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Isolation and Characterization of Bacteria from the Deep Sea And Isolation and characterization of bacteria from the deep sea and their potential to produce bioactive natural products Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel Vorgelegt von Andrea Gärtner Kiel 2011 Referent: Prof. Dr. Johannes F. Imhoff Korreferent: Prof. Dr. Peter Schönheit Tag der mündlichen Prüfung: 25.03.2011 Zum Druck genehmigt: 25.03.2011 gez. Prof. Dr. Lutz Kipp, Dekan Table of Contents Summary 4 Zusammenfassung 5 Introduction 1. Prokaryotic life in the deep sea 8 1.1. Microbial life in the oligotrophic deep sea 12 1.1.1.The Eastern Mediterranean Sea 13 1.2.Microbial life at deep-sea hydrothermal vent fields 15 1.2.1.The Logatchev hydrothermal vent field (LHF) 16 2. The deep sea as a treasure crest for new natural products 18 3. Aims of the thesis 23 4. Thesis outline 25 Chapters Chapter I: Isolation and characterization of bacteria from the Eastern 28 Mediterranean deep sea Chapter II: Micromonospora strains from the Mediterranean deep sea as 48 promising sources for new natural products Chapter III: Levantilide A and B, novel macrolides isolated from the 67 deep-sea Micromonospora sp. isolate M71_A77 Chapter IV: Bacteria from the Logarchev hydrothermal vent field exhibit 81 antibiotic activities Chapter V: Amphritea atlantica gen. nov. spec. nov., a novel gamma- 89 proteobacterium isolated from the Logatchev hydrothermal vent field Chapter VI: Functional genes as markers for sulfur cycling and CO2 102 fixation in microbial communities of hydrothermal vents of the Logatchev field Discussion 127 References 135 Personal contribution to multiple-author manuscripts 140 List of Publications 142 Danksagung 143 Appendix 145 Summary Due to the high re-discovery rate of already known active compounds in recent drug research it appears reasonable to expand the search on unexplored environments with unique living conditions and yet undiscovered organisms. The deep sea demonstrates such a marginally investigated environment harboring presumably undiscovered bacterial taxa which are adapted to the extreme living conditions in the deep sea environment and which might possess unknown metabolites. The aim of the present thesis was therefore the characterization of deep-sea bacteria with the purpose to find novel and bioactive substances produced by these bacteria. Heterotrophic mesophilic bacterial strains were recovered and phylogenetically characterized from two totally different deep-sea habitats: the extremely oligotrophic Eastern Mediterranean and the Logatchev hydrothermal vent field (LHF) located at 15°N along the Mid Atlantic Ridge. The antimicrobially active bacteria isolated from the hydrothermal environments were mainly assigned to the Gammaproteobacteria. One bioactive strain, M41T, revealed to be a representative of a novel genus and species, Amphritea atlanticaT. This strain was isolated from a mussel field at LHF and physiological analysis showed that it is well adapted to the mesophilic temperatures of hydrothermally influenced environments. In addition, the bacterial community of diffusive fluids emanating out of a mussel field at LHF was investigated. A 16S rRNA gene library was analyzed in combination with functional genes involved in biochemical pathways of CO2 fixation (aclB, cbbM, cbbL) and sulfur oxidation/reduction (soxB, aprA). It turned out, that Epsilonproteobacteria and Gammaproteobacteria comprise a considerable part of the microbial community in diffuse fluids and have the genetic potential to use different pathways for carbon fixation and sulfur oxidation. The bacterial strains obtained from the Eastern Mediterranean deep sea were also analyzed for specifically adapted bacterial strains and antimicrobial activities. Predominantly Gram-positive strains were isolated from the untreated sediment, while incubation of sediment at in situ pressure revealed that Gammaproteobacteria were enriched at the simulated deep-sea conditions. Bacterial strains affiliating to the genus Micromonospora were selected for further analysis in order to investigate their potential to produce bioactive substances. This led to the discovery and structure elucidation of the novel cytotoxic macrolide levantilide A and a derivative thereof, 4 levantilide B, both of which are produced by a deep-sea Micromonospora strain, strain A77. Thus, the results of the present study demonstrate that deep-sea habitats are a promising source for novel bacterial taxa and for the discovery of new natural products as well. Zusammenfassung Im Zuge der hohen Wiederentdeckungsrate bekannter Verbindungen in der heutigen Wirkstoffforschung erscheint es sinnvoll, die Suche auf neue Habitate mit einzigartigen Lebensbedingungen und bislang unbekannten Organismen auszudehnen. Ein solches bislang nur marginal untersuchtes Gebiet stellt die Tiefsee dar. Es ist zu erwarten, dass in der Tiefsee noch viele neue Bakterien-Taxa auf ihre Entdeckung warten, die physiologisch an die extremen Lebensbedingungen angepasst sind und über neue Metabolite verfügen, die wiederum für die biotechnologische oder medizinische Forschung von Interesse sein können. Ziel der vorliegenden Arbeit war es daher, Tiefseebakterien näher zu charakterisieren und sie hinsichtlich ihres Potenzials zur Wirkstoffproduktion zu untersuchen. Mesophile Bakterien wurden von zwei sehr unterschiedlichen Tiefseestandorten isoliert und charakterisiert: die extrem nährstoffarmen Tiefseesedimente des östlichen Mittelmeeres sowie das Logatchev-Hydrothermalfeld (LHF) am Mittelatlantischen Rücken. Die vom LHF isolierten Stämme mit antimikrobieller Aktivität waren hauptsächlich den Gammaproteobakterien zuzuordnen. Unter diesen befand sich auch der Stamm M41T, welcher im Zuge dieser Studien als Repräsentant einer neuen Gattung, Ampritea atlanticaT, beschrieben wurde. Physiologische Untersuchungen dieses von einem Muschelfeld isolierten Stammes zeigten, dass dieser gut an die mesophilen Temperaturen von hydrothermal beeinflussten Gebieten angepasst ist. Des Weiteren wurde die Bakteriengemeinschaft an einer diffusen Fluidaustrittstelle über einem Muschelfeld des LHF untersucht. Die Ergebnisse aus einer 16S rRNA Genbank und die kombinierte Untersuchung von Schlüsselenzymen für verschiedene CO2- Fixierungswege und den Schwefelkreislauf ergaben, dass Epsilonproteobakterien und Gammaproteobakterien einen beachtlichen Teil der Bakteriengemeinschaften auszumachen scheinen und darüber hinaus das genetische Potenzial haben, 5 unterschiedliche Biosynthesewege für die CO2-Fixierung und die Schwefeloxidation zu verwenden. Auch die Isolate aus dem östlichen Mittelmeer wurden hinsichtlich des Vorkommens neuer Arten, spezieller Anpassungen sowie antimikrobieller Aktivitäten untersucht. Während aus den unbehandelten Sedimenten in erster Linie Gram-positive Isolate gewonnen wurden, hatte eine Inkubation des Sedimentes bei in situ Druck eine Verschiebung der Bakteriengemeinschaft, hauptsächlich hin zu Vertretern der Gammaproteobakterien, zur Folge. Von den gewonnenen Isolaten wurden die Vertreter der Gattung Micromonospora für die Suche nach bioaktiven Wirkstoffen ausgewählt. So konnte ein neues zytotoxisch wirksames Makrolid, levantilide A, und ein Derivat, levantilide B, aus einem der Micromonospora-Stämme, Isolat A77, isoliert und beschrieben werden. Die Ergebnisse der vorliegenden Arbeit zeigen, dass aus Tiefsee-Standorten eine Vielzahl unbekannter Bakterien-Taxa kultiviert werden können und dass Tiefseebakterien eine vielversprechende Quelle für neue Wirkstoffe darstellen. 6 Introduction INTRODUCTION 1. Prokaryotic life in the deep sea The historical beginning of deep-sea research is connected to the Challenger Expedition in 1872-1876, which included all major oceans except the Arctic. Only ten years later, first evidence of bacterial life in the deep-sea environment was provided by Certes during the Travaillier and Talisman Expeditions (1883- 1886). Certes found few bacteria in the bottom debris at 5100 m depth and demonstrated growth of these bacteria under hydrostatic pressure. More than 75 % of all ocean water is deep-sea water, being located primarily at depths between 1000 m - 6000 m (Figure 1). Thus, the deep sea can be regarded as the largest habitat on earth (Warrant and Locket, 2004). Unfortunately, there is no strict definition about the minimum depth defining the deep sea and thus the literature data about the deep sea refer to arbitrary water depths from 50 m (the maximum depth for scuba diving), 200 - 300 m (the maximum depth for the penetration of light into the water column) to depths of 1000 m – 6000 m (referring to the various definitions of bathyal, abyssal and hadal). Depths greater than 200 – 300 m are characterized by complete darkness and life in these depths depends on the primary biomass production from the photic zone. Generally, from the continental shelf break at 200 m the temperature rapidly decreases down to 1000 m and does not exceed 5°C in depths greater than 1000 m. Within this thesis, the term “deep sea” refers to water depths of ≥ 1000 m, where hydrostatic pressure of 100 bar persists and raises up to 1100 bar at the world´s deepest point, the Mariana Trench. Apart from several hot spots like cold seeps and hydrothermal vent fields, the majority of the deep-sea bottom surface is covered by soft and muddy sediment. Historically, the deep-sea floor was believed to be an “azoic” zone by Forbes (1844). This “azoic hypothesis” based on Forbes´ dredging work in the Aegean Sea inspired further
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