Classifying the bacterial gut microbiota of termites and cockroaches: A curated phylogenetic reference database (DictDb)

Systematic and Applied Microbiology

Volumn 38, Issue 7, 2015, Pages 472-482

  Mikaelyan, Aram ^a,b   Köhler, Tim ^a   Lampert, Niclas ^a   Rohland, Jeffrey ^a   Boga, Hamadi ^a   Meuser, Katja ^a   Brune, Andreas ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

16S rRNA; Cockroaches; Deep sequencing; Gut microbiota; Insects; Termites

Indexed keywords

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

ALISTIPES; AMPLICON; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL FLORA; COCKROACH; COMMUNITY STRUCTURE; COMPARATIVE STUDY; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; DICTYOPTERA; FIBROBACTERES; GENE LIBRARY; INTESTINE FLORA; ISOPTERA; MICROBIAL COMMUNITY; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PHYLUM; PRIORITY JOURNAL; REFERENCE DATABASE; SEQUENCE ANALYSIS; SPECIES DIVERSITY; TAXONOMY; TREPONEMA; ANIMAL; BACTERIUM; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY;

ANIMALS; BACTERIA; CLUSTER ANALYSIS; COCKROACHES; DNA, BACTERIAL; DNA, RIBOSOMAL; GASTROINTESTINAL MICROBIOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; ISOPTERA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84944150078     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2015.07.004     Document Type: Article

References (65)

1. Anisimova M., Gil M., Dufayard J.-F., Dessimoz C., Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst. Biol. 2011, 60:685-699.
2. Bauer E., Lampert N., Mikaelyan A., Köhler T., Maekawa K., Brune A. Physicochemical conditions, metabolites, and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae). FEMS Microbiol. Ecol. 2014, 91:1-14.
3. Bell W., Roth L., Nalepa C. Cockroaches: Ecology, Behavior and Natural History 2007, Johns Hopkins University Press, Baltimore.
4. Breznak J.A., Leadbetter J.R. Termite gut spirochetes. Prokaryotes 2006, 318-329. Springer, New York. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
5. Breznak J.A. Phylogenetic diversity and physiology of termite gut spirochetes. Integr. Comp. Biol. 2002, 42:313-318.
6. Brune A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 2014, 12:168-180.
7. Brune A., Dietrich C. The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu. Rev. Microbiol. 2015, 69.
8. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., Mcdonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
9. Cole J.R., Wang Q., Fish J.A., Chai B., McGarrell D.M., Sun Y., Brown C.T., Porras-Alfaro A., Kuske C.R., Tiedje J.M. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014, 42:D633-D642.
10. Degnan P.H., Ochman H. Illumina-based analysis of microbial community diversity. ISME J. 2012, 6:183-194.
11. Dietrich C., Köhler T., Brune A. The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 2014, 80:2261-2269.
12. Dröge S., Rachel R., Radek R., König H. Treponema isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes tabogae. Int. J. Syst. Evol. Microbiol. 2008, 58:1079-1083.
13. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
14. Edgar R.C., Haas B.J., Clemente J.C., Quince C., Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27:2194-2200.
15. Eggleton P., Tayasu I. Feeding groups, lifetypes and the global ecology of termites. Ecol. Res. 2001, 16:941-960.
16. Engel M., Grimaldi D., Krishna K. Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am. Mus. Novit. 2009, 1-27.
17. Ezaki T., Li N.A., Kawamura Y. The anaerobic Gram-positive cocci. Prokaryotes 2006, 795-808. Springer, New York. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
18. Felsenstein J. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
19. Garrity G.M., Bell J.A., Lilburn T.G. Taxonomic Outline of the Prokaryotes. Bergey's Manual of Systematic Bacteriology, Release 5 2004, Springer, New York.
20. 2-acetogenic spirochete from termite hindguts. Appl. Environ. Microbiol. 2004, 70:1307-1314.
21. Graber J.R., Leadbetter J.R., Breznak J.A. Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl. Environ. Microbiol. 2004, 70:1315-1320.
22. Griffen A.L., Beall C.J., Firestone N.D., Gross E.L., Difranco J.M., Hardman J.H., Vriesendorp B., Faust R.A., Janies D.A., Leys E.J. CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS ONE 2011, 6:e19051.
23. Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
24. He S., Ivanova N., Kirton E., Allgaier M., Bergin C., Scheffrahn R.H., Kyrpides N.C., Warnecke F., Tringe S.G., Hugenholtz P. Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS ONE 2013, 8:e61126.
25. Herlemann D.P.R., Geissinger O., Brune A. The Termite Group I phylum is highly diverse and widespread in the environment. Appl. Environ. Microbiol. 2007, 73:6682-6685.
26. Hongoh Y., Deevong P., Hattori S., Inoue T., Noda S., Noparatnaraporn N., Kudo T., Ohkuma M. Phylogenetic diversity, localization, and cell morphologies of members of the candidate phylum TG3 and a subphylum in the phylum Fibrobacteres, recently discovered bacterial groups dominant in termite guts. Appl. Environ. Microbiol. 2006, 72:6780-6788.
27. Hongoh Y., Ekpornprasit L., Inoue T., Moriya S., Trakulnaleamsai S., Ohkuma M., Noparatnaraporn N., Kudo T. Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol. Ecol. 2006, 15:505-516.
28. Hongoh Y., Ohkuma M., Kudo T. Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol. Ecol. 2003, 44:231-242.
29. Huang X.-F., Bakker M.G., Judd T.M., Reardon K.F., Vivanco J.M. Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb. Ecol. 2013, 65:531-536.
30. Hulsen T., de Vlieg J., Alkema W. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 2008, 9:488.
31. Husseneder C., Ho H.-Y., Blackwell M. Comparison of the bacterial symbiont composition of the formosan subterranean termite from its native and introduced range. Open Microbiol. J. 2010, 4:53-66.
32. Iida T. Symbiotic spirochetes in the termite hindgut: phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol. Ecol. 2000, 34:17-26.
33. Köhler T., Dietrich C., Scheffrahn R.H., Brune A. High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl. Environ. Microbiol. 2012, 78:4691-4701.
34. Lane D.J., Pace B., Olsen G.J., Stahl D.A., Sogin M.L., Pace N.R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. 1985, 82:6955-6959.
35. Lilburn T.G., Schmidt T.M., Breznak J.A. Phylogenetic diversity of termite gut spirochaetes. Environ. Microbiol. 1999, 1:331-345.
36. Lucey K.S., Leadbetter J.R. Catechol 2,3-dioxygenase and other meta-cleavage catabolic pathway genes in the anaerobic termite gut spirochete Treponema primitia. Mol. Ecol. 2014, 23:1531-1543.
37. Ludwig W., Bauer S.H., Bauer M., Held I., Kirchhof G., Schulze R., Huber I., Spring S., Hartmann A., Schleifer K.H. Detection and in situ identification of representatives of a widely distributed new bacterial phylum. FEMS Microbiol. Lett. 1997, 153:181-190.
38. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Buchner A., Lai T., Steppi S., Jobb G., Förster W., et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
39. Makonde H.M., Boga H.I., Osiemo Z., Mwirichia R., Mackenzie L.M., Göker M., Klenk H.-P. 16S-rRNA-based analysis of bacterial diversity in the gut of fungus-cultivating termites (Microtermes and Odontotermes species). Antonie Van Leeuwenhoek 2013, 104:869-883.
40. Mikaelyan A., Strassert J.F.H., Tokuda G., Brune A. The fibre-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (Nasutitermes spp.). Environ. Microbiol. 2014, 16:2711-2722.
41. Minkley N., Fujita A., Brune A., Kirchner W.H. Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insectes Soc. 2006, 53:339-344.
42. Newton I.L.G., Roeselers G. The effect of training set on the classification of honey bee gut microbiota using the Naïve Bayesian Classifier. BMC Microbiol. 2012, 12:221.
43. Ngugi D.K., Brune A. Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.). Environ. Microbiol. 2012, 14:860-871.
44. Noda S., Ohkuma M., Yamada A., Hongoh Y. Phylogenetic position and in situ identification of ectosymbiotic spirochetes on protists in the termite gut. Appl. Environ. Microbiol. 2003, 69:625-633.
45. Ohkuma M., Iida T., Kudo T. Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol. Lett. 1999, 181:123-129.
46. Otani S., Mikaelyan A., Nobre T., Hansen L.H., Koné N.A., Sørensen S.J., Aanen D.K., Boomsma J.J., Brune A., Poulsen M. Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 2014, 18:4631-4644.
47. Paul K., Nonoh J.O., Mikulski L., Brune A. Methanoplasmatales, Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl. Environ. Microbiol. 2012, 78:8245-8253.
48. Reid N.M., Addison S.L., West M.A., Lloyd-Jones G. The bacterial microbiota of Stolotermes ruficeps (Stolotermitidae), a phylogenetically basal termite endemic to New Zealand. FEMS Microbiol. Ecol. 2014, 90:678-688.
49. Santana R.H., Catão E.C.P., Lopes F.A.C., Constantino R., Barreto C.C., Krüger R.H. The gut microbiota of workers of the litter-feeding termite Syntermes wheeleri (Termitidae: Syntermitinae): archaeal, bacterial, and fungal communities. Microb. Ecol. 2015, 70:545-556.
50. Schauer C., Thompson C., Brune A. Pyrotag sequencing of the gut microbiota of the cockroach Shelfordella lateralis reveals a highly dynamic core but only limited effects of diet on community structure. PLOS ONE 2014, 9:1-8.
51. Schauer C., Thompson C.L., Brune A. The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 2012, 78:2758-2767.
52. 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., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75:7537-7541.
53. Seedorf H., Kittelmann S., Henderson G., Janssen P.H. RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. PeerJ 2014, 2:e494.
54. Shinzato N., Muramatsu M., Matsui T., Watanabe Y. Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Biosci. Biotechnol. Biochem. 2007, 71:906-915.
55. Sogin M.L., Morrison H.G., Huber J.A., Mark Welch D., Huse S.M., Neal P.R., Arrieta J.M., Herndl G.J. Microbial diversity in the deep sea and the underexplored rare biosphere. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12115-12120.
56. Sorokin D.Y., Gumerov V.M., Rakitin A.L., Beletsky A.V., Damsté J.S.S., Muyzer G., Mardanov A.V., Ravin N.V. Genome analysis of Chitinivibrio alkaliphilus gen. nov., sp. nov., a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum Termite Group 3. Environ. Microbiol. 2014, 16:1549-1565.
57. Strassert J.F.H., Köhler T., Wienemann T.H.G., Ikeda-Ohtsubo W., Faivre N., Franckenberg S., Plarre R., Radek R., Brune A. Candidatus Ancillula trichonymphae, a novel lineage of endosymbiotic Actinobacteria in termite gut flagellates of the genus Trichonympha. Environ. Microbiol. 2012, 14:3259-3270.
58. Thompson C.L., Vier R., Mikaelyan A., Wienemann T., Brune A. Candidatus Arthromitus revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environ. Microbiol. 2012, 14:1454-1465.
59. van Dijk E.L., Auger H., Jaszczyszyn Y., Thermes C. Ten years of next-generation sequencing technology. Trends Genet. 2014, 30:418-426.
60. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73:5261-5267.
61. Warnecke F., Luginbühl P., Ivanova N., Ghassemian M., Richardson T.H., Stege J.T., Cayouette M., McHardy A.C., Djordjevic G., Aboushadi N., Sorek R., Tringe S.G., Podar M., Martin H.G., Kunin V., Dalevi D., Madejska J., Kirton E., Platt D., Szeto E., Salamov A., Barry K., Mikhailova N., Kyrpides N.C., Matson E.G., Ottesen E.A., Zhang X., Hernández M., Murillo C., Acosta L.G., Rigoutsos I., Tamayo G., Green B.D., Chang C., Rubin E.M., Mathur E.J., Robertson D.E., Hugenholtz P., Leadbetter J.R. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450:560-565.
62. Werner J.J., Koren O., Hugenholtz P., DeSantis T.Z., Walters W.A., Caporaso J.G., Angenent L.T., Knight R., Ley R.E. Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J. 2012, 6:94-103.
63. Yang H., Schmitt-Wagner D., Stingl U., Brune A. Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ. Microbiol. 2005, 7:916-932.
64. Yarza P., Yilmaz P., Pruesse E., Glöckner F.O., Ludwig W., Schleifer K.-H., Whitman W.B., Euzéby J., Amann R., Rosselló-Móra R. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 2014, 12:635-645.
65. Yilmaz P., Parfrey L.W., Yarza P., Gerken J., Pruesse E., Quast C., Schweer T., Peplies J., Ludwig W., Glöckner F.O. The SILVA and All-species Living Tree Project (LTP) taxonomic frameworks. Nucleic Acids Res. 2014, 42:D643-D648.