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Titel:Diversity, ultrastructure, and comparative genomics of “Methanoplasmatales”, the seventh order of methanogens
Autor:Lang, Kristina
Weitere Beteiligte: Brune, Andreas (Prof. Dr.)
URN: urn:nbn:de:hebis:04-z2014-04786
DDC: Biowissenschaften, Biologie
Titel (trans.):Diversität, Ultrastruktur und vergleichende Genomik der Methanoplasmatales, der 7. Ordnung von Methanogenen


Archaea, Methanomassiliicoccales, Arthropoda, Biologie, Life sciences, "Methanoplasmatales", Biowissenschaften

Methanogenic archaea are strict anaerobes that occur in diverse environments like marine and freshwater sediments, soils, hot springs, sewage sludge and the digestive tracts of animals and humans. Methanogens belong to the phylum Euryarchaeota, which comprises both methanogenic and non-methanogenic orders and many lineages of uncultivated archaea with unknown properties. By a comprehensive phylogenetic analysis, we connected the 16S rRNA gene sequences of one of these deep-branching lineages, distantly related to Thermoplasmatales, to a large clade of unknown mcrA gene sequences, a functional marker for methanogenesis. The analysis suggested that both genes stem from the same organism, indicating the methanogenic nature of this group. This was further confirmed by our two highly enriched cultures of methanogenic archaea, Candidatus Methanoplasma termitum strain MpT1 from a higher termite and strain MpM2 from the millipede gut, which had 16S rRNA genes that fell within in this lineage. Together with the recent isolation of Methanomassiliicoccus luminyensis from human feces, the results of our study supported that the entire lineage, distantly related to the Thermoplasmatales, represents the seventh order of methanogens, the “Methanoplasmatales” (now referred to as Methanomassiliicoccales). To gain deeper insight into this novel order of methanogens, we sequenced and analyzed the genome of Ca. Mp. termitum strain MpT1, and compared it to the three other genomes of the order Methanomassiliicoccales available to date. Our results confirmed that all members of the lineage are obligately hydrogen-dependent methylotrophs that perform methanogenesis by the hydrogen-dependent reduction of methanol or methylamines and lack the entire C1 pathway for reduction CO2 to CH4. However, this raises questions concerning the mechanism of energy conservation that had so far escaped attention. Our comparative analysis revealed that energy conversion in Methanomassiliicoccales differs from those of other obligately hydrogen-dependent methylotrophs. We identified a complex encoded by all four genomes that is related to the membrane-bound F420:methanophenazine oxidoreductase (Fpo) of Methanosarcinales, but lacks the F420-oxidzing module, as in the apparently ferredoxin-dependent Fpo-like homolog in Methanosaeta thermophila. We suggests that this Fpo-like complex of the Methanomassiliicoccales uses the present D subunit of the heterodisulfide reductase as an electron acceptor to form an energy-converting ferredoxin:heterodisulfide oxidoreductase. This suggests that in Methanomassiliicoccales, the heterodisulfide serves two functions: the production of reduced ferredoxin during electron bifurcation at the cytoplasmic MvhADG/HdrABC complex, and the generation of a membrane portential during the reoxidation of ferredoxin via a membrane-bound electron transport chain. This dual function of heterodisulfide may be a unique characteristic of the entire order. Furthermore, we identified an unusual two-membrane system in Ca. Mp. termitum and strain MpM2 by transmission electron micrographs that might be typical for the complete order. While methanogenesis in insect guts has been investigated by numerous authors, almost nothing is known about methanogenesis and the methanogenic community structure in millipedes, the only other group of arthropods that emit methane. Our analysis of the phylogenetic diversity of archaea associated with tropical millipedes documented that most methanogens in their guts fall into the orders Methanobacteriales, Methanosarcinales, Methanomicrobiales and Methano-massiliicoccales. Their close relatedness to methanogens from the guts of termites, cockroaches and scarab beetle larvae suggests that methanogenic community structure in methane-emitting arthropods is not necessarily shaped by cospeciation. Recently, it has been shown that bacterial communities mirror major events in the evolutionary history of the termites and cockroaches, which leads to the speculation if this is also case for the archaeal community. Here, we present a study that consists of both clone libraries and high-throughput sequencing which concludes that the archaeal community structure and phylogeny is shaped more by the major host groups than by coevolution and diet. This indicates that the host habitat is the major driving force for the selection of the archaeal community.

Bibliographie / References

  1. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post- analysis of large phylogenies. Bioinformatics 30:1312–1313.
  2. Keltjens JT, Vogels GD. 1993. Conversion of methanol and methylamines to methane and carbon dioxide, pp. 253–303. In Ferry JG. (ed.), Methanogenesis. Chapman & Hall, New York, United States of America.
  3. Miller TL, Meyer J W. 1985. Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Arch. Microbiol. 141:116–122.
  4. Seedorf H, Dreisbach A, Hedderich R, Shima S, Thauer RK. 2004. F 420 H 2 oxidase (FprA) from Methanobrevibacter arboriphilus, a coenzyme F 420 -dependent enzyme involved in O 2 detoxification. Arch. Microbiol. 182:126–137.
  5. Junglas B, Briegel A, Burghardt T, Walther P, Reinhard W, Huber H, Rachel R. 2008. Ignicoccus hospitalis and Nanoarchaeum equitan: ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190:395–408.
  6. Moparthi VK, Hägerhäll C. 2011. The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits. J. Mol. Evol. 72:484– 497.
  7. Brune A, 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.
  8. Segerer A, Langworthy TA, Stetter KO. 1988. Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Syst. Appl. Microbiol. 10:161- 171.
  9. Albers SV, Meyer BH. 2011. The archaeal cell envelope. Nat. Rev. Microbiol. 9:414– 426.
  10. Sprenger WW, van Belzen MC, Rosenberg J, Hackstein JHP, Keltjens JT. 2000. Methanomicrococcus blatticola gen. nov., sp., nov., a methanol-and methylamine- reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int. J. Syst. Evol. Microbiol. 50:1989–1999.
  11. Mander GJ, Pierik AJ, Huber H, Hedderich R. 2004. Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus. Eur. J. Biochem. 271:1106–1116.
  12. Lindinger W, Taucher J, Jordan A, Hansel A, Vogel W. 1997. Endogenous production of methanol after the consumption of fruit. Alcohol. Clin. Exp. Res. 21:939–943.
  13. Tokura M, Ohkuma M and Kudo T. 2000. Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol. Ecol. 33:233–240.
  14. Egert M, Wagner B, Lemke T, Brune A, 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.
  15. Porat I, Kim W, Hendrickson EL, Xia Q, Zhang Y, Wang T, Taub F, Moore BC, Anderson IJ, Hackett M, Leigh JA, Whitman WB. 2006. Disruption of the operon encoding Ehb hydrogenase limits anabolic CO 2 assimilation in the archaeon Methanococcus maripaludis. J. Bacteriol. 188:1373–1380.
  16. Hara K, Shinzato N, Seo M, Oshima T, Yamagishi A. 2002. Phylogenetic analysis of symbiotic archaea living in the gut of xylophagous cockroaches. Microb. Environ. 17:185–190.
  17. Huber H, Burggraf S, Mayer T, Wyschkony I, Rachel R, Stetter KO. 2000. Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov. Int. J. Syst. Evol. Microbiol. 50:2093–2100.
  18. Paper W, Jahn U, Hohn MJ, Kronner M, Nähter DJ, Burghardt T, Rachel R, Stetter KO, Huber H. 2007. Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans'. Int. J. Syst. Evol. Microbiol. 57:803–808.
  19. Lineages of acidophilic archaea revealed by community genomic analysis. Science 314:1933–1935.
  20. Genome sequence of "Candidatus Methanomassiliicoccus intestinalis" Issoire-Mx1, a third Thermoplasmatales-related methanogenic archaeon from human feces. Genome Announc 1:e00453–13.
  21. Wickham H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York, United States of America.
  22. Hedderich R, Hamann N, Bennati M. 2005. Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster. Biol. Chem. 386:961–970.
  23. Reysenbach A-L, Liu Y, Banta AB, Breveridge TJ, Kirshtein JD, Schouten S, Tivey MK, Von Damm KL, Voytek MA. 2006. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447.
  24. Hackstein JHP, van Alen TA. 1996. Fecal methanogens and vertebrate evolution. Evolution 50:559–572.
  25. Huber H, Stetter KO. 2006. Thermoplasmatales, pp. 101–112. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. (ed.), The Prokaryotes, vol. 3. Springer, New York, United States of America.
  26. International Committee on Systematic Bacteriology. 1985. International Committee on Systematics of Prokaryotes: Subcommittee on the taxonomy of Mollicutes. Minutes of the Interim Meeting, 21 and 26 June 1984, Jerusalem, Israel . Int. J. Syst. Bacteriol. 35:378–381.
  27. Brioukhanov A, Netrusov A, Sordel M, Thauer RK, Shima S. 2000. Protection of Methanosarcina barkeri against oxidative stress: identification and characterization of an iron superoxide dismutase. Arch. Microbiol. 174:213–216.
  28. Gorlas A, Robert C, Gimenez G, Drancourt M, Raoult D. 2012. Complete Genome Sequence of Methanomassiliicocus luminyensis, the largest genome of a human- associated Archaea species. J. Bacteriol. 194:4745.
  29. Zellner G, Alten C, Stackebrandt E, Conway de Macario E and Winter J. 1987. Isolation and characterization of Methanocorpusculum parvum, gen. nov., spec. nov., a new tungsten requiring, coccoid methanogen. Arch. Microbiol. 147:13–20.
  30. Sustr V, Chronáková A, Semanová S, Tajovský K and Simek M. 2014. Methane production and methanogenic archaea in the digestive tracts of millipedes (Diplopoda). PLoS ONE 9:e102659.
  31. methanogen from the hindgut of the cockroach Periplaneta americana. Int.
  32. Tsai YH and Cahill KM. 1970. Parasites of the german cockroach (Blattella germanica L.) in New York City. J. Parasitol. 56:375–377.
  33. Deuel H, Stutz E. 1958. Pectic substances and pectic enzymes. Adv. Enzymol. Relat. Subj. Biochem. 20:341–382.
  34. Mander GJ, Duin EC, Linder D, Stetter KO, Hedderich R. 2002. Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur. J. Biochem. 269:1895–1904.
  35. Fricke WF, Seedorf H, Henne A, Kruer M, Liesegang H, Hedderich R, Gottschalk G, Thauer RK. 2006. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H 2 for methane formation and ATP synthesis. J. Bacteriol. 188:642–658.
  36. Luton PE, Wayne JM, Sharp RJ, Riley PW. 2002. The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530.
  37. Kendall MM, Boone DR. 2006. The order Methanosarcinales, pp. 244–256. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. (ed.), The prokaryoets, vol.
  38. Comolli LR, Baker BJ, Downing KH, Siegerist CE, Banfield JF. 2009. Three- dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J. 3:159–167.
  39. Brioukhanov AL, Netrusov AI, Eggen RIL. 2006. The catalase and superoxide dismutase genes are transcriptionally up-regulated upon oxidative stress in the strictly anaerobic archaeon Methanosarcina barkeri. Microbiology 152:1671–1677.
  40. Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schram A, Jørgensen BB. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215– 218.
  41. Welte C, Deppenmeier U. 2011. Re-evaluation of the function of the F 420 dehydrogenase in electron transport in Methanosarcina mazei. FEBS J. 278:1277–1287.
  42. Earl J, Hall G, Pickup R W, Ritchie D A, Edwards C. 2003. Analysis of methanogen diversity in a hypereutrophic lake using PCR-RFLP analysis of mcr sequences. Microb. Ecol. 46:270–278.
  43. Thauer R K, Kaster A-K, Seedorf H, Buckel W, Hedderich R. 2008. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6:579–591.
  44. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA. 1992. International Code of Nomenclature of Bacteria -Bacteriological Code, 1990 Revision. ASM Press, Washington (DC).
  45. Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ. 28:244–250.
  46. Rose CS, Pirt SJ. 1981. Conversion of glucose to fatty acids and methane: roles of two mycoplasmal agents. J. Bacteriol. 147:248–254.
  47. Balch WE, Fox GE, Magrum LG, Woese CR, Wolfe RS. 1979. Methanogens: reevaluation of a unique biological group. Microbiol. Rev. 43:260–296.
  48. Borrel G, Harris HMB, Tottey W, Mihajlosvki A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O'Toole PW, Brugère J-F. 2012. Genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J. Bacteriol. 194:6944–6945.
  49. Borrel G, O'Toole PW, Harris HMB, Peyret P, Brugère J-F, Gribaldo S. 2013b. Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol. Evol. 194: 6944–6945.
  50. Thauer RK, Jungermann K, Decker K. 1977. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41:100–180.
  51. Castro H, Ogram A, Reddy KR. 2004. Phylogenetic characterization of methanogenic assemblages in eutrophic and oligotrophic areas of the Florida Everglades. Appl. Environ. Microbiol. 70:6559–6568.
  52. Grosskopf R, Stubner S, Liesack W. 1998. Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl. Environ. Microbiol. 64:4983–4989.
  53. Shinzato N, Matsumoto T, Yamaoka I, Oshima T, Yamagishi A. 1999. Phylogenetic diversity of symbiotic methanogens living in the hindgut of the lower termite Reticulitermes speratus analyzed by PCR and in situ hybridization. Appl. Environ. Microbiol. 65:837–840.
  54. 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. 67:4880–4890.
  55. Welte C, Deppenmeier U. 2014. Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim. Biophys. Acta 1837:1130–1147.
  56. Rosell K-G and Svennson S. 1974. Studies of the distribution of the 4-O-methyl-D- glucuronic acid residues in birch xylan. Carbohydrate Research 42:297–304.
  57. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, Uchiyama H, 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.
  58. Bapteste E, Brochier C, Boucher Y. 2005. Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1:353–363.
  59. Rachel R, Wyschkony I, Riehl S and Huber H. 2002. The ultrastructure of Ignicoccus: Evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1:9–18.
  60. Ragon M, Van Driessche A E S, García-Ruíz J M, Moreira D, López-García P. 2013. Microbial diversity in the deep-subsurface hydrothermal aquifer feeding the giant gypsum crystal-bearing Naica Mine, Mexico. Front. Microbiol. 4:1–11.
  61. Dridi B, Fardeau M-L, Ollivier B, Raoult D, Drancourt M. 2012. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces . Int. J. Syst. Evol. Microbiol. 62:1902–1907.

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