
35. Potrikus CJ, Breznak JA, (1977) Nitrogen-Fixing Enterobacter-Agglomerans Isolated from Guts of Wood-Eating Termites. Appl Environ Microbiol 33: 392-399.
36. Anand AAP, Sripathi K, (2004) Digestion of cellulose and xylan by symbiotic bacteria in the intestine of the Indian flying fox (Pteropus giganteus). Comp Biochem Physiol, A: Mol Integr Physiol 139: 65-69.
37. Rowell RM, Pettersen R, Han JS, Rowell JS, Tshabalala MA (2005) Cell Wall Chemistry. In: Rowell RM, editor. Handbook of Wood Chemistry and Wood Composites. Boca Raton, Florida: CRC Press. 35-74.
38. Emami K, Nagy T, Fontes C, Ferreira LMA, Gilbert HJ, (2002) Evidence for temporal regulation of the two Pseudomonas cellulosa xylanases belonging to glycoside hydrolase family 11. J Bacteriol 184: 4124-4133.
39. Rössler ME, (1961) Ernährungsphysiologische untersuchungen an Scarabaeidenlarven (Oryctes Nasicornis L., Melolontha melontha L.). J Insect Physiol 1961: 62-80.
40. Brune A, Emerson D, Breznak JA, (1995) The termite gut microflora as an oxygen sink: Microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61: 2681-2687.
41. Brune A, Frenzel P, Cypionka H, (2000) Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24: 691-710.
42. Zhou JP, Huang HQ, Meng K, Shi PJ, Wang YR, et al. (2009) Molecular and biochemical characterization of a novel xylanase from the symbiotic Sphingobacterium sp TN19. Appl Microbiol Biotechnol 85: 323-333.
43. Chester B, Cooper LH, (1979) Achromobacter species (cdc group vd)- morphological and biochemical characterization. J Clin Microbiol 9: 425-436.
44. Steinhaus EA, (1941) A study of the bacteria associated with thirty species of insects. J Bacteriol 42: 757-790.
45. Li H, Medina F, Vinson SB, Coates CJ, (2005) Isolation, characterization, and molecular identification of bacteria from the red imported fire ant (Solenopsis invicta) midgut. J Invertebr Pathol 89: 203-209.
46. Wiegel J, Tanner R, Rainey FA (2006) An Introduction to the Family Clostridiaceae. In: Dworkin M, et al., editors. Prokaryotes: A Handbook on the Biology of Bacteria, vol. 4, 3rd edition:Bacteria: Firmicutes, Cyanobacteria. 654-678.
47. Ping L, Platzer M, Wen G, Delaroque N, (2012) Coevolution of aah: A dps-Like Gene with the Host Bacterium Revealed by Comparative Genomic Analysis. TheScientificWorld J 2012: 1-9.
48. Huber T, Faulkner G, Hugenholtz P, (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
49. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7.
50. Magurran AE (2004) Measuring Biological Diversity. Oxford Blackwell Science Ltd. 256 p.
51. 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. Appl Environ Microbiol 75: 7537-7541.
52. Lozupone C, Hamady M, Knight R (2006) UniFrac- An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7.
53. Hamady M, Lozupone C, Knight R, (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27.
54. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, et al. (1990) Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial-populations. Appl Environ Microbiol 56: 1919-1925.
55. Hung WL, Wade WG, Boden R, Kelly DP, Wood AP, (2011) Facultative methylotrophs from the human oral cavity and methylotrophy in strains of Gordonia, Leifsonia, and Microbacterium. Arch Microbiol 193: 407-417.
56. Lehman RM, Lundgren JG, Petzke LM, (2009) Bacterial communities associated with the digestive tract of the predatory ground beetle, Poecilus chalcites, and their modification by laboratory rearing and antibiotic treatment. Microb Ecol 57: 349-358.
57. Hongoh Y, Ohkuma M, Kudo T, (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44: 231-242.
58. Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S, et al. (2006) Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol Ecol 15: 505-516.
59. Yu H, Wang Z, Liu L, Xia Y, Cao Y, et al. (2008) Analysis of the intestinal microflora in Hepialus gonggaensis larvae Using 16S rRNA sequences. Curr Microbiol 56: 391-396.
60. Cuiv PO, Klaassens ES, Durkin AS, Harkins DM, Foster L, et al. (2011) Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J Bacteriol 193: 1288-1289.
61. Biebl H, Schwab-Hanisch H, Spröer C, Lusdorf H, (2000) Propionispora vibrioides, nov. gen., nov. sp., a new gram-negative, spore-forming anaerobe that ferments sugar alcohols. Arch Microbiol 174: 239-247.