Publikationsserver der Universitätsbibliothek Marburg
Titel:The bacterial gut microbiota of wood- and humus-feeding termites: Diazotrophic populations and compartment-specific response of bacterial communities to environmental factors
Autor:Wang, Wanyang
Weitere Beteiligte: Brune, Andreas (Prof. Dr.)
Veröffentlicht:2018
URI:https://archiv.ub.uni-marburg.de/diss/z2018/0091
URN: urn:nbn:de:hebis:04-z2018-00914
DOI: https://doi.org/10.17192/z2018.0091
DDC: Biowissenschaften, Biologie
Publikationsdatum:2018-02-28
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
gut microbiota, Darmbakterien, Termite, Termites, diazotroph, Diazotrophen

Summary:
The subject of this thesis is the influence of the microenvironment on the symbiosis between higher termites and their intestinal bacteria. The gut environmental factors pH, hydrogen partial pressure, redox potential and nitrogen pool size were measured. Bacterial gut community structure from each highly compartmentalized gut section was investigated. Furthermore, one specific function, nitrogen fixation, was comparatively analyzed in lower termites, higher termites and cockroaches. Hydrogen partial pressure, pH and redox potential in the gut compartments of humus- and soil-feeding termites were measured using microsensors. The size of the entire bacterial communities in each compartment was determined by 16S rRNA gene copies in qPCR. The diets of humus- and soil-feeders are nitrogen-rich, so the pool size of ammonia, nitrite and nitrate were also quantified by colorimetric assay. Higher termites have adapted to utilize diverse lignocellulosic diets in various stages of humification, like wood, humus and soil. The high alkalinity in the anterior hindgut of humus- and soil-feeding termites may play an important role in the digestion of proteins and polypeptides. Our comprehensive determination of physicochemical parameters reinforce the hypothesis that intestinal microenvironments are evolutionarily adapted to diet-related differences. The analysis of bacterial diversity by amplicon sequencing (Miseq) of 16S rRNA genes underscored that the community structure of intestinal bacteria in each gut section is influenced by multiple environmental factors like pH, hydrogen and host dietary substrate. The gut bacteria in homologous compartments of hindguts of humus- and soil-feeders showed similarity even when the hosts were from different subfamilies. In wood- and grass- feeding termites, dominating gut microbiota were from Actinobacteria, Fibrobacteres and Spirochaetes. On the other hand, abundant genera were from Bacteroidetes, Spirochaetes and Firmicutes in humus- and litter-feeding termites. This suggests that they make essential contributions to the digestive processes. Nitrogen supply should also influences the composition of the microbiota in termite guts, especially in wood-feeding termites, where diazotrophy is of major importance. From the study of nitrogen metabolism in different gut sections, the high concentrations of ammonia, nitrite and nitrate were found in the gut of humus- and soil-feeding termites not in wood-feeding termites. This phenomenon associated with the intake of the termites. For the wood feeders, they rely on a nitrogen-limiting diet with a high carbon to nitrogen ratio. They need some strategies to overcome this difficulty. Nitrogen fixation of symbiotic gut bacteria helps them in nitrogen nutrition supply. Quantification of nitrogen fixing populations was carried at DNA level by qPCR, using the nifH gene as a molecular marker. After normalized by 16S rRNA gene copy numbers, the ratio of nifH to 16S rRNA gene copy numbers was less than 0.15 in all termite species studied. Nevertheless, this surprisingly low proportion of diazotrophs is sufficient to account for the nitrogen fixation rate of the termites. It is supported by the nitrogen fixation ability measured by acetylene reduction assay of Treponema isolates from Zootermopsis angusticollis and live Zootermopsis sp. The bacterial symbionts of flagellate protists contribute to the nitrogen fixation in lower termites. Especially in Kalotermitidae, the abundant nifH genes which clustered with nifH genes from flagellate symbionts are consistent with the cospeciation of flagellates and lower termites. Nitrogen fixed by the endosymbiont can be converted to more valuable nitrogenous compounds such as amino acids and supplied directly for protein synthesis of the protist. This asset allows the protist to grow stably and independently, and ensures that the host termite maintains the essential cellulolytic protists. In wood-feeding higher termites, flagellates are lost and the diazotrophs in the gut link with fiber-associated bacteria. This was verified by comparative analysis of nifH genes in amplicon libraries and annotated metagenomes. Apart from flagellate symbionts, another interesting nifH subcluster is in Group IV. The verified diazotroph with only nif genes encoding Group IV nitrogenase revealed potential functional nifH subgroup in previously unfunctional Group IV. Endomicrobium cluster is abundant in Kalotermitidae, Termopsidae and Cryptoceridae. This is the first analysis of the diazotrophic communities in termite gut which take into account the potential diazotrophs with functional nifH in Group IV.

Bibliographie / References

  1. Cotta, M., and Forster, R. (2006). "The Family Lachnospiraceae, including the genera Butyrivibrio, Lachnospira and Roseburia," in The Prokaryotes (New York, NY: Springer US), 1002-1021. doi:10.1007/0-387-30744-3_35.
  2. Leschine, S., Paster, B. J., and Canale-Parola, E. (2006). "Free-living saccharolytic spirochetes: The genus Spirochaeta," in The Prokaryotes (New York, NY: Springer New York), 195-210. doi:10.1007/0-387-30747-8_7.
  3. Young, J. P. W. (2005). "The phylogeny and evolution of nitrogenases," in Genomes and Genomics of Nitrogen-fixing Organisms (Berlin/Heidelberg: Springer- Verlag), 221-241. doi:10.1007/1-4020-3054-1_14.
  4. Canale-Parola, E. (1992). "Free-living saccharolytic Spirochetes: the genus Spirochaeta," in The Prokaryotes (New York, NY: Springer New York), 3524- 3536. doi:10.1007/978-1-4757-2191-1_29.
  5. Bignell, D. E. (2016). "The role of symbionts in the evolution of termites and their rise to ecological dominance in the tropics," in The Mechanistic Benefits of Microbial Symbionts, ed. C. J. Hurst (Cham, Springer), 121-172. doi:10.1007/978-3-319-28068-4_6.
  6. Brune, A. (2012). "Microbial symbioses in the digestive tract of lower termites," in Beneficial Microorganisms in Multicellular Life Forms, eds. E. Rosenberg, U. Gophna (Berlin, Heidelberg: Springer Berlin Heidelberg), 3-25. doi:10.1007/978-3-642-21680-0_1.
  7. Brune, A. (2013). "Symbiotic associations between termites and prokaryotes," in The Prokaryotes: Prokaryotic Biology and Symbiotic Associations, eds. M. Dworkin, S. Falkow, E. Rosenberg, K. Schleifer, E. Stackebrandt (Dordrecht: Springer Netherlands) doi:10.1007/978-3-642-30194-0_20.
  8. Eggleton, P. (2011). "An introduction to termites: Biology, taxonomy and functional morphology," in Biology of Termites: A Modern Synthesis doi:10.1007/978-90- 481-3977-4_1.
  9. Bignell, D. E. (2010). "Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland," in Biology of Termites: a Modern Synthesis, eds. D. E. Bignell, Y. Roisin, and N. Lo (Dordrecht: Springer Netherlands), 375-412. doi:10.1007/978-90-481-3977-4_14.
  10. Ohkuma, M., and Brune, A. (2010). "Diversity, structure, and evolution of the termite gut microbial community," in Biology of Termites: a Modern Synthesis (Dordrecht: Springer Netherlands), 413-438. doi:10.1007/978-90-481-3977- 4_15.
  11. Brune, A., and Ohkuma, M. (2011). "Role of the termite gut microbiota in symbiotic digestion," in Biology of Termites: A Modern Synthesis doi:10.1007/978-90-481- 3977-4_16.
  12. Jones, D. T., and Eggleton, P. (2010). "Global biogeography of termites: a compilation of sources," in Biology of Termites: a Modern Synthesis (Dordrecht: Springer Netherlands), 477-498. doi:10.1007/978-90-481-3977-4_17.
  13. Brauman, A., Bignell, D. E., and Tayasu, I. (2000). "Soil-feeding termites: biology, microbial associations and digestive mechanisms," in Termites: Evolution, Sociality, Symbioses, Ecology, eds. Y. Abe, D. E. Bignell, T. Higashi (Dordrecht: Springer Netherlands), 233-259. doi:10.1007/978-94-017-3223-9_11.
  14. Inoue, T., Kitade, O., Yoshimura, T., and Yamaoka, I. (2000). "Symbiotic associations with protists," in Termites: Evolution, Sociality, Symbioses, Ecology (Dordrecht: Springer Netherlands), 275-288. doi:10.1007/978-94-017-3223- 9_13.
  15. Bignell, D. E., and Eggleton, P. (2000). "Termites in ecosystems," in Termites: Evolution, Sociality, Symbioses, Ecology, eds. Y. Abe, D. E. Bignell, T. Higashi (Dordrecht: Springer Netherlands), 363-387. doi:10.1007/978-94-017-3223- 9_17.
  16. Nalepa, C. A., and Bandi, C. (2000). "Characterizing the ancestors: paedomorphosis and termite evolution," in Termites: Evolution, Sociality, Symbioses, Ecology (Dordrecht: Springer Netherlands), 53-75. doi:10.1007/978-94-017-3223-9_3.
  17. Wood, T. G. (1988). Termites and the soil environment. Biol. Fertil. Soils 6, 228-236. doi:10.1007/BF00260819.
  18. Schulten, H.-R. (1995). The three-dimensional structure of humic substances and soil organic matter studied by computational analytical chemistry. Fresenius. J. Anal. Chem. 351, 62-73. doi:10.1007/BF00324293.
  19. Garnier-Sillam, E., and Harry, M. (1995). Distribution of humic compounds in mounds of some soil-feeding termite species of tropical rainforests: its influence on soil structure stability. Insectes Soc. 42, 167-185. doi:10.1007/BF01242453.
  20. Bignell, D. E., and Eggleton, P. (1995). On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insectes Soc. 42, 57-69. doi:10.1007/BF01245699.
  21. Kovoor, J. (1967). Le pH intestinal d'un Termite supérieur (Microcerotermes edentatus, Was., amitermitinae). Insectes Soc. 14, 157-160. doi:10.1007/BF02223265.
  22. Nalepa, C. A., Bignell, D. E., and Bandi, C. (2001). Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Soc. 48, 194-201. doi:10.1007/PL00001767.
  23. Hongoh, Y. (2011). Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell. Mol. Life Sci. 68, 1311-1325. doi:10.1007/s00018-011-0648-z.
  24. Ballor, N. R., Paulsen, I., and Leadbetter, J. R. (2012). Genomic analysis reveals multiple [FeFe] hydrogenases and hydrogen sensors encoded by Treponemes from the H2-rich termite gut. Microb. Ecol. 63, 282-294. doi:10.1007/s00248- 011-9922-8.
  25. Ballor, N. R., and Leadbetter, J. R. (2012). Analysis of extensive [FeFe] hydrogenase gene diversity within the gut microbiota of insects representing five families of Dictyoptera. Microb. Ecol. 63, 586-595. doi:10.1007/s00248-011-9941-5.
  26. Du, X., Li, X., Wang, Y., Peng, J., Hong, H., and Yang, H. (2012). Phylogenetic diversity of nitrogen fixation genes in the intestinal tract of Reticulitermes chinensis snyder. Curr. Microbiol. 65, 547-551. doi:10.1007/s00284-012-0185- 5.
  27. Ji, R., and Brune, A. (2001). Transformation and mineralization of 14 C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termite Cubitermes orthognathus. Biol. Fertil. Soils 33, 166-174. doi:10.1007/s003740000310.
  28. Thongaram, T., Hongoh, Y., Kosono, S., Ohkuma, M., Trakulnaleamsai, S., Noparatnaraporn, N., and Kudo, T. (2005). Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles 9, 229-238. doi:10.1007/s00792-005-0440-9.
  29. Ji, R., and Brune, A. (2006). Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78, 267-283. doi:10.1007/s10533-005-4279-z.
  30. Ngugi, D. K., Ji, R., and Brune, A. (2011). Nitrogen mineralization, denitrification, and nitrate ammonification by soil-feeding termites: A 15N-based approach. Biogeochemistry 103, 355-369. doi:10.1007/s10533-010-9478-6.
  31. Miltner, A., Bombach, P., Schmidt-Brücken, B., and Kästner, M. (2012). SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41-55. doi:10.1007/s10533-011-9658-z.
  32. Eutick, M. L., O'Brien, R. W., and Slaytor, M. (1976). Aerobic state of gut of Nasutitermes exitiosus and Coptotermes lacteus, high and low caste termites. J. Insect Physiol. 22, 1377-1380. doi:10.1016/0022-1910(76)90161-X.
  33. Bignell, D. E., and Anderson, J. M. (1980). Determination of pH and oxygen status in the guts of lower and higher termites. J. Insect Physiol. 26, 183-188. doi:10.1016/0022-1910(80)90079-7.
  34. Veivers, P. C., O'Brien, R. W., and Slaytor, M. (1980). The redox state of the gut of termites. J. Insect Physiol. 26, 75-77. doi:10.1016/0022-1910(80)90112-2.
  35. Bentley, B. L. (1984). Nitrogen fixation in termites: Fate of newly fixed nitrogen. J. Insect Physiol. 30, 653-655. doi:10.1016/0022-1910(84)90050-7.
  36. Anklin-Mühlemann, R., Bignell, D. E., Veivers, P. C., Leuthold, R. H., and Slaytor, M. (1995). Morphological, microbiological and biochemical studies of the gut flora in the fungus-growing termite Macrotermes subhyalinus. J. Insect Physiol. 41, 929-940. doi:10.1016/0022-1910(95)00062-Y.
  37. Taguchi, F., Hasegawa, K., Saito-Taki, T., and Hara, K. (1996). Simultaneous production of xylanase and hydrogen using xylan in batch culture of Clostridium sp. strain X53. J. Ferment. Bioeng. 81, 178-180. doi:10.1016/0922- 338X(96)87600-8.
  38. Liu, H., and Beckenbach, A. T. (1992). Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol. Phylogenet. Evol. 1, 41-52. doi:10.1016/1055-7903(92)90034-E.
  39. Rubio, L. M., and Ludden, P. W. (2002). "The Gene Products of the nif Regulon," in Nitrogen Fixation at the Millennium ed. G.J. Leigh (Elsevier), 101-136. doi:10.1016/B978-044450965-9/50004-5.
  40. Doolittle, M., Raina, A., Lax, A., and Boopathy, R. (2008). Presence of nitrogen fixing Klebsiella pneumoniae in the gut of the Formosan subterranean termite (Coptotermes formosanus). Bioresour. Technol. doi:10.1016/j.biortech.2007.07.013.
  41. Rawls, J. F., Mahowald, M. A., Ley, R. E., and Gordon, J. I. (2006). Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423-33. doi:10.1016/j.cell.2006.08.043.
  42. 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.doi:10.1016/j.ejop.2012.06.002.
  43. Physicochemical conditions and metal ion profiles in the gut of the fungus- growing termite Odontotermes formosanus. J. Insect Physiol. 58, 1368-1375. doi:10.1016/J.JINSPHYS.2012.07.012.
  44. Ji, R., and Brune, A. (2005). Digestion of peptidic residues in humic substances by an alkali-stable and humic-acid-tolerant proteolytic activity in the gut of soil- feeding termites. Soil Biol. Biochem. 37, 1648-1655. doi:10.1016/j.soilbio.2005.01.026.
  45. Inward, D. J. G., Vogler, A. P., and Eggleton, P. (2007). A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol. Phylogenet. Evol. 44, 953-967. doi:10.1016/j.ympev.2007.05.014.
  46. Brune, A., and Kühl, M. (1996). pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J. Insect Physiol. 42, 1121-1127. doi:10.1016/S0022-1910(96)00036-4.
  47. Ji, R., Kappler, A., and Brune, A. (2000). Transformation and mineralization of synthetic 14C-labeled humic model compounds by soil-feeding termites. Soil Biol. Biochem. 32, 1281-1291. doi:10.1016/S0038-0717(00)00046-8.
  48. Kappler, A., and Brune, A. (2002). Dynamics of redox potential and changes in redox state of iron and humic acids during gut passage in soil-feeding termites (Cubitermes spp.). Soil Biol. Biochem. 34, 221-227. doi:10.1016/S0038- 0717(01)00176-6.
  49. Knicker, H., Schmidt, M. W. I., and Kögel-Knabner, I. (2000). Nature of organic nitrogen in fine particle size separates of sandy soils of highly industrialized areas as revealed by NMR spectroscopy. Soil Biol. Biochem. 32, 241-252. doi:10.1016/S0038-0717(99)00154-6.
  50. Watanabe, K., Kodama, Y., and Harayama, S. (2001). Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting. J. Microbiol. Methods 44, 253-262. doi:10.1016/S0167- 7012(01)00220-2.
  51. Brune, A. (1998). Termite guts: the world's smallest bioreactors. Trends Biotechnol. 16, 16-21. doi:10.1016/S0167-7799(97)01151-7.
  52. Hethener, P., Brauman, A., and Garcia, J. L. (1992). Clostridium termitidis sp. nov., a cellulolytic bacterium from the gut of the wood-feeding termite, Nasutitermes lujae. Syst. Appl. Microbiol. 15, 52-58. doi:10.1016/S0723-2020(11)80138-4.
  53. Kappler, A., and Brune, A. (1999). Influence of gut alkalinity and oxygen status on mobilization and size-class distribution of humic acids in the hindgut of soil- feeding termites. Appl. Soil Ecol. 13, 219-229. doi:10.1016/S0929- 1393(99)00035-9.
  54. Breznak, John A., Winston J. Brill, James W. Mertins, and H. C. C. (1973). Nitrogen fixation in termites. Nature 244, 577-580. doi:10.1038/244577a0.
  55. Desai, M. S., and Brune, A. (2011). Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J. Adv. online Publ. 6, 1302-1313. doi:10.1038/ismej.2011.194.
  56. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565. doi:10.1038/nature06269.
  57. Brune, A. (2014). Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168-180. doi:10.1038/nrmicro3182.
  58. Barelli, C., Albanese, D., Donati, C., Pindo, M., Dallago, C., Rovero, F., Cavalieri, D., Tuohy, K. M., Hauffe, H. C., and Filippo, C. D. (2015). Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci. Rep. 5, 14862. doi:10.1038/srep14862.
  59. Donovan, S. E., Eggleton, P., and Bignell, D. E. (2001). Gut content analysis and a new feeding group classification of termites. Ecol. Entomol. 26, 356-366. doi:10.1046/j.1365-2311.2001.00342.x.
  60. Eggleton, P., and Tayasu, I. (2001). Feeding groups, lifetypes and the global ecology of termites. Ecol. Res. 16, 941-960. doi:10.1046/j.1440-1703.2001.00444.x.
  61. De, B. L., and Conacher, A. (1990). The role of termites and ants in soil modification -a review. Aust. J. Soil Res. 28, 55-93. doi:10.1071/SR9900055.
  62. Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., and Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A. 102, 11070-5. doi:10.1073/pnas.0504978102.
  63. Ohkuma, M., Noda, S., Hattori, S., Iida, T., Yuki, M., Starns, D., Inoue, J., Darby, A., C., and Hongoh, Y. (2015). Acetogenesis from H2 plus CO2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist. PNAS 112, 10224-10230. doi:10.1073/pnas.1423979112.
  64. Aanen, D. K., Eggleton, P., Rouland-Lefevre, C., Guldberg-Froslev, T., Rosendahl, S., and Boomsma, J. J. (2002). The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl. Acad. Sci. U. S. A. 99, 14887- 14892. doi:10.1073/pnas.222313099.
  65. d'Ettorre, P. (2017). "Distributed agency in ants," in Distributed Agency, ed. N. J. Enfield and Paul Kockelman (Oxford Scholarship Online), 131-137. doi:10.1093/acprof:oso/9780190457204.001.0001.
  66. Paradis, E., Claude, J., and Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. doi:10.1093/bioinformatics/btg412.
  67. Mikaelyan, A., Meuser, K., and Brune, A. (2016). Microenvironmental heterogeneity of gut compartments drives bacterial community structure in wood-and humus- feeding higher termites. FEMS Microbiology Ecology, 93. doi:10.1093/femsec/fiw210.
  68. Raymond, J., Siefert, J. L., Staples, C. R., and Blankenship, R. E. (2004). The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541-54. doi:10.1093/molbev/msh047.
  69. French, J. R., Turner, G. L., and Bradbury, J. F. (1976). Nitrogen fixation by bacteria from the hindgut of termites. J. Gen. Microbiol. 96, 202-206. doi:10.1099/00221287-95-2-202.
  70. Ueki, A., Akasaka, H., Suzuki, D., and Ueki, K. (2006). Paludibacter propionicigenes gen. nov., sp. nov., a novel strictly anaerobic, gram-negative, propionate- producing bacterium isolated from plant residue in irrigated rice-field soil in Japan. Int. J. Syst. Evol. Microbiol. doi:10.1099/ijs.0.63896-0.
  71. Nielsen, M. B., Kjeldsen, K. U., and Ingvorsen, K. (2006). Desulfitibacter alkalitolerans gen. nov., sp. nov., an anaerobic, alkalitolerant, sulfite-reducing bacterium isolated from a district heating plant. Int. J. Syst. Evol. Microbiol. doi:10.1099/ijs.0.64356-0.
  72. Mikaelyan, A., Strassert, J. F. H., Tokuda, G., and Brune, A. (2014). The fibre- associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites ( N asutitermes spp.). Environ. Microbiol. 16, 2711-2722. doi:10.1111/1462-2920.12425.
  73. Okwakol, M. J. N. (1980). Estimation of soil and organic matter consumption by termites of the genus Cubitermes. Afr. J. Ecol. 18, 127-131. doi:10.1111/j.1365- 2028.1980.tb00276.x.
  74. Sleaford, F., Bignell, D. E., and Eggleton, P. (1996). A pilot analysis of gut contents in termites from the Mbalmayo Forest Reserve, Cameroon. Ecol. Entomol. 21, 279-288. doi:10.1111/j.1365-2311.1996.tb01245.x.
  75. Swift, R. S., and Posner, A. M. (1972). Autoxidation of humic acid under alkaline conditions. J. Soil Sci. 23, 381-393. doi:10.1111/j.1365-2389.1972.tb01669.x.
  76. Hongoh, Y., Ekpornprasit, L., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., Noparatnaraporn, N., and Kudo, T. (2005). Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol. Ecol. 15, 505-516. doi:10.1111/j.1365- 294X.2005.02795.x.
  77. Yamada, A., Inoue, T., Noda, S., Hongoh, Y., and Ohkuma, M. (2007). Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol. Ecol. 16, 3768-77. doi:10.1111/j.1365- 294X.2007.03326.x.
  78. Ikeda-Ohtsubo, W., and Brune, A. (2009). Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and "Candidatus Endomicrobium trichonymphae". Mol. Ecol. 18, 332-42. doi:10.1111/j.1365- 294X.2008.04029.x.
  79. Pester, M., and Brune, A. (2006). Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ. Microbiol. 8, 1261-1270. doi:10.1111/j.1462- 2920.2006.01020.x.
  80. Ngugi, D. K., 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. doi:10.1111/j.1462-2920.2011.02648.x.
  81. Thompson, C. L., 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. doi:10.1111/j.1462-2920.2012.02731.x.
  82. Otani, S., Mikaelyan, A., Nobre, T., Hansen, L. H., Koné, N. A., Sørensen, S. J., Aanen, D. K., Boomsma, J. J., Brune, A., and Poulsen, M. (2014). Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23. doi:10.1111/mec.12874.
  83. Mikaelyan, A., Dietrich, C., Köhler, T., Poulsen, M., Sillam-Dussès, D., and Brune, A. (2015a). Diet is the primary determinant of bacterial community structure in the guts of higher termites. Mol. Ecol. 24, 5284-5295. doi:10.1111/mec.13376.
  84. Ruby, E., Henderson, B., and McFall-Ngai, M. (2004). Microbiology. We get by with a little help from our (little) friends. Science 303, 1305-1307. doi:10.1126/science.1094662.
  85. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Toh, H., Taylor, T. D., Kudo, T., akaki, Y., Toyoda, A., Hattori, M., and Ohkuma, M. (2008). Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322, 1108-1109. doi:10.1126/science.1165578.
  86. Benemann, J. R. (1973). Nitrogen fixation in termites. Science 181, 164-165. doi:10.1126/science.181.4095.164
  87. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-7. doi:10.1128/AEM.00062-07.
  88. Tai, V., Carpenter, K. J., Weber, P. K., Nalepa, C. A., Perlman, S. J., and Keeling, P. J. (2016). Genome evolution and nitrogen-fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches. Appl. Environ. Microbiol. 82, 4682-4695., AEM.00611-16-. doi:10.1128/AEM.00611-16.
  89. Köhler, T., Dietrich, C., Scheffrahn, R. H., 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, 4691-701. doi:10.1128/AEM.00683-12.
  90. Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., and Schloss, P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112-5120. doi:10.1128/AEM.01043- 13.
  91. Paul, K., Nonoh, J. O., 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. doi:10.1128/AEM.02193-12.
  92. Fall, S., Hamelin, J., Ndiaye, F., Assigbetse, K., Aragno, M., Chotte, J. L., and Brauman, A. (2007). Differences between bacterial communities in the gut of a soil-feeding termite (Cubitermes niokoloensis) and its mounds. Appl. Environ. Microbiol. 73:5199-5208 doi:10.1128/AEM.02616-06.
  93. Dietrich, C., Kohler, T., and Brune, A. (2014). The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80, 2261-2269. doi:10.1128/AEM.04206-13.
  94. Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl. Environ. Microbiol. 78, 1544-1555. doi:10.1128/AEM.06466-11.
  95. Leaphart, A. B., and Lovell, C. R. (2001). Recovery and analysis of formyltetrahydrofolate synthetase gene sequences from natural populations of acetogenic bacteria. Appl. Environ. Microbiol. 67, 1392-1395. doi:10.1128/AEM.67.3.1392-1395.2001.
  96. Egert, M., Wagner, B., Lemke, T., Brune, A., and Friedrich, M. W. (2003). Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl. Environ. Microbiol. 69, 6659-6668. doi:10.1128/AEM.69.11.6659-6668.2003.
  97. Graber, J. R., Leadbetter, J. R., and Breznak, J. A. (2004). the first Spirochetes isolated from termite guts. Appl. Environ. Microbiol. 70, 1315-1320. doi:10.1128/AEM.70.3.1315-1320.2004.
  98. Lozupone, C., and Knight, R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235. doi:10.1128/AEM.71.12.8228-8235.2005.
  99. Brune, A., and Dietrich, C. (2015). The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu. Rev. Microbiol 69, 145-66. doi:10.1146/annurev-micro-092412-155715.
  100. Liu, Y., Yang, H., Zhang, X., Xiao, Y., Guo, X., and Liu, X. (2016). Genomic analysis unravels reduced inorganic sulfur compound oxidation of heterotrophic acidophilic Acidicaldus sp. strain DX-1. Biomed Res. Int. doi:10.1155/2016/8137012.
  101. Noda, S., Hongoh, Y., Sato, T., and Ohkuma, M. (2009). BMC Evolutionary biology complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites. BMC Evol. Biol. 9. doi:10.1186/1471-2148-9-158.
  102. Rossmassler, K., Dietrich, C., Thompson, C., Mikaelyan, A., Nonoh, J. O., Scheffrahn, R. H., Sillam-Dussès, D., and Brune, A. (2015). Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood-or soil-feeding higher termites. Microbiome 3, 56. doi:10.1186/s40168-015-0118-1.
  103. Krishna, K., Grimaldi, D. A., Krishna, V., and Engel, M. S. (2013). Treatise on the Isoptera of the World. Bull. Am. Museum Nat. Hist. 377, 1-202. doi:10.1206/377.6.
  104. Deevong, P., Hongoh, Y., Inoue, T., Trakulnaleamsai, S., Kudo, T., Noparatnaraporn, N., Ohkuma, M. (2006). Effect of temporal sample preservation on the molecular study of a complex microbial community in the gut of the termite Microcerotermes sp. Microbes Environ. 21, 78-85. doi:10.1264/jsme2.21.78.
  105. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2 -Approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490. doi:10.1371/journal.pone.0009490.
  106. Noda, S., Mantini, C., Meloni, D., Inoue, J. I., Kitade, O., Viscogliosi, E., and Ohkuma, M. (2012). Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α. PLoS One. doi:10.1371/journal.pone.0029938.
  107. Sylvester-Bradley, R., Bandeira, A. G., Oliveira, L. A. de, Sylvester-Bradley, R., Bandeira, A. G., and Oliveira, L. A. de (1978). Fixação de nitrogênio (redução de acetileno) em cupins (Insecta: Isoptera) da Amazônia Central. Acta Amaz. 8, 621-627. doi:10.1590/1809-43921978084621.
  108. Austin, J. W., Szalanski, A. L., and Cabrera, B. J. (2004). Phylogenetic analysis of the subterranean termite family Rhinotermitidae (Isoptera) by using the mitochondrial cytochrome oxidase II Gene. Ann. Entomol. Soc. Am. 97, 548- 555. doi:10.1603/0013-8746(2004)097[0548:PAOTST]2.0.CO;2.
  109. Gontijo, T. A., and Domingos, D. J. (1991). Guild distribution of some termites from Cerrado Vegetation in south-east Brazil. J. Trop. Ecol. 7, 523-529. doi:10.2307/2559217.
  110. Makonde, H. M., Boga, H. I., Osiemo, Z., Mwirichia, R., Mackenzie, L. M., Göker, M., and Klenk, H. P. (2013). 16S-rRNA-based analysis of bacterial diversity in the gut of fungus-cultivating termites (Microtermes and Odontotermes species).
  111. Yoneda, T., Yoda, K., and Kira, T. (1977). Accumulation and decomposition of big wood litter in Pasoh Forest, West Malaysia. Jap. J. Ecol. 27, 53-60.
  112. Slaytor, M., Veivers, P., and Lo, N. (1997). Aerobic and anaerobic metabolism in the higher termite Nasutitermes walkeri (Hill). Insect Biochem. Mol. Biol. 27, 291- 303.
  113. Kuhnigk, Thomas, Jürgen Branke, Daniel Krekeler, Heribert Cypionka, and H. K. (1996). A feasible role of sulfate-reducing bacteria in the termite gut. Syst. Appl. Microbiol. 19, 139-149.
  114. Whelan, S., and Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach.
  115. Li, H., Dietrich, C., Zhu, N., Mikaelyan, A., Ma, B., Pi, R., Liu, Y., Yang, M., Brune, A. (2016). Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus. Environ.
  116. Gaby, J. C., and Buckley, D. H. (2011). A global census of nitrogenase diversity.
  117. Rieu-Lesme, F., Morvan, B., Collins, M. D., Fonty, G., and Willems, A. (1996). A new H2/CO2-using acetogenic bacterium from the rumen: description of Ruminococcus schinkii sp. nov. FEMS Microbiol. Lett. 140, 281-6.
  118. Nonoh, J. O. (2013). Archaeal diversity and community structure in the compartmented gut of higher termites. [dissertation] Philipps-Universität Marburg.
  119. Chen, J., Bittinger, K., Charlson, E. S., Hoffmann, C., Lewis, J., Wu, G. D, Collman, R. G., Bushman, F. D., and Li, H. (2012). Associating microbiome composition with environmental covariates using generalized UniFrac distances.
  120. Anderson, J. M., and Bignell, D. E. (1980). Bacteria in the food, gut contents and faeces of the litter-feeding millipede glomeris marginata (villers). Soil Biol.
  121. Breznak, J. A., and Canale-Parola, E. (1973). Biology of nonpathogenic, host- associated Spirochetes. CRC Critical Reviews in Microbiology 2, 457-489.
  122. Breznak, J. A., and Canale-Parola, E. (1973). Biology of nonpathogenic, host- associated Spirochetes. CRC Critical Reviews in Microbiology 2, 457-489.
  123. Mikaelyan, A., Köhler, T., Lampert, N., Rohland, J., Boga, H., Meuser, K., and Brune, A. (2015b). Classifying the bacterial gut microbiota of termites and cockroaches: A curated phylogenetic reference database (DictDb). Syst. Appl.
  124. Schulz, M., Slaytor, M., Hogan, M., and O'brien, R. (1986). Components of cellulase from the higher termite, Nasutitermes walkeri. Insect Biochem. 16, 929-932.
  125. Noda, S., Ohkuma, M., Usami, R., Horikoshi, K., and Kudo, T. (1999). Culture- independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis.
  126. Ohkuma, M., Noda, S., Usami, R., Horikoshi, K., and Kudo, T. (1996). Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus. Appl. Environ. Microbiol. 62, 2747-2752.
  127. Breznak, J. A. (2000). "Ecology of prokaryotic microbes in the guts of wood-and litter-feeding termites," in Termites: Evolution, Sociality, Symbioses, Ecology eds T. Abe, D. E. Bignell and M. Higashi (Dordrecht: Springer Netherlands), 209-231.
  128. Bourguignon, T., Šobotník, J., Lepoint, Gi., Martin, J.-M., Hardyt, O. J., Dejean, A., Roisin, Y. (2011). Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios. Ecol.
  129. Noirot, C. (1992). "From wood-to humus-feeding: an important trend in termite evolution," in Biology and evolution of social insects, ed J. Billen (Belgium, Leuven University Press), 107-119.
  130. Bignell, D. E., and Roisin Y, Lo N. (2011). "Global biogeography of termites," in Biology of Termites: A Modern Synthesis, eds. D. E. Bignell, Y. Roisin, and N.
  131. Piccolo, A. (1996). "Humus and soil conservation," In Humic substances in terrestrial ecosystems. ed. A. Piccolo (Amsterdam, Elsevier), 225-264.
  132. Stevenson, F. J. (1994). Humus chemistry : genesis, composition, reactions. 2nd ed. (New York, John Wiley & Sons).
  133. Ebert, A., and Brune, A. (1997). Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 63, 4039-4046.
  134. Schmitt-Wagner, D., and Brune, A. (1999). Hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl. Environ. Microbiol. 65, 4490-4496.
  135. Breznak, J. A., and Pankratz, H. S. (1977). In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki].
  136. König, H., and Varma, A. (Ajit) (2006). Intestinal microorganisms of termites and other invertebrates. Springer.
  137. Taguchi, F., Dan Chang, J., Mizukami, N., Saito-taki, T., Hasegawa, K., and Morimoto, M. (1993). Isolation of a hydrogen-producing bacterium, Clostridium beijerinckii strain AM21B, from termites. Canadian Journal of Microbiology 39, 726-730.
  138. Tholen, A., and Brune, A. (1999). Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl. Environ. Microbiol. 65, 4497-505.
  139. Kudo, T., Ohkuma, M., Moriya, S., Noda, S., and Ohtoko, K. (1998). Molecular phylogenetic identification of the intestinal anaerobic microbial community in the hindgut of the termite, Reticulitermes speratus, without cultivation. Extremophiles 2, 155-161.
  140. Oksanen, J. (2015). Multivariate analysis of ecological communities in R: vegan tutorial. University Oulu, Finland
  141. Wright, P. A. (1995). Nitrogen excretion: three end products, many physiological roles. J. Exp. Biol. 198, 272-81.
  142. Lilburn, T. G., Kim, K. S., Ostrom, N. E., Byzek, K. R., Leadbetter, J. R., & Breznak, J. A. (2001). Nitrogen fixation by symbiotic and free-living Spirochetes. Science 292, 2495-2498.
  143. Noda, S., Ohkuma, M., and Kudo, T. (2002). Nitrogen fixation genes expressed in the symbiotic microbial community in the gut of the termite Coptotermes formosanus. Microbes and Environments. 17, 139-143.
  144. Potrikus, C. J., and Breznak, J. A. (1977). Nitrogen-fixing Enterobacter agglomerans isolated from guts of wood-eating termites. Appl. Environ. Microbiol. 33, 392- 399.
  145. Rohrmann, G. F., and Rossman, A. Y. (1980). Nutrient strategies of Macrotermes ukuzii (Isoptera: Termitidae). Pedobiologia 20, 61-73.
  146. Occurrence of rhizobia in the gut of the higher termite Nasutitermes nigriceps.
  147. Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.). Appl. Environ.
  148. Ohkuma, M., Noda, S., and 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.
  149. Paster, B. J., Dewhirst, F. E., Cooke, S. M., Fussing, V., Poulsen, L. K., and Breznak, J. A. (1996). Phylogeny of not-yet-cultured spirochetes from termite guts. Appl. Environ. Microbiol. 62, 347-352.
  150. Honigberg, B. M. (1970). "Protozoa associated with termites and their role in digestion," in Biology of termites, ed. K. Krishna and F. M. Weesner (New York: Academic Press), 2, 1-36.
  151. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R- project.rg/.
  152. Cataldo, D. A., Maroon, M., Schrader, L. E., and Youngs, V. L. (1975). Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid.
  153. Prusch, R. D. (1972). Secretion of NH4Cl by the hindgut of Sarcophaga bullata larva.
  154. Bignell, D. (1994). "Soil-feeding and gut morphology in higher termites," in Nourishment Evol. insect Soc., eds. J. H. Hunt and C. A. alepa (Boulder, Westview Press), 131-158.
  155. Lo, N., and Eggleton, P. (2011). "Termite phylogenetics and co-cladogenesis with symbionts," in Biology of Termites: A Modern Synthesis, eds. D. Bignell, Y.
  156. John A. HoltA, M. L. (2000). "Termites and soil properties," in Termites: Evolution, Sociality, Symbioses, Ecology, eds. Y. Abe, D. E. Bignell, T. Higashi (Dordrecht: Springer Netherlands), 389-407.
  157. Bignell, D. E. (2006). "Termites as soil engineers and soil processors," in Intestinal Microorgansims of Termites and Other Invertebrates, eds. König, H., and Varma, A (Berlin/Heidelberg: Springer-Verlag), 183-220.
  158. Noirot, C. (2001). The gut of termites (Isoptera) comparative anatomy systematics, phylogeny,. II. -higher termites (Termitidae). Ann. Soc. Entomol. Fr 37, 431- 471.
  159. Noirot, C. (1995). The gut of termites (isoptera): Comparative anatomy, systematics, phylogeny. I: Lower termites. Ann. la Société Entomol. Fr. 31, 197-226.
  160. Matsumoto, T. (1976). The role of termites in an equatorial rain forest ecosystem of west Malaysia I. population density, biomass, carbon, nitrogen and calorific content and respiration rate. Oecologia (Berl.) 22, 153-178.
  161. Brune, A., Emerson, D., and Breznak, J. A. (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, 2681-7.
  162. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Natl. Acad.
  163. Ji, R. (2000). Transformation and mineralization of organic matter by soil-feeding termites. [dissertation]. [Konstanz]: University of Chicago
  164. Täyasu, I., A. Sugimoto, E. Wada, and T. A. (1994). Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81, 229-231.

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