Microbial Ecology

, Volume 70, Issue 2, pp 545–556 | Cite as

The Gut Microbiota of Workers of the Litter-Feeding Termite Syntermes wheeleri (Termitidae: Syntermitinae): Archaeal, Bacterial, and Fungal Communities

  • Renata Henrique Santana
  • Elisa Caldeira Pires Catão
  • Fabyano Alvares Cardoso Lopes
  • Reginaldo Constantino
  • Cristine Chaves Barreto
  • Ricardo Henrique KrügerEmail author
Host Microbe Interactions


The gut microbiota of termites allows them to thrive on a variety of different materials such as wood, litter, and soil. For that reason, they play important roles in the decomposition of biomass in diverse biomes. This function is essential in the savanna, where litter-feeding termites are one of the few invertebrates active during the dry season. In this study, we describe the gut microbiota of workers (third and fourth instars) of the species Syntermes wheeleri, a litter-feeding termite from the Brazilian savanna. Results of 16S and 18S ribosomal RNA (rRNA) gene-targeted pyrosequencing using primers sets specific to each domain have revealed its bacterial, archaeal, and fungal diversities. Firmicutes accounted for more than half of the operational taxonomic units of the Bacteria domain. The most abundant fungal species were from the class Dothideomycetes of the phylum Ascomycota. The methanogenic orders Methanobacteriales, Methanosarcinales, and Methanomicrobiales of the phylum Euryarchaeota accounted for the greatest part of the Archaea detected in this termite. A comparison of the gut microbiota of the two instars revealed a difference in operational taxonomic unit (OTU) abundance but not in species richness. This description of the whole gut microbiota represents the first study to evaluate relationships among bacteria, archaea, fungi, and host in S. wheeleri.


Termite Gut microbiota Brazilian savanna Pyrosequencing 16S rRNA gene 18S rRNA gene 



This work was supported by grants from the Federal District Research Support Foundation (FAPDF) and National Council for Scientific and Technological Development (CNPq). We thank Dr. Andreas Brune for sharing the DictDb v. 2.3 database.

Supplementary material

248_2015_581_Fig4_ESM.gif (27 kb)
Figure S1

Relative abundance of OTUs from Firmicutes phylum at family level. (GIF 26 kb)

248_2015_581_MOESM1_ESM.tif (444 kb)
High resolution image (TIFF 444 kb)
248_2015_581_Fig5_ESM.gif (54 kb)
Figure .S2

Abundance of microorganisms differed significantly between the third- and fourth-instar workers of Syntermes wheeleri: (a) the bacterial phylum TG3, (b) the archaeal order Methanobacteriales; and (c) fungal classes. STAMP analysis using two-sided Fisher’s exact test with Bonferroni multiple test correction and effect size filter (ratio of proportions < 2.0). (GIF 53 kb)

248_2015_581_MOESM2_ESM.tif (322 kb)
High resolution image (TIFF 321 kb)
248_2015_581_MOESM3_ESM.xlsx (34 kb)
ESM 1 (XLSX 34 kb)


  1. 1.
    Bignell D (2006) Termites as Soil Engineers and Soil Processors. In: König H, Varma A (eds) Intestinal Microorganisms of Termites and Other Invertebrates, vol 6. Soil Biology. Springer Berlin, Heidelberg, pp 183–220. doi: 10.1007/3-540-28185-1_8 CrossRefGoogle Scholar
  2. 2.
    Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell D (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur J Soil Biol 47:215–222. doi: 10.1016/j.ejsobi.2011.05.005 CrossRefGoogle Scholar
  3. 3.
    Ngugi DK, 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 PubMedCrossRefGoogle Scholar
  4. 4.
    Ngugi DK, Ji R, Brune A (2011) Nitrogen mineralization, denitrification, and nitrate ammonification by soil-feeding termites: a N-15-based approach. Biogeochemistry 103:355–369. doi: 10.1007/s10533-010-9478-6 CrossRefGoogle Scholar
  5. 5.
    Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180. doi: 10.1038/nrmicro3182 PubMedCrossRefGoogle Scholar
  6. 6.
    Rouland-Lefèvre C, Bignell DE (2002) Cultivation of symbiotic fungi by termites of the subfamily Macrotermitinae. In: Seckbach J (ed) Symbiosis, vol 4. Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer Netherlands, pp 731–756. doi: 10.1007/0-306-48173-1_46
  7. 7.
    Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. doi: 10.1146/annurev.ento.49.061802.123416 PubMedCrossRefGoogle Scholar
  8. 8.
    Scharf ME, Tartar A (2008) Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod Biorefin 2:540–552. doi: 10.1002/bbb.107 CrossRefGoogle Scholar
  9. 9.
    Dietrich C, Kohler T, Brune A (2014) The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol. doi: 10.1128/AEM. 04206-13 Google Scholar
  10. 10.
    Otani S, Mikaelyan A, Nobre T, Hansen LH, Kone NA, Sorensen SJ, Aanen DK, Boomsma JJ, Brune A, Poulsen M (2014) Identifying the core microbial community in the gut of fungus-growing termites. Mol Ecol. doi: 10.1111/mec.12874 PubMedGoogle Scholar
  11. 11.
    Ohkuma M, Brune A (2011) Diversity, structure, and evolution of the termite gut microbial community. In: Bignell DE, Roisin Y, Lo N (eds) Biology of Termites: a Modern Synthesis. Springer Netherlands, pp 413–438. doi: 10.1007/978-90-481-3977-4_15
  12. 12.
    Constantino R (2005) Padrões de diversidade e endemismo de térmitas no bioma Cerrado. In: Scariot AO, Silva JCS, Felfili JM (eds) Biodiversidade. Ecologia e Conservação do Cerrado. Ministério do Meio Ambiente, Brasilia, pp 319–333Google Scholar
  13. 13.
    He S, Ivanova N, Kirton E, Allgaier M, Bergin C, Scheffrahn RH, Kyrpides NC, Warnecke F, Tringe SG, Hugenholtz P (2013) Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS One 8:e61126. doi: 10.1371/journal.pone.0061126 PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Liu N, Zhang L, Zhou H, Zhang M, Yan X, Wang Q, Long Y, Xie L, Wang S, Huang Y, Zhou Z (2013) Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). Plos One 8:e69184. doi: 10.1371/journal.pone.0069184
  15. 15.
    Warnecke F, Luginbuhl 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, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565, PubMedCrossRefGoogle Scholar
  16. 16.
    Hongoh Y (2010) Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 74:1145–1151PubMedCrossRefGoogle Scholar
  17. 17.
    Constantino R (1995) Revision of the neotropical termite genus Syntermes Holmgren (Isoptera: Termitidae). Univ Kans Sci Bull 55:455–518Google Scholar
  18. 18.
    Emerson AE (1945) The neotropical genus Syntermes (Isoptera: Termitidae). Bull Am Mus Nat Hist 83:427–472Google Scholar
  19. 19.
    Liu N, Yan X, Zhang M, Xie L, Wang Q, Huang Y, Zhou X, Wang S, Zhou Z (2011) Microbiome of fungus-growing termites: a new reservoir for lignocellulase genes. Appl Environ Microbiol 77:48–56. doi: 10.1128/aem. 01521-10 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Armougom F, Raoult D (2009) Exploring microbial diversity using 16S rRNA high-throughput methods. J Comput Sci Syst Biol 2:74–92CrossRefGoogle Scholar
  21. 21.
    Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555PubMedCrossRefGoogle Scholar
  22. 22.
    Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621PubMedCentralPubMedGoogle Scholar
  23. 23.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth.f.303 PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669. doi: 10.1038/nmeth0910-668b PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi: 10.1093/bioinformatics/btq461 PubMedCrossRefGoogle Scholar
  26. 26.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr381 PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi: 10.1093/nar/gkm864 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. doi: 10.1093/nar/gks1219 PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA Gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. doi: 10.1128/aem. 03006-05 PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Köhler T, Dietrich C, Scheffrahn RH, 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. doi: 10.1128/aem. 00683-12 PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. doi: 10.1093/bioinformatics/btp636 PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi: 10.1128/AEM. 01541-09 PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi: 10.1128/AEM. 00062-07 PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Chao A, Shen T-J (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ Ecol Stat 10:429–443. doi: 10.1023/A:1026096204727 CrossRefGoogle Scholar
  35. 35.
    Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270. doi: 10.2307/4615964 Google Scholar
  36. 36.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264. doi: 10.1093/biomet/40.3-4.237 CrossRefGoogle Scholar
  37. 37.
    Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721. doi: 10.1093/bioinformatics/btq041 PubMedCrossRefGoogle Scholar
  38. 38.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: Community Ecology Package. R package version 2.2–1.
  39. 39.
    Wickham H (2009) ggplot2: elegant graphics for data analysis. Use R. Springer New York. doi: 10.1007/978-0-387-98141-3
  40. 40.
    Brune A (2011) Methanogens in the Digestive Tract of Termites (Endo)symbiotic Methanogenic Archaea. In: Hackstein JHP (ed) Microbiology Monographs, 19th edn. Springer Berlin, Heidelberg, pp 81–100. doi: 10.1007/978-3-642-13615-3_6 Google Scholar
  41. 41.
    Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269. doi: 10.1016/S1369-5274(00)00087-4 PubMedCrossRefGoogle Scholar
  42. 42.
    Schmitt-Wagner D, Friedrich MW, Wagner B, 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 69:6007–6017PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Brune A (2013) Symbiotic associations between termites and prokaryotes. In: Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer Berlin Heidelberg, pp 545–577. doi: 10.1007/978-3-642-30194-0_20
  44. 44.
    Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A (2003) Axial dynamics, stability, and interspecies similarity of bacterial community structure in the highly compartmentalized gut of soil-feeding termites (Cubitermes spp.). Appl Environ Microbiol 69:6018–6024PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Thongaram T, Hongoh Y, Kosono S, Ohkuma M, Trakulnaleamsai S, Noparatnaraporn N, Kudo T (2005) Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles: Life Under Extreme Cond 9:229–238. doi: 10.1007/s00792-005-0440-9 CrossRefGoogle Scholar
  46. 46.
    Bugg TDH, Ahmad M, Hardiman EM, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400. doi: 10.1016/j.copbio.2010.10.009 PubMedCrossRefGoogle Scholar
  47. 47.
    Thompson CL, Vier R, Mikaelyan A, Wienemann T, 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 PubMedCrossRefGoogle Scholar
  48. 48.
    Mikaelyan A, Strassert JFH, Tokuda G, Brune A (2014) The fibre-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (Nasutitermes spp.). Environ Microbiol 16:2711–2722. doi: 10.1111/1462-2920.12425 CrossRefGoogle Scholar
  49. 49.
    Schmitt-Wagner D, 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 65:4490–4496PubMedCentralPubMedGoogle Scholar
  50. 50.
    Paul K, Nonoh JO, Mikulski L, Brune A (2012) ‘Methanoplasmatales’: Thermoplasmatales-related archaea in termite guts and other environments are the seventh order of methanogens. Appl Environ Microbiol. doi: 10.1128/aem. 02193-12 Google Scholar
  51. 51.
    Friedrich MW, Schmitt-Wagner D, Lueders T, 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 67:4880–4890PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Prillinger H, Messner R, König H, Bauer R, Lopandic K, Molnar O, Dangel P, Weigang F, Kirisits T, Nakase T, Sigler L (1996) Yeasts associated with termites: a phenotypic and genotypic characterization and use of coevolution for dating evolutionary radiations in asco- and basidiomycetes. Syst Appl Microbiol 19:265–283. doi: 10.1016/S0723-2020(96)80053-1 CrossRefGoogle Scholar
  53. 53.
    Mathew GM, Ju YM, Lai CY, Mathew DC, Huang CC (2012) Microbial community analysis in the termite gut and fungus comb of Odontotermes formosanus: the implication of Bacillus as mutualists. Fems Microbiol Ecol 79:504–517. doi: 10.1111/j.1574-6941.2011.01232.x PubMedCrossRefGoogle Scholar
  54. 54.
    Matos I, Cassa-Barbosa LA, Galvao RDM, Nunes-Silva CG, Astolfi S (2014) Isolation, taxonomic identification and investigation of the biotechnological potential of wilt-type Meyerozyma guilliermondii associated with Amazonian termites able to ferment D-xylose. Biosci J 30:260–266Google Scholar
  55. 55.
    Vega FE, Dowd PF (2005) The role of yeasts as insect endosymbionts. In: Vega FE, Blackwell M (eds) Insect–Fungal Associations. Oxford University Press, New YorkGoogle Scholar
  56. 56.
    Geiser DM, Gueidan C, Miadlikowska J, Lutzoni F, Kauff F, Hofstetter V, Fraker E, Schoch CL, Tibell L, Untereiner WA, Aptroot A (2006) Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98:1053–1064. doi: 10.3852/mycologia.98.6.1053 PubMedCrossRefGoogle Scholar
  57. 57.
    Schoch CL, Crous PW, Groenewald JZ, Boehm EW, Burgess TI, de Gruyter J, de Hoog GS, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya T, Huhndorf SM, Hyde KD, Jones EB, Kohlmeyer J, Kruys A, Li YM, Lucking R, Lumbsch HT, Marvanova L, Mbatchou JS, McVay AH, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, Owensby CA, Phillips AJ, Phongpaichit S, Pointing SB, Pujade-Renaud V, Raja HA, Plata ER, Robbertse B, Ruibal C, Sakayaroj J, Sano T, Selbmann L, Shearer CA, Shirouzu T, Slippers B, Suetrong S, Tanaka K, Volkmann-Kohlmeyer B, Wingfield MJ, Wood AR, Woudenberg JH, Yonezawa H, Zhang Y, Spatafora JW (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15S10. doi: 10.3114/sim.2009.64.01 PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Wang Z, Binder M, Schoch CL, Johnston PR, Spatafora JW, Hibbett DS (2006) Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): a nuclear rDNA phylogeny. Phylogenet Evol 41:295–312. doi: 10.1016/j.ympev.2006.05.031 CrossRefGoogle Scholar
  59. 59.
    Zhang N, Castlebury LA, Miller AN, Huhndorf SM, Schoch CL, Seifert KA, Rossman AY, Rogers JD, Kohlmeyer J, Volkmann-Kohlmeyer B, Sung G-H (2006) An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny. Mycologia 98:1076–1087. doi: 10.3852/mycologia.98.6.1076 PubMedCrossRefGoogle Scholar
  60. 60.
    Weir A, Blackwell M (2005) Fungal biotrophic parasites of insects and other arthropods. In: Vega FE, Blackwell M (eds) Insect–Fungal Associations. Oxford University Press, New YorkGoogle Scholar
  61. 61.
    Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N, 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. doi: 10.1111/j.1365-294X.2005.02795.x PubMedCrossRefGoogle Scholar
  62. 62.
    Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, Hugenholtz P (2010) Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4:642–647. doi: 10.1038/ismej.2009.153 PubMedCrossRefGoogle Scholar
  63. 63.
    Sun DL, Jiang X, Wu QL, Zhou NY (2013) Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol 79:5962–5969. doi: 10.1128/AEM. 01282-13 PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS (2009) Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 75:5227–5236. doi: 10.1128/AEM. 00592-09 PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Rio RVM, Lefevre C, Heddi A, Aksoy S (2003) Comparative genomics of insect-symbiotic bacteria: influence of host environment on microbial genome composition. Appl Environ Microbiol 69:6825–6832. doi: 10.1128/aem. 69.11.6825-6832.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3:850–861. doi: 10.1038/nrg931 PubMedCrossRefGoogle Scholar
  67. 67.
    Bignell DE (2011) Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland. In: Bignell DE, Roisin Y, Lo N (eds) Biology of Termites: a Modern Synthesis. Springer Netherlands, pp 375–412. doi: 10.1007/978-90-481-3977-4_14
  68. 68.
    Costa PS, Oliveira PL, Chartone-Souza E, Nascimento AMA (2013) Phylogenetic diversity of prokaryotes associated with the mandibulate nasute termite Cornitermes cumulans and its mound. Biol Fertil Soils 49:567–574. doi: 10.1007/s00374-012-0742-x CrossRefGoogle Scholar
  69. 69.
    Grieco MAB, Cavalcante JJV, Cardoso AM, Vieira RP, Machado EA, Clementino MM, Medeiros MN, Albano RM, Garcia ES, de Souza W, Constantino R, Martins OB (2013) Microbial Community Diversity in the Gut of the South American Termite Cornitermes cumulans (Isoptera: Termitidae). Microb Ecol 65:197–204. doi: 10.1007/s00248-012-0119-6
  70. 70.
    Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, Chen Z, Childers CP, Glastad KM, Gokhale K, Gowin J, Gronenberg W, Hermansen RA, Hu H, Hunt BG, Huylmans AK, Khalil SMS, Mitchell RD, Munoz-Torres MC, Mustard JA, Pan H, Reese JT, Scharf ME, Sun F, Vogel H, Xiao J, Yang W, Yang Z, Yang Z, Zhou J, Zhu J, Brent CS, Elsik CG, Goodisman MAD, Liberles DA, Roe RM, Vargo EL, Vilcinskas A, Wang J, Bornberg-Bauer E, Korb J, Zhang G, Liebig J (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun 5. doi: 10.1038/ncomms4636
  71. 71.
    Bradford MA, Warren Ii RJ, Baldrian P, Crowther TW, Maynard DS, Oldfield EE, Wieder WR, Wood SA, King JR (2014) Climate fails to predict wood decomposition at regional scales. Nat Clim Change (advance online publication). doi: 10.1038/nclimate2251

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Renata Henrique Santana
    • 1
  • Elisa Caldeira Pires Catão
    • 2
  • Fabyano Alvares Cardoso Lopes
    • 2
  • Reginaldo Constantino
    • 3
  • Cristine Chaves Barreto
    • 1
  • Ricardo Henrique Krüger
    • 2
    • 4
    Email author
  1. 1.Genomic Sciences and BiotechnologyUniversidade Católica de BrasíliaBrasíliaBrazil
  2. 2.Cellular Biology DepartmentUniversidade de BrasíliaBrasíliaBrazil
  3. 3.Zoology DepartmentUniversidade de BrasíliaBrasíliaBrazil
  4. 4.Departamento de Biologia Celular, Instituto Central de Ciências Sul, Laboratório de EnzimologiaUniversidade de Brasília—UnBBrasíliaBrazil

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