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Phylogenetic and Functional Characterization of Symbiotic Bacteria in Gutless Marine Worms (Annelida, Oligochaeta)

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Phylogenetic and Functional Characterization of Symbiotic Bacteria in Gutless Marine Worms (Annelida, Oligochaeta) Phylogenetic and functional characterization of symbiotic bacteria in gutless marine worms (Annelida, Oligochaeta) Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften -Dr. rer. nat.- dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Anna Blazejak Oktober 2005 Die vorliegende Arbeit wurde in der Zeit vom März 2002 bis Oktober 2005 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: 22. November 2005 Contents Summary ………………………………………………………………………………….… 1 Zusammenfassung ………………………………………………………………………… 2 Part I: Combined Presentation of Results A Introduction .…………………………………………………………………… 4 1 Definition and characteristics of symbiosis ...……………………………………. 4 2 Chemoautotrophic symbioses ..…………………………………………………… 6 2.1 Habitats of chemoautotrophic symbioses .………………………………… 8 2.2 Diversity of hosts harboring chemoautotrophic bacteria ………………… 10 2.2.1 Phylogenetic diversity of chemoautotrophic symbionts …………… 11 3 Symbiotic associations in gutless oligochaetes ………………………………… 13 3.1 Biogeography and phylogeny of the hosts …..……………………………. 13 3.2 The environment …..…………………………………………………………. 14 3.3 Structure of the symbiosis ………..…………………………………………. 16 3.4 Transmission of the symbionts ………..……………………………………. 18 3.5 Molecular characterization of the symbionts …..………………………….. 19 3.6 Function of the symbionts in gutless oligochaetes ..…..…………………. 20 4 Goals of this thesis …….…………………………………………………………... 23 B Results and Discussion …….……………………………………………………. 25 1 Symbiotic community structure in gutless oligochaetes from different Environments ………………………………………………………………………. 26 1.1 Host species ……………………………………………………..……………. 26 1.2 Molecular identification and phylogeny of the bacterial symbionts ………. 27 1.2.1 Gammaproteobacterial symbionts ……………………………………. 27 1.2.2 Deltaproteobacterial symbionts ……………………………………….. 30 1.2.3 Alphaproteobacterial symbionts ………………………………………. 34 1.2.3.1 Bacterial symbionts related to mitochondrial 16S rRNA gene sequences ………………………………………………... 35 1.2.4 Spirochete symbionts ………………………………………………….. 37 1.3 Conclusions ……………………………………………………………………. 38 1.3.1 Phylogenetic diversity ………………………………………………….. 38 1.3.2 Functional aspects of the bacterial symbionts ………………………. 39 2 Metabolic diversity of bacterial symbionts ……………………………………….. 43 2.1 PCR based approaches ………………………………………………………. 43 2.1.1 CO2 fixation ……………………………………………………………... 43 2.1.1.1 Calvin- Benson-Bassham cycle ………………………………. 43 2.1.1.2 Reverse tricarboxylic acid cycle ………………………………. 45 2.1.2 Energy metabolism ……………………………………………………. 46 2.1.2.1 Sulfur energy metabolism ……………………………………… 46 2.1.2.2 Nitrogen energy metabolism …………………………………... 49 2.2 Comparative metagenomics …………………………………………………. 51 2.2.1 Bacterial artificial chromosome library construction and analysis …. 51 2.2.2 Thioautotrophic metabolism of the O. algarvensis symbiont ..…….. 54 2.2.2.1 Dsr gene cluster ………………………………………………… 56 2.2.2.2 Cbb gene cluster ……………………………………………….. 56 2.2.3 Novel genes …………………………………………………………….. 57 3 Outlook ………………………………………………………………………………. 58 C References ……………………………………………………………………… 61 Part II: Publications A Contributions to the manuscript …………………………………………… 76 B Publications ……………………………………………………………………. 77 1 Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin …………. 77 2 Phylogeny of 16S rRNA, RubisCO, and APS reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and Bahamas …………………………………………………….. 89 3 Metagenomic analysis of co-occurring symbionts in marine worms from the Mediterranean ……………………………………………………………………… 117 4 Multiple symbioses with sulfur oxidizers, sulfate reducers and spirochetes in two gutless marine worms (Oligochaeta) from Mediterranean sediments low in sulfide ……………………………………………………………………………. 157 C List of Publications ..……………………….………………………………… 161 Summary Summary Symbioses between chemoautotrophic bacteria and eukaryotic hosts are widespread in marine environments. In most chemosynthetic endosymbioses, only a single, or at most two bacterial phylotypes co-occur within a host species. In this study the phylogenetic and metabolic diversity of bacterial endosymbionts in gutless marine worms (Annelida, Oligochaeta) from different environments was investigated. Almost all host species harbor a gammaproteobacterial sulfur oxidizer indicating the importance of these Gamma 1 symbionts for the nutrition of the gutless oligochaetes. A second gammaproteobacterial symbiont and deltaproteobacterial symbionts were detected in hosts from coastal silicate sediments, while in hosts from calcareous sands alphaproteobacterial symbionts were identified. Spirochetes were found in hosts from both types of sediments. The phylogenetic diversity of the bacterial symbionts mirrors their different metabolic capabilities. The Deltaproteobacteria have been identified as sulfate reducers and the secondary gammaproteobacterial symbionts are hypothesized to be sulfur oxidizers. Key genes involved in oxidative and reductive sulfur metabolism, CO2 fixation via the Calvin-Benson-Bassham (CBB) cycle, and nitrogen metabolism were successfully detected. Based on phylogenetic analyses it was possible to make potential assignments of genes to a respective symbiont. The use of comparative metagenomics gave first insights into the genome of a gutless oligochaete symbiont. A contiguous sequence of 51 kb from a bacterial artificial chromosome insert contained genes involved in significant metabolic pathways for these symbioses such as sulfur oxidation and CO2 fixation via the CBB cycle indicating that this sequence originated from a thioautotrophic symbiont. This study showed that the symbiotic community in marine gutless oligochaetes with at least three and as many as six different symbiotic phylotypes is much more complex than previously assumed. Despite the high phylogenetic diversity, these associations are clearly specific and stable for most phylotypes within a given host species. 1 Zusammenfassung Zusammenfassung Symbiosen zwischen chemoautotrophen Bakterien und eukaryontischen Wirten sind weit verbreitet in marinen Lebensräumen. In den meisten chemosynthetischen Endosymbiosen ist innerhalb einer Wirtspezies nur ein einziger bakterieller Phylotyp zu finden oder es coexistieren höchstens zwei Phylotypen. In dieser Studie zur phylogenetischen und metabolischen Diversität der bakteriellen Endosymbionten in darmlosen, marinen Würmern (Annelida, Oligochaeta) wurden Spezies aus unterschiedlichen Habitaten untersucht. Nahezu alle Wirtspezies beherbergen gammaproteobakterielle Schwefeloxidierer, ein Hinweis auf die Bedeutung dieser Gamma 1 Symbionten für die Ernährung der darmlosen Wirte. Ein zweiter gammaproteobakterieller Symbiont sowie deltaproteobakterielle Symbionten wurden in Wirten aus silikathaltigen Küstensedimenten detektiert, während in Wirten aus kalkhaltigen Sedimenten alphaproteobakterielle Symbionten identifiziert wurden. Spirocheten wurden in Wirten aus beiden Sedimenttypen gefunden. Die phylogenetische Diversität der bakteriellen Symbionten spiegelt ihre metabolischen Fähigkeiten wider. Die Deltaproteobakterien sind Sulfatreduzierer, als Funktion der sekundären gammaproteobakteriellen Symbonten wird die Schwefeloxidation vermutet. Verschiedene Schlüsselenzyme des oxidativen und reduktiven Schwefelmetabolismus, der CO2 Fixierung mittels Calvin-Benson- Bassham (CBB) Zyklus, und des Stickstoffmetabolismus wurden in diesen Symbionten erfolgreich detektiert. Phylogenetische Analysen der gefundenen Schlüsselenzyme ermöglichten eine potentielle Zuordnung der Gene zu den entsprechenden Symbionten. Die Analyse einer Metagenomgenbank gewährte erste Einblicke in das Genom eines Symbionten. So trug z.B. ein Klon ein 51 kb großes Insert mit Genclustern, die maßgeblich für die Stoffwechselwege dieser Symbiosen, wie z.B. Schwefeloxidation und CO2 Fixierung via CBB Zyklus, sind und auf einen Ursprung aus einem thiotrophen Symbionten hinweisen. Diese Studie hat gezeigt, dass die symbiontische Gemeinschaft in den marinen, darmlosen Oligochaeten mit mindestens drei und höchstens sechs unterschiedlichen Phylotypen komplexer ist als früher angenommen. Trotz der hohen phylogenetischen Diversität sind diese Assoziationen eindeutig spezifisch und für die meisten Phylotypen innerhalb eines Wirtes stabil. 2 Part I: Combined Presentation of Results 3 Introduction A Introduction 1 Definition and characteristics of symbiosis The term “symbiosis” originates from the Greek word sumbiosis for “living together”. The first usage of this word in a biological context is attributed to the German lichenologist Albert B. Frank who carried out detailed studies of lichens, mutualistic associations of microscopic green algae or cyanobacteria and filamentous fungi (Frank, 1877). Only two years later, in 1879, the German scientist Anton de Bary defined symbiosis as the living together of differently named organisms and is now cited in almost all text books as having defined the term symbiosis (De Bary, 1879). De Bary included all cases of intimate associations between species in the term symbiosis including (i) mutualistic associations, in which all partners benefit from the relationship, (ii) parasitic associations, in which one of the organisms benefits at the expense of the other, and (iii) commensalistic associations, in which one partner benefits and the
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