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

Environmental Microbiology

Volumn 18, Issue 1, 2016, Pages 191-204

  Zheng, Hao ^a   Dietrich, Carsten ^a   Radek, Renate ^b   Brune, Andreas ^a,c  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLENE; NITROGEN; NITROGENASE; RNA 16S;

ANIMAL; BACTERIUM; CELL CYCLE; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; ISOPTERA; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; OXIDATION REDUCTION REACTION; PHYLOGENY; SYMBIOSIS;

ACETYLENE; ANIMALS; BACTERIA; CELL CYCLE; ISOPTERA; NITROGEN; NITROGEN FIXATION; NITROGENASE; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84956593690     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12960     Document Type: Article

References (69)

1. Austin, J.W., Szalanski, A.L., Scheffrahn, R.H., Messenger, M.T., Dronnet, S., and Bagnères, A.G. (2005) Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Ann Entomol Soc Am 98: 395-401.
2. Bauer, S., Tholen, A., Overmann, J., and Brune, A. (2000) Characterization of abundance and diversity of lactic acid bacteria in the hindgut of wood- and soil-feeding termites by molecular and culture-dependent techniques. Arch Microbiol 173: 126-137.
3. Berleman, J.E., and Bauer, C.E. (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology 150: 383-390.
4. Boga, H.I., and Brune, A. (2003) Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol 69: 779-786.
5. Brune, A. (2012) Endomicrobia: intracellular symbionts of termite gut flagellates. J Endocytobiosis Cell Res 23: 11-15.
6. Brune, A. (2014a) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12: 168-180.
7. Brune, A. (2014b) The family Elusimicrobiaceae. In The Prokaryotes. Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds). Berlin: Springer, pp. 637-640.
8. Brune, A., and Ohkuma, M. (2011) Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: A Modern Synthesis. Bignell, D.E., Roisin, Y., and Lo, N. (eds). Dordrecht: Springer, pp. 439-475.
9. Desai, M.S., and Brune, A. (2012) Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J 6: 1302-1313.
10. Desai, M.S., Strassert, J.F.H., 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.
11. Dos Santos, P.C., Fang, Z., Mason, S.W., Setubal, J.C., and Dixon, R. (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13: 162.
12. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I.M., Barbe, V., etal. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020-10025.
13. Eady, R.R. (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96: 3013-3030.
14. Eddy, S.R. (2011) Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195.
15. Fani, R., Gallo, R., and Lio, P. (2000) Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J Mol Evol 51: 1-11.
16. Geissinger, O., Herlemann, D.P.R., Morschel, E., Maier, U.G., and Brune, A. (2009) The ultramicrobacterium 'Elusimicrobium minutum' gen. nov., sp. nov., the first cultivated representative of the Termite Group 1 phylum. Appl Environ Microbiol 75: 2831-2840.
17. Graber, J.R., Leadbetter, J.R., and Breznak, J.A. (2004) Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl Environ Microbiol 70: 1315-1320.
18. Hardy, R.W.F., Burns, R.C., and Holsten, R.D. (1973) Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5: 47-81.
19. Herlemann, D.P.R., Geissinger, O., Ikeda-Ohtsubo, W., Kunin, V., Sun, H., Lapidus, A., etal. (2009) Genomic analysis of 'Elusimicrobium minutum', the first cultivated representative of the phylum 'Elusimicrobia' (formerly Termite Group 1). Appl Environ Microbiol 75: 2841-2849.
20. Hirsch, P. (1974) Budding bacteria. Annu Rev Microbiol 28: 391-444.
21. Hongoh, Y. (2011) Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell Mol Life Sci 68: 1311-1325.
22. Hongoh, Y., Ohkuma, M., and Kudo, T. (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44: 231-242.
23. Hongoh, Y., Deevong, P., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., etal. (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.
24. Hongoh, Y., Sharma, V.K., Prakash, T., Noda, S., Taylor, T.D., Kudo, T., etal. (2008) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 105: 5555-5560.
25. Howard, J.B., Kechris, K.J., Rees, D.C., and Glazer, A.N. (2013) Multiple amino acid sequence alignment nitrogenase component 1: insights into phylogenetics and structure-function relationships. PLoS ONE 8: e72751.
26. 2. J Bacteriol 194: 3689-3699.
27. 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: 332-342.
28. 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.
29. 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.
30. Inoue, J.I., Oshima, K., Suda, W., Sakamoto, M., Iino, T., Noda, S., etal. (2015) Distribution and evolution of nitrogen fixation genes in the phylum Bacteroidetes. Microb Environ 30: 44-50.
31. Katoh, K., and Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780.
32. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acids Techniques in Bacterial Systematics. Stackebrandt, E., and Goodfellow, M. (eds). Chichester: John Wiley & Sons, pp. 115-175.
33. Lang, C.A. (1958) Simple microdetermination of Kjeldahl nitrogen in biological materials. Anal Chem 30: 1692-1694.
34. Lemke, T., Stingl, U., Egert, M., Friedrich, M.W., and Brune, A. (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69: 6650-6658.
35. Lilburn, T.G., Kim, K.S., Ostrom, N.E., Byzek, K.R., Leadbetter, J.R., and Breznak, J.A. (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292: 2495-2498.
36. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
37. Mehta, M.P., and Baross, J.A. (2006) Nitrogen fixation at 92°C by a hydrothermal vent archaeon. Science 314: 1783-1786.
38. Merrick, M.J. (1992) Regulation of nitrogen fixation genes in bacteria. In Biological Nitrogen Fixation. Stacey, G., Burris, R.H., and Evans, H.J. (eds). New York: Chapman and Hall, pp. 835-876.
39. Moore, R.L. (1981) The biology of Hyphomicrobium and other prosthecate, budding bacteria. Annu Rev Microbiol 35: 567-594.
40. Murray, R.G.E., Doetsch, R.N., and Fobinow, C.F. (1994) Determinative and cytological light microscopy. In Methods for General and Molecular Bacteriology. Gerhardt, P., Murray, R.G.E., Wood, W.A., and Krieg, N.R. (eds). Washington, DC: American Society for Microbiology, pp. 21-41.
41. Nakamura, K., and Mizushima, S. (1975) In vitro reassembly of the membranous vesicle from Escherichia coli outer membrane components. Role of individual components and magnesium ions in reassembly. Biochim Biophys Acta 413: 371-393.
42. Neidhart, F.C., Ingraham, J.I., and Schaechter, M. (1990) Physiology of the Bacterial Cell: A Molecular Approach. Sunderland, Mass., USA: Sinauer Associates.
43. 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.
44. 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. Appl Environ Microbiol 65: 4935-4942.
45. Ohkuma, M., and Brune, A. (2011) Diversity, structure, and evolution of the termite gut microbial community. In Biology of Termites: A Modern Synthesis. Bignell, D.E., Roisin, Y., and Lo, N. (eds). Dordrecht: Springer, pp. 413-438.
46. Ohkuma, M., and Kudo, T. (1996) Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl Environ Microbiol 62: 461-468.
47. 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.
48. 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.
49. Pester, M., and Brune, A. (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1: 551-565.
50. Pfennig, N., and Trüper, H.G. (1981) Isolation of members of the families Chromatiaceae and Chlorobiaceae. In The Prokaryotes. Starr, M.P., Stolp, H., Trüper, H.G., Balows, A., and Schlegel, H.G. (eds). Berlin: Springer-Verlag, pp. 229-289.
51. Raymond, J., Siefert, J.L., Staples, C.R., and Blankenship, R.E. (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
52. Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208-212.
53. Roll, J.T., Shah, V.K., Dean, D.R., and Roberts, G.P. (1995) Characteristics of NIFNE in Azotobacter vinelandii strains. J Biol Chem 270: 4432-4437.
54. Schut, G.J., and Adams, M.W. (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191: 4451-4457.
55. Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31-43.
56. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
57. Staples, C.R., Lahiri, S., Raymond, J., Von Herbulis, L., Mukhophadhyay, B., and Blankenship, R.E. (2007) Expression and association of group IV nitrogenase NifD and NifH homologs in the non-nitrogen-fixing archaeon Methanocaldococcus jannaschii. J Bacteriol 189: 7392-7398.
58. 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.
59. Strassert, J.F.H., Desai, M.S., Radek, R., and Brune, A. (2010) Identification and localization of the multiple bacterial symbionts of the termite gut flagellate Joenia annectens. Microbiology 156: 2068-2079.
60. Sutherland, I.W., and Mackenzie, C.L. (1977) Glucan common to the microcyst walls of cyst-forming bacteria. J Bacteriol 129: 599-605.
61. Tholen, A., Pester, M., and Brune, A. (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62: 303-312.
62. Wertz, J.T., Kim, E., Breznak, J.A., Schmidt, T.M., and Rodrigues, J.L.M. (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.
63. Winnepenninckx, B., Backeljau, T., and De Wachter, R. (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9: 407.
64. Wu, M., and Scott, A.J. (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28: 1033-1034.
65. Wu, M., Chatterji, S., and Eisen, J.A. (2012) Accounting for alignment uncertainty in phylogenomics. PLoS ONE 7: e30288.
66. 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: 3768-3777.
67. Yang, H., Schmitt-Wagner, D., Stingl, U., and Brune, A. (2005) Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ Microbiol 7: 916-932.
68. Zheng, H., and Brune, A. (2015) Complete genome sequence of Endomicrobium proavitum, a free-living relative of the intracellular symbionts of termite gut flagellates (phylum Elusimicrobia). Genome Announc 3: e00679-15. doi:10.1128/genomeA.00679-15.
69. Zheng, H., Dietrich, C., Thompson, C.L., Meuser, K., and Brune, A. (2015) Population structure of Endomicrobia in single host cells of termite gut flagellates (Trichonympha spp. Microbes Environ 30: 92-98.