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Molecular Ecology of the NOR5/OM60 Group Of Molecular Ecology of the NOR5/OM60 Group of Gammaproteobacteria Dissertation zur Erlangung des akademischen Grades Doktors der Naturwissenschaften (Dr. rer. nat.) Dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von YAN Shi Bremen Februar 2009 Die vorliegende Arbeit wurde in der Zeit von April 2006 bis Februar 2009 am Max- Planck-Institut für marine Mikrobiologie in Bremen angefertigt. 1. Gutachter: Prof. Dr. Rudolf Amann 2. Gutachter: Prof. Dr. Ulrich Fischer Tag des Promotionskolloquiums: 26. März 2009 Table of Contents Summary............................................................................................................................ 1 Zusammenfassung............................................................................................................. 2 ᨬ㽕 .................................................................................................................................... 3 List of Abbreviations ........................................................................................................ 4 1 Introduction................................................................................................................. 5 1.1 Marine bacteria that utilize light............................................................................ 5 1.2 The NOR5/OM60 group.......................................................................................... 6 1.2.1 Phylogeny of Bacteria ............................................................................................ 6 1.2.2 History, phylogeny and abundance of the NOR5/OM60 clade .............................. 7 1.2.3 Strain KT71........................................................................................................... 10 1.2.4 Members of NOR5/OM60 group are AAnPs ....................................................... 11 1.3 Sampling stations ................................................................................................... 11 1.3.1 Yangtze River estuary........................................................................................... 11 1.3.2 Namibian upwelling region................................................................................... 12 1.3.3 Vision cruise......................................................................................................... 13 1.3.4 German Bight........................................................................................................ 14 1.3.5 North Sea sediment............................................................................................... 14 1.3.6 Other sampling stations......................................................................................... 15 1.4 Methodological aspects.......................................................................................... 15 1.4.1 The 16S rRNA approach....................................................................................... 16 1.4.2 Genomics and metagenomics ............................................................................... 17 1.4.3 Culturing ............................................................................................................... 17 1.5 Aims of this study................................................................................................... 17 2 Results and Discussion.............................................................................................. 18 2.1 Phylogeny................................................................................................................ 18 2.2 Biogeography.......................................................................................................... 20 2.2.1 Worldwide existence............................................................................................. 20 2.2.2 Design and optimization of new probes sets......................................................... 24 2.2.3 Quantification of NOR5/OM60 in the environment............................................. 26 2.3 North Sea strains of NOR5/OM60........................................................................ 28 2.3.1 Isolation sources and growth features................................................................... 28 2.3.2 Pigments................................................................................................................ 30 2.3.3 General genomic features ..................................................................................... 30 2.3.4 pufM genes............................................................................................................ 31 2.4 Genomics................................................................................................................. 31 2.4.1 General comparison of the genomes..................................................................... 31 2.4.2 Functional genes ................................................................................................... 34 2.5 Evolution and functions of NOR5/OM60 group in the ocean............................ 39 3 Outlook....................................................................................................................... 41 3.1 Phylogeny and biogeography................................................................................... 41 3.2 Comparative genomics............................................................................................. 41 3.3 Gene searching in metagenomic libraries................................................................ 42 3.4 Combining detection of FISH and functions ........................................................... 42 3.5 Physiological tests for the model strains of NOR5/OM60 ...................................... 42 4 References.................................................................................................................. 44 List of Publications and Manuscripts ........................................................................... 49 Unit 1 Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria................................................................................................ 51 Unit 2 Potential novel photoautotrophy in the NOR5/OM60 clade of Gammaproteobacteria discovered by genome comparison .................................... 83 Unit 3 Characterization of the NOR5/OM60 strains from the North Sea............... 113 Acknowledgement......................................................................................................... 122 Summary In this thesis, a newly discovered gammaproteobacterial group – the NOR5/OM60 clade, which includes the novel aerobic anoxygenic phototrophs (AAnPs), was studied in the aspects of phylogeny, biogeography and physiology using both molecular and culturing methods. By means of 16S rRNA phylogenetic analysis, NOR5/OM60 group was defined as a monophyletic clade inside the class Gammaproteobacteria. More than 500 16S rRNA sequences of this clade were retrieved from public databases. Further studies classified the sequences into 13 subclades. My studies on the biogeography of NOR5/OM60 clade showed a cosmopolitan distribution. They were found in all oceans and at the coasts of all the continents. NOR5/OM60 seems to be most abundant in marine coastal water and sediment. However, they have also been encountered in surface water of open ocean, deep-sea sediment, freshwater, saline lakes and soil. The abundance of members of the NOR5/OM60 clade in various marine sites was determined by fluorescence in situ hybridization (FISH) with a newly designed and optimized probe set. In the ocean, the common relative abundance ranges from <1% in the open ocean to about 10% in the North Sea coastal water. The existence in coastal sediment and freshwater was also proved by FISH. More than 30 strains of the NOR5/OM60 clades had been isolated as pure cultures in several studies. Of these, the genomes of five strains (KT71, RAp1red, Ivo14, HTCC2080 and HTCC2148) were fully sequenced. In this thesis, these five genomes were compared to each other and to a closely related strain, HTCC2143 from the BD1-7 group. The photosynthesis (PS) superoperon, the key genes of 3-hydroxypropionate cycle for carbon fixation, and the sox operon for sulfur compound oxidation were found in four strains: KT71, RAp1red, Ivo14 and HTCC2080. Genomic comparison indicated that, like KT71, many NOR5/OM60 members may also be AAnPs and potentially be able to use light as energy source. 1 Zusammenfassung In dieser Arbeit wurde eine kürzlich entdeckte Gruppe, die NOR5/OM60-Gruppe der Gammaproteobacteria, einige von dessen Mitglieder den aeroben anoxygenen und phototrophen Bakterien (AAnP) gehöhren, in Phylogenie, Biogeographie und Physiologie anhand molekularer und kultivierungsbasierender Methoden untersucht. Anhand der phylogenetischen Analyse der 16S rRNA Sequenzen wurde die NOR5/OM60-Gruppe als eine Monophylie in der Klasse Gammaproteobacteria begrenzt. Mehr als 500 16S rRNA Sequenzen aus dieser Gruppe wurden in öffentlichen Daten- banken gefunden. Weitere Studien klassifizierten die Sequenzen in 13 Untergruppen. Biogeographische Untersuchungen zeigten eine weltweite Verteilung der NOR5/OM60- Gruppe, welche in allen Ozeanen und an Küsten aller Kontinenten vorkommt. Diese Organismen scheinen am häufigsten in marinen Küstengewässer und Sediment aufzu- treten, jedoch kommen sich auch in Hochseeoberflächengewässer, Tiefseesedimenten, Süßwasser, Salzseen und im Boden vor. Die Abundanz der
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