Ecological and evolutionary drivers of microbial community structure in termite guts

Presumably descending from subsocial cockroaches 150 million years ago, termites are an order of social insects that gained the ability to digest wood through the acquisition of cellulolytic flagellates. These eukaryotic protists fill up the bulk of the hindgut volume and are the major habitat of...

Ausführliche Beschreibung

Gespeichert in:
1. Verfasser: Dietrich, Carsten
Beteiligte: Brune, Andreas (Prof. Dr.) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Sprache:Englisch
Veröffentlicht: Philipps-Universität Marburg 2015
Biologie
Ausgabe:http://dx.doi.org/10.17192/z2015.0344
Schlagworte:
Online Zugang:PDF-Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!

1. http://archiv.ub.uni-marburg.de/diss/z2008/0074


2. Rosenthal AZ, Matson EG, Eldar A and Leadbetter JR (2011). RNA-seq reveals cooperative metabolic interactions between two termite-gut spirochete species in co-culture. ISME J. 5:1133–1142.


3. Eddy SR (2011). Accelerated profile HMM searches. PLoS Comp. Biol. 7:e1002195.


4. Wu M, Chatterji S and Eisen JA (2012). Accounting for alignment uncertainty in phylogenomics. PLoS One (1):e30288.


5. Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, Nielsen R and Willerslev E (2007). The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2: e197.


6. Qian ZQ (2014). The complete mitogenome of the dampwood termite Zootermopsis nevadensis (Insecta: Isoptera: Termopsidae). doi:10.3109/19401736.2014.936419.


7. Rawls JF, Mahowald MA, Ley RE and Gordon JI (2006). Reciprocal Gut Microbiota Transplants from Zebrafish and Mice to Germ-free Recipients Reveal Host Habitat Selection. Cell 127:423–433.


8. Douglas AE (2014). The molecular basis of bacterial-insect symbiosis. J. Mol. Biol. 426:3830–3837.


9. Wu M and Scott AJ (2012). Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinf. 28(7):1033–1034.


10. Katoh K and Standley DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780.


11. Hahn C, Bachmann L and Chevreux B (2013). Reconstructing mitochondrial genomes directly from genomic next- generation sequencing reads—a baiting and iterative mapping approach. Nucl. Acids Res. 41:e129.


12. Douglas AE (2015). Multiorganismal insects: Diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34.


13. Bulmer MS, Denier D, Velenovsky J, Hamilton C (2012). A common antifungal defense strategy in Cryptocercus woodroaches and termites. Insect. Soc. 59:469–478.


14. Otani S, Mikaelyan A, Nobre T, Hansen LH, Koné NA, Sørensen SJ, Aanen DK, Boomsma JJ, Brune A and Poulsen M (2014). Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23:4631–4644.


15. Cameron SL, Lo N, Bourguignon T, Svenson GJ and Evans TA (2012). A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relationships and molecular synapomorphies define major clades. Mol. Phylogenet. Evol. 65(1):163-73.


16. Bourguignon T, Lo N, Cameron SL, Šobotník J, Hayashi Y, Shigenobu S, Watanabe D, Roisin Y, Miura T and Evans TA (2015). The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol. Biol. Evol. 32:406–421.


17. Noda S, Mantini C, Meloni D, Inoue J-I, Kitade O, Viscogliosi E, Ohkuma M (2012). Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1 . PLoS ONE 7:e29938.


18. Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn B, Hugenholtz P (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8:e1000546.


19. Rahman NA, Parks DH, Willner DL, Engelbrektson AL, Goffredi SK, Warncke F, Scheffrahn H and Hugenholtz P (2015). A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. Microbiome (in press)


20. Boucias DG, Cai Y, Sun Y, Lietze V-U, Sen R, Raychoudhury R and Scharf ME (2013). The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol. Ecol. 22:1836–1853.


21. Ngugi DK and Brune A (2012). Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.). Environ. Microbiol. 14:860–871.


22. Prestat E, David MM, Hultman J, Ta ş N, Lamendella R, Dvornik J, Mackelprang R, Myrold DD, Jumpponen A, Tringe SG, Holman E, Mavromatis K, Jansson JK (2014). FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus. Nucleic Acids Res. 2014 42:e145.


23. Grassi B and Sandias A (1897). The constitution and development of the society of termites: observations on their habits; with appendices on the parasitic protozoa of Termitidae, and on the Embiidae. Quart. J. Microsc. Sci. 39: 245-332.


24. Li H*, Dietrich C*, Zhu N, Mikaelyan A, Ma B, Pi R, Liu Y, Yang M, Brune A und Mo J (submitted). Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus.


25. Nalepa CA (2011). Altricial development in wood-feeding cockroaches: the key antecedent of termite eusociality, pp. 69–95. In Bignell DE, Roisin Y, Lo N (eds.), Biology of Termites: A Modern Synthesis. Springer, Dordrecht.


26. Kuenen JG (2008). Anammox bacteria: from discovery to application. Nat. Rev. Microbiol. 6:320–326.


27. Awards and Honors Among the best 10% of his diploma year 2011 IMPRS—MIC scholarship for doctoral research 2011–2014


28. Sakamoto M and Ohkuma M (2013). Bacteroides reticulotermitis sp. nov., isolated from the gut of the subterranean termite (Reticulitermes speratus). Int. J. Syst. Evol. Microbiol. 63:691–695.


29. Strassert JFH, Köhler T, Wienemann THG, Ikeda-Ohtsubo W, Faivre N, Franckenberg S, Plarre R, Radek R and Brune, A (2012). 'Candidatus Ancillula trichonymphae', a novel lineage of endosymbiotic Actinobacteria in termite gut flagellates of the genus Trichonympha. Environ. Microbiol. 14:3259–3270.


30. Thompson CL, Vier R, Mikaelyan A, Wienemann T and Brune A (2012). 'Candidatus Arthromitus' revised: Segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environ. Microbiol. 14:1454–1465.


31. Guichard P, Desfosses A, Maheshwari A, Hachet V, Dietrich C und Brune, A, Ishikawa T, Sachse, C und Gönczy P (2012). Cartwheel architecture of Trichonympha basal body. Science 337:553–554.


32. Tamschick S and Radek R (2013). Colonization of termite hindgut walls by oxymonad flagellates and prokaryotes in Incisitermes tabogae, I. marginipennis and Reticulitermes flavipes. Eur. J. Protistol. 49:1–14.


33. He S, Ivanova N, Kirton E, Allgaier M, Bergin C, Scheffrahn RH, Kyrpides NC, Warnecke F, Tringe SG and Hugenholtz P (2013). Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS ONE 8:e61126.


34. van Orsouw NJ, Hogers RCJ, Janssen A et al. (2007). Complexity reduction of polymorphic sequences (CRoPSTM): A novel approach for large-scale polymorphism discovery in complex genomes. PLoS One 2: e1172.


35. Noda S, Kitade O, Inoue T, Kawai M, Kanuka M, Hiroshima K, Hongoh Y, Constantino R, Uys V, Zhong J Kudo T and Ohkuma M (2007). Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol. Ecol. 16:1257–1266.


36. Ikeda-Ohtsubo W und Brune A (2009). Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae'. Mol. Ecol. 18:332–342.


37. Curriculum vitae Basic information Name Carsten Dietrich Date of Birth 6th of July, 1985


38. Mikaelyan A, Lampert N, Köhler T, Rohland J, Boga H, Meuser K and Brune A (2015). DictDb: an expanded reference database for the highly resolved classification of the bacterial gut microbiota of termites and cockroaches. Submitted manusript.


39. Ohkuma M and Brune A (2011). Diversity, structure, and evolution of the termite gut microbial community, pp. 413–438. In Bignell DE, Roisin Y, Lo N (eds.), Biology of Termites: A Modern Synthesis. Springer, Dordrecht.


40. Colman DR, Toolson EC and Takacs-Vesbach CD (2012). Do diet and taxonomy influence insect gut bacterial communities? Mol. Ecol. 21:5124–5137.


41. Carlsen T, Aas AB, Lindner D, Vralstad T, Schumacher T and Kauserud H (2012). Don't make a mista(g)ke: is tag switching an overlooked source of error in amplicon pyrosequencing studies? Fungal Ecol. 5: 747-749.


42. Carlton JM, Hirt RP, Silva JC, et al. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315: 207-212.


43. Yang YJ, Zhang N, Ji SQ, Lan X, Zhang KD, Shen YL, Li FL, Ni JF (2014). Dysgonomonas macrotermitis sp. nov., isolated from the hindgut of a fungus-growing termite. Int. J. Syst. Evol. Microbiol. 64:2956–2961.


44. Breznak JA (2000). Ecology of prokaryotic microbes in the guts of wood-and litter-feeding termites, pp. 209–231. In Abe T, Bignell DE and Higashi M (eds.). Termites: Evolution, Sociality, Symbiosis, Ecology, vol. 1. Kluwer Academic Publishers, Dordrecht.


45. Messer AC and Lee MJ (1989). Effect of chemical treatments on methane emission by the hindgut microbiota in the termite Zootermopsis angusticollis. Microb. Ecol. 18: 275-284.


46. Brune A (2012). Endomicrobia: intracellular symbionts of termite gut flagellates. J. Endocytobiosis Cell Res. 23:11–15.


47. Zheng H, Dietrich C, Radek R and Brune A (submitted). Endomicrobium proavitum, the first isolate of Endomicrobia class. nov. (phylum Elusimicrobia) – an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase.


48. Mira A and Moran NA (2002). Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44: 137-143.


49. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R and Gordon JI (2008). Evolution of Mammals and Their Gut Microbes. Science 320:1647–1651.


50. Glenn TC (2011). Field guide to next-generation DNA sequencers. Mol. Ecol. Resour. 11: 759-769.


51. Thomson N, Bentley S, Holden M and Parkhill J (2003). Fitting the niche by genomic adaptation. Nat. Rev. Microbiol. 1:92–93.


52. Kirby H (1932). Flagellates of the genus Trichonympha in termites. Univ. Calif. Publ. Zool. 37: 349-476.


53. Genome analysis of Chitinivibrio alkaliphilus gen. nov., sp. nov., a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum TG3. Environ. Microbiol. 16:1549–1565.


54. Wernegreen JJ (2002). Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3: 850-861.


55. Wertz JT, Kim E, Breznak JA, Schmidt TM and Rodrigues JLM (2012). Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colotermitum gen. nov., sp. nov. reveals microaerophily and nitrogen fixation genes. Appl. Environ. Microbiol. 78:1544–1555.


56. Moran NA, McCutcheon JP and Nakabachi A (2008). Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42: 165-190.


57. Place of Birth Erfurt, Germany Marital Status Single Nationality German Higher education Diploma in Environmental engineering, THM Giessen 2011


58. Moreira D, von der Heyden S, Bass D, López-García P, Chao E and Cavalier-Smith T (2007). Global eukaryote phylogeny: Combined small-and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol. Phylogenet. Evol. 44: 255-266.


59. Thongaram T, Kosono S, Ohkuma M, Hongoh Y, Kitada M, Yoshinaka T, Trakulnaleamsai S, Noparatnaraporn N and Kudo T (2003). Gut of higher termites as a niche for alkaliphiles as shown by culture-based and culture-independent studies. Microb. Environ. 18:152–159.


60. Day A (2012). heatmap.plus – heatmap with more sensible behavior. R package version 1.3. Available at http://cran.r- project.org/web/packages/heatmap.plus/index.html.


61. Köhler T, Dietrich C, Scheffrahn RH and Brune A (2012). High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher hermites (Nasutitermes spp.).


62. Cleveland LR (1949). Hormone-induced sexual cycles of flagellates. I. gametogenesis, fertilization, and meiosis in Trichonympha. J. Morphol. 85: 197-295.


63. Wenzel M, Radek R, Brugerolle G and König H (2003). Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur. J. Protistol. 39:11–24.


64. Tholen A and Brune A (2000). Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environ. Microbiol. 2:436–449.


65. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, Uchiyama H and Tanaka H (2007). Influence of feed components on symbiotic bacterial community structure in the gut of the wood-feeding higher termite Nasutitermes takasagoensis. Biosci. Biotechnol. Biochem. 71:1244–1251.


66. Tanaka H, Aoyagi H, Shina S, Dodo Y, Yoshimura T, Nakamura R, Uchiyama H (2006). Influence of the diet components on the symbiotic microorganisms community in hindgut of Coptotermes formosanus Shiraki. Appl. Microbiol. Biotechnol. 71:907–917.


67. Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Vongkaluang C, Noparatnaraporn N and Kudo T (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.


68. Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N and 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.


69. Riesenfeld CS, Schloss PD and Handelsman J (2004). Metagenomics: genomic analysis of microbial communities. Ann. Rev. Genet. 38:525–552.


70. Brune A (2010). Methanogens in the digestive tract of termites, pp. 81–100. In Hackstein JHP (ed.), (Endo)symbiotic Methanogenic Archaea. Springer, Heidelberg.


71. Brune A (2011). Microbial symbioses in the digestive tract of lower termites, p. 3-25. In E. Rosenberg, and U. Gophna (ed.), Beneficial Microorganisms in Multicellular Life Forms. Springer, Heidelberg.


72. Cameron SL and Whiting MF (2007). Mitochondrial genomic comparisons of the subterranean termites from the Genus Reticulitermes (Insecta: Isoptera: Rhinotermitidae). Genome 50(2): 188-202.


73. MITOS: Improved de novo Metazoan Mitochondrial Genome Annotation. Mol. Phylogenet. Evol. 69(2):313-319


74. Gile GH, Carpenter KJ, James ER, Scheffrahn RH and Keeling PJ (2013). Morphology and Molecular Phylogeny of Staurojoenina mulleri sp. nov. (Trichonymphida, Parabasalia) from the Hindgut of the Kalotermitid Neotermes jouteli. J. Euk. Microbiol. 60:203–213.


75. Carpenter KJ, Chow L and Keeling PJ (2009). Morphology, phylogeny, and diversity of Trichonympha (Parabasalia: Hypermastigida) of the wood-feeding cockroach Cryptocercus punctulatus. J. Eukaryotic Microbiol. 56: 305-313.


76. Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R and Brune A (2015). New mode of energy metabolism in the seventh order of methanogens as indicated by comparative genome analysis of "Candidatus Methanoplasma termitum". Appl. Environ. Microbiol. 81:1338–52.


77. Slaytor M and Chappell DJ (1994). Nitrogen metabolism in termites. Comp. Biochem. Physiol. 107:1–10.


78. Köhler T, Stingl U, Meuser K and Brune A (2008). Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ. Microbiol. 10:1260–1270.


79. PhD Student at the Max Planck Institute Marburg, Germany 2011–2015


80. Ikeda-Ohtsubo W, Desai M, Stingl U and Brune A (2007). Phylogenetic diversity of 'Endomicrobia' and their specific affiliation with termite gut flagellates. Microbiology 153: 3458-3465.


81. Radek R, Strassert JFH, Krüger J, Meuser K, Scheffrahn RH and Brune A (2014). Phylogeny and ultrastructure of Oxymonas jouteli, a rostellum-free species, and Opisthomitus longiflagellatus sp. nov., oxymonadid flagellates from the gut of Neotermes jouteli. Protist 165:384–399


82. Ikeda-Ohtsubo W, Faivre N and Brune A (2010). Putatively free-living 'Endomicrobia' – ancestors of the intracellular symbionts of termite gut flagellates? Environ. Microbiol. Rep. 2:554–559.


83. Quality insurance at the Pharmaserv GmbH & Co. KG, Giessen 2009–2010


84. Brune A and Ohkuma M (2011). Role of the termite gut microbiota in symbiotic digestion, p. 439-475. In Bignell DE, Roisin Y, and Lo N (eds.), Biology of Termites: A Modern Synthesis. Springer, Dordrecht.


85. Mikaelyan A, Dietrich C, Köhler T, Meuser K, Sillam-Dussès D und Brune A (submitted). Dietary and phylogenetic determinants of bacterial gut community structure in higher termites.


86. Dietrich C*, Nonoh J*, Lang K, Mikulski L, Meuser K, Köhler T, Boga HI, Ngugi DK, Sillam-Dussès S und Brune A (submitted). Habitat selection and vertical inheritance drive archaeal community structure in arthropod guts.


87. Tholen A, Pester M and Brune A (2007). Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol. Ecol. 2:303-312.


88. Tai V, James ER, Perlman SJ and Keeling PJ (2013). Single-cell DNA carcoding using sequences from the small subunit rRNA and internal transcribed spacer region identifies new species of Trichonympha and Trichomitopsis from the hindgut of the Termite Zootermopsis angusticollis. PLoS ONE 8:e58728.


89. Desai MS, Strassert JFH, Meuser K, Hertel H, Ikeda-Ohtsubo W, Radek R and Brune A (2010). Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ. Microbiol. 12:2120–2132.


90. Koidzumi M (1921). Studies on the intestinal protozoa found in the termites of Japan. Parasitology 13: 235-305.


91. Kofoid CA and Swezy (1919a). Studies on the parasites of the termites III. On Trichonympha campanula sp. nov. Univ. Calif. Publ. Zool. 20: 41-98.


92. Kofoid CA and Swezy O (1919b). Studies on the parasites of the termites IV. On Leidyopsis sphaerica gen. nov., sp. nov. Univ. Calif. Publ. Zool. 20: 99-116.


93. Brune A (2006). Symbiotic associations between termites and prokaryotes, pp. 439–474. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds.), The Prokaryotes, 3rd ed., Volume 1: Symbiotic associations, Biotechnology, Applied Microbiology, vol. 1. Springer, New York.


94. Brune A (2014). Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12:168–180.


95. Breznak JA and Leadbetter JR (2006). Termite gut spirochetes, pp. 318–329. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds.), The Prokaryotes, 3rd ed., Volume 7: Proteobacteria: Delta and Epsilon Subclasses. Deeply Rooting Bacteria, vol. 7. Springer, New York.


96. Brune A (1998). Termite guts: the world's smallest bioreactors. Trends Biotechnol. 16:16–21.


97. Reid NM, Addison SL, West MA, Lloyd-Jones G (2014). The bacterial microbiota of Stolotermes ruficeps (Stolotermitidae), a phylogenetically basal termite endemic to New Zealand. FEMS Microbiol. Ecol. 90:678–688.


98. Tokuda G, Isagawa H and Sugio K (2012). The complete mitogenome of the Formosan termite, Coptotermes formosanus Shiraki. Insect. Soc. 59:17-24.


99. Dietrich C und Brune A (2014). The complete mitogenomes of six higher termite species reconstructed from metagenomic datasets (Cornitermes sp., Cubitermes ugandensis, Microcerotermes parvus, Nasutitermes corniger, Neocapritermes taracua, and Termes hospes). Mitochondr. DNA. Dec 4:1-2.


100. Trager W (1934). The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol. Bull. 66: 182-190.


101. Mikaelyan A, Strassert JFH, Tokuda G and Brune A (2014). The fiber-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (Nasutitermes spp.). Environ. Microbiol. 16:2711–2722.


102. Engel P and Moran NA (2013). The gut microbiota of insects -diversity in structure and function. FEMS Microbiol. Rev. 37:699–735.


103. Leidy J (1881). The parasites of the termites. J. Acad. Nat. Sci. Philadelphia. 2nd Ser. 8: 425-477.


104. Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ and Keeling PJ (2014). The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Appl. Environ. Microbiol. 81:1059–70


105. Brune A und Dietrich C (2015). The termite gut microbiota: Digesting the diversity in the light of ecology and evolution. Ann. Rev. Microbiol. 69 (release in october 2015).


106. Hongoh Y (2011). Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell. Mol. Life Sci. 68:1311–1325.


107. James ER, Tai V, Scheffrahn RH and Keeling PJ (2013). Trichonympha burlesquei from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. Int. J. Syst. Evol. Microbiol. 63:3873–3876.


108. Garcıá-Martı́nezMartı́nez J, Acinas SG, Antón AI and Rodriguez-Valera F (1999). Use of the 16S-23S ribosomal genes spacer region in studies of prokaryotic diversity. J. Microbiol. Methods 36: 55-64.


109. Huang X-F, Bakker MG, Judd TM, Reardon KF and Vivanco JM (2013). Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb. Ecol. 65:531–536.


110. Klass K-D, Nalepa CA and Lo N (2008). Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus vs. Parasphaeria boleiriana. Mol. Phylogenet. Evol. 46:809–817.


111. Edgar RC (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.


112. Bauer E, Lampert N, Mikaelyan A, Köhler T, Maekawa K and Brune A (2015). Physicochemical conditions, metabolites, and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae). FEMS Microbiol. Ecol. (in Press).


113. Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M and Ohkuma M (2008b). Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109.


114. Sato T, Hongoh Y Noda S, Hattori S, Ui S and Ohkuma M (2009). Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ. Microbiol. 11:1007–1015.


115. Ohkuma M, Noda S, Hongoh Y, Nalepa CA and Inoue T (2009). Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc. R. Soc. B 276: 239-245.


116. Inoue J, Noda S, Hongoh Y and Ohkuma M (2008). Identification of endosymbiotic methanogen and ectosymbiotic spirochetes of gut protists of the termite Coptotermes formosanus. Microb. Environ. 23:94–97.


117. Yamada A, Inoue T, Noda Y, Hongoh H and Ohkuma M (2007). Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol. Ecol. 16:3768-3777.


118. Ohkuma M, Sato T, Noda S, Ui S, Kudo T and Hongoh Y (2007). The candidate phylum 'Termite Group 1' of bacteria: phylogenetic diversity, distribution, and endosymbiont members of various gut flagellated protists. FEMS Microbiol. Ecol. 60: 467-476.


119. Nakajima H, Hongoh Y, Noda S, Yoshida Y, Usami R, Kudo T and Ohkuma M (2006). Phylogenetic and morphological diversity of Bacteroidales members associated with the gut wall of termites. Biosci. Biotechnol. Biochem. 70:211–218.


120. Hongoh Y and Ohkuma M (2010). Termite gut flagellates and their methanogenic and eubacterial symbionts, pp. 55–79. In Hackstein JHP (ed.), (Endo)symbiotic Methanogenic Archaea, Springer, Heidelberg.


121. Sato T, Kuwahara H, Fujita K, Noda S, Kihara K, Yamada A, Ohkuma M and Hongoh Y (2014). Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut. ISME J. 8:1008– 1019.


122. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P and Leadbetter JR (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nat. 450:560–565.


123. Genomic analysis of Elusimicrobium minutum the first cultivated representative of the phylum Elusimicrobia (formerly Termite Group 1). Appl. Environ. Microbiol. 75:2841–2849.


124. Wu YW, Tang YH, Tringe SG, Simmons BA and Singer SW (2014). MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbi. 2:26.


125. Poulsen M, Hu H, Li C, Chen Z, Xu L, Otani S, Nygaard S, Nobre T, Klaubauf S, Schindler PM, Hauser F, Pan H, Yang Z, Sonnenberg ASM, de Beer AW, Zhang Y, Wingfield MJ, Grimmelikhuijzen CJP, de Vries RP, Korb J, Aanen DK, Wang J, Boomsma JJ and Zhang G (2014). Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc. Natl. Acad. Sci. USA 111:14500–14505.


126. Stingl U, Radek R, Yang H and Brune A (2005). "Endomicrobia": cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl. Environ. Microbiol. 71: 1473-1479.


127. Hugenholtz P (2002). Exploring prokaryotic diversity in the genomic era. Genome Biol. 3:S0003.


128. Sawada H, Takeuchi T and Matsuda I (1997). Comparative analysis of Pseudomonas syringae pv. actinidiae and pv. phaseolicola based on phaseolotoxin-resistant ornithine carbamoyltransferase gene (argK) and 16S-23S rRNA intergenic spacer sequences. Appl. Environ. Microbiol. 63: 282-288.


129. Schmitt-Wagner D, Friedrich MW, Wagner B and Brune A (2003). Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.). Appl. Environ. Microbiol. 69:6007–6017.


130. Wertz JT and Breznak JA (2007). Stenoxybacter acetivorans gen. nov., sp. nov., an acetate-oxidizing obligate microaerophile among diverse O2-consuming bacteria from termite guts. Appl. Environ. Microbiol. 73:6819–6828.


131. Wertz JT and Breznak JA (2007). Physiological ecology of Stenoxybacter acetivorans, an obligate microaerophile in termite guts. Appl. Environ. Microbiol. 73:6829-6841.


132. Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M and Ohkuma M (2008a). Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc. Natl. Acad. Sci. USA 105:5555–5560.


133. Inward D, Beccaloni G and Eggleton P (2007). Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Lett. 3:331-335.


134. Suen G, Weimer PJ, Stevenson DM, Aylward FO, Boyum J, Deneke J, Drinkwater C, Ivanova NN, Mikhailova N, Chertkov O, Goodwin LA, Currie CR, Mead D and Brumm PJ (2011). The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS One 6(4):e18814.


135. Yamada T, Letunic I, Okuda S, Kanehisa M and Bork P (2011). iPath2.0: interactive pathway explorer. Nucl. Res. 39:W412–415.


136. Pester M, Schleper C and Wagner M (2011). The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14:300–306.


137. Sabree ZL, Huang CY, Arakawa G, Tokuda G, Lo N, Watanabe H and Moran NA (2012). Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis. Appl. Environ. Microbiol. 78:204–210.


138. Schauer C, Thompson CL and Brune A (2012). The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 78:2758–2767.


139. Köhler T, Dietrich C, Scheffrahn RH and Brune A (2012). 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. 78:4691–4701.


140. Desai MS and Brune A (2012). Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry- wood termites. ISME J. 6:1302–1313.


141. Yin Y, Mao X, Yang JC, Chen X, Mao F and Xu Y (2012). dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucl. Res. 40:445–451.


142. Zhang X and Leadbetter JR (2012). Evidence for cascades of perturbation and adaptation in the metabolic genes of higher termite gut symbionts. mBio 3:e00223–12.


143. Hamady M, Walker JJ, Harris JK, Gold NJ and Knight R (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5: 235-237.


144. Paul, K, Nonoh JO, Mikulski L and Brune A (2012). "Methanoplasmatales," Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl. Environ. Microbiol. 78:8245–8253.


145. Tai V, James ER, Perlman SJ and Keeling PJ (2013). Single-cell DNA barcoding using sequences from the small subunit rRNA and internal transcribed spacer region identifies new species of Trichonympha and Trichomitopsis from the hindgut of the termite Zootermopsis angusticollis. PLoS One 8: e58728.


146. Meyer BH, Peyfoon E, Dietrich C, Hitchen P, Panico M, Morris HR, Dell A und Albers SV (2013). Agl16, a thermophilic glycosyltransferase mediating the last step of N-glycan biosynthesis in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. J. Bacteriol. 195:2177–2186.


147. Rosenthal AZ, Zhang X, Lucey KS, Ottesen EA, Trivedi V, Choi HMT, Pierce NA and Leadbetter JR (2013). Localizing transcripts to single cells suggests an important role of uncultured Deltaproteobacteria in the termite gut hydrogen economy. Proc. Natl. Acad. Sci. USA 110:16163–16168


148. Ludwig W, Strunk O, Westram R, et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32: 1363-1371.


149. Morris RL and Schmidt TM (2013). Shallow breathing: bacterial life at low O2. Nat. Rev. Microbiol. 11:205-212.


150. Stamatakis A (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.


151. Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, Rey FE, Smith MI, Simon GM, Scheffrahn RH, Woebken D, Spormann AM, Van Treuren W, Ursell LK, Pirrung M, Robbins-Pianka A, Cantarel BL, Lombard V, Henrissat B, Knight R and Gordon JI (2014). Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159:254– 266


152. Ohkuma M, Noda S, Kudo T (1999). Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol. 65:4926–4934.


153. Friedrich MW, Schmitt-Wagner D, Lueders T and 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.


154. Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, Chen Z, et al. (2014). Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636


155. Schauer C, Thompson CL and Brune A (2014). 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 9:e85861.