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Diversity, Ultrastructure, and Comparative Genomics of “Methanoplasmatales”, the Seventh Order of Methanogens

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Diversity, Ultrastructure, and Comparative Genomics of “Methanoplasmatales”, the Seventh Order of Methanogens Diversity, ultrastructure, and comparative genomics of “Methanoplasmatales”, the seventh order of methanogens Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) am Fachbereich Biologie der Philipps-Universität Marburg vorgelegt von Kristina Lang, geb. Paul aus Herborn Universitätsstadt Marburg, 2014 Marburg (Lahn), 2014 Die Untersuchungen zur vorliegenden Arbeit wurden von Oktober 2011 bis Oktober 2014 am Max-Planck-Institut für terrestrische Mikrobiologie in Marburg unter der Leitung von Prof. Dr. Andreas Brune durchgeführt. Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation angenommen am: 20.10.2014 Erstgutachter: Prof. Dr. Andreas Brune Zweitgutachter: Prof. Dr. Rudolf K. Thauer Tag der Disputation: 09.12.2014 Die in dieser Dissertation beschriebenen Ergebnisse sind in folgenden Publikationen veröffentlicht bzw. zur Veröffentlichung vorgesehen: Paul K, Nonoh JO, Mikulski L, and Brune A. (2012). “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl. Environ. Microbiol.78, 8245–8253. Lang K, Schuldes J, Klingl A, Daniel R, and Brune, A. Comparative genome analysis of “Candidatus Methanoplasma termitum” indicates a new mode of energy metabolism in the seventh order of methanogens. (Eingereicht) Lang K, Mikulski L, Dietrich C, Meuser K, and Brune A. Methanogenic community structure in the digestive tracts of tropical millipedes. (In Vorbereitung) Dietrich C, Nonoh JO, Lang K, Mikulski L, Meuser K, Köhler T, Boga HI, Ngugi DK, Sillam-Dussès D, and Brune A. Not coevolution but host specificity and habitat selection drive archaeal community structure in arthropod guts. (In Vorbereitung) Table of Content Summary ................................................................................................................... 1 Zusammenfassung ................................................................................................... 3 General Introduction ................................................................................................ 6 1.1 Methane ............................................................................................................ 7 1.2 Methanogenic archaea ...................................................................................... 7 1.3 Methanogenic pathways ................................................................................... 8 1.4 Methanogenesis in arthropods ........................................................................ 11 1.5. The uncultured Thermoplasmatales ............................................................... 12 1.6. Aims ............................................................................................................... 14 1.7 References ...................................................................................................... 15 “Methanoplasmatales”: Thermoplasmatales-related archaea in termite guts and other environments are the seventh order of methanogens .............................. 22 2.1 Abstract ........................................................................................................... 23 2.2 Introduction ..................................................................................................... 24 2.3 Material and Methods ...................................................................................... 26 2.4 Results ............................................................................................................ 29 2.5 Discussion ....................................................................................................... 38 2.6 Acknowledgments ........................................................................................... 44 2.7 References ...................................................................................................... 44 Comparative genome analysis of “Candidatus Methanoplasma termitum” indicates a new mode of energy metabolism in the seventh order of methanogens .......................................................................................................... 50 3.1 Abstract ........................................................................................................... 52 3.2 Introduction ..................................................................................................... 53 I 3.3 Material and Methods ...................................................................................... 55 3.4 Results and Discussion ................................................................................... 58 3.5 Acknowledgments ........................................................................................... 79 3.6 References ...................................................................................................... 80 3.7 Supplementary Information ............................................................................. 87 Methanogenic community structure in the digestive tracts of tropical millipedes ................................................................................................................................. 93 4.1 Abstract ........................................................................................................... 94 4.2 Introduction ..................................................................................................... 95 4.3 Material and Method ....................................................................................... 97 4.4 Results ............................................................................................................ 99 4.5 Discussion ..................................................................................................... 110 4.6 Acknowledgments ......................................................................................... 117 4.7 References .................................................................................................... 117 Not coevolution but host specificity and habitat selection drive archaeal community structure in arthropod guts ............................................................. 123 5.1 Abstract ......................................................................................................... 125 5.2 Introduction ................................................................................................... 126 5.3 Material and Methods .................................................................................... 128 5.4 Results .......................................................................................................... 132 5.5 Discussion ..................................................................................................... 161 5.6 Acknowledgements ....................................................................................... 166 5.7 References .................................................................................................... 166 5.8 Supplementary Information ........................................................................... 173 General Discussion .............................................................................................. 176 6.1 The methyl-reducing pathway ....................................................................... 178 6.2 Evolution of genes involved in methanogenesis ........................................... 181 II 6.3 Cell wall less archaea ................................................................................... 187 6.4 Concluding remarks and future perspective .................................................. 190 6.5 References .................................................................................................... 191 Danksagung .......................................................................................................... 197 Erklärung der Eigenständigkeit ........................................................................... 198 III Summary Summary 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
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