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Cospeciation and Nitrogen Fixation in the Gut of Dry-Wood Termites

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Cospeciation and Nitrogen Fixation in the Gut of Dry-Wood Termites Bacterial symbionts of termite gut flagellates: cospeciation and nitrogen fixation in the gut of dry-wood termites Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) im Fachbereich Biologie der Philipps-Universität Marburg vorgelegt von Mahesh S. Desai aus Pune, Indien Marburg/Lahn 2008 Die Untersuchungen zur folgenden Arbeit wurden von Oktober 2005 bis Oktober 2008 am Max-Planck-Institut für terrestrische Mikrobiologie in Marburg unter Leitung von Prof. Dr. Andreas Brune durchgeführt. Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation angenommen am: Erstgutachter: Prof. Dr. Andreas Brune Zweitgutachter: Prof. Dr. Rolf Thauer Tag der Disputation: 22.12.2008 Erklärung Ich versichere, dass ich meine Dissertation „Bacterial symbionts of termite gut flagellates: cospeciation and nitrogen fixation in the gut of dry-wood termites” selbständig und ohne unerlaubte Hilfe angefertigt habe und mich keiner als der von mir ausdrücklich bezeichneten Quellen und Hilfen bedient habe. Diese Dissertation wurde in der jetzigen oder einer ähnlichen Form noch bei keiner anderen Hochschule eingereicht und hat noch keinen sonstigen Prüfungszwecken gedient. Marburg, November 2008 List of publications Ikeda-Ohtsubo, W., Desai, M., Stingl, U., and Brune, A. (2007) Phylogenetic diversity of "Endomicrobia" and their specific affiliation with termite gut flagellates. Microbiol 153: 3458–3465. Strassert, J. F. H., Desai, M. S., Brune, A., and Radek, R. The true diversity of devescovinid flagellates in the gut of termite Incisitermes marginipennis. Protist, in revision. Desai, M. S., Strassert, J. F. H., Meuser, K., Ikeda-Ohtsubo, W., Radek, R., Hertel, H., and Brune, A. Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environmental Microbiology, submitted. In preparation Desai, M. S., and Brune, A. Are symbionts of flagellates responsible for nitrogen fixation in the gut of dry-wood termites (Kalotermitidae). Strassert, J., Desai, M. S., Radek, R., and Brune, A. Identification and localization of the multiple bacterial symbionts of the termite gut flagellate Joenia annectens. For my beloved parents Table of Contents 1 General introduction 1 ————————————————————————————— Biology of lower termites 1 Termite hindgut: a structured environment 2 Flagellate symbionts: diversity and functions 3 Bacterial symbionts of flagellates: diversity and functions 5 Nitrogen fixation: a crucial process in the termite gut 7 The aims of this study 9 References 10 2 The true diversity of devescovinid flagellates in the gut of the termite Incisitermes marginipennis 18 ————————————————————————————— Abstract 18 Introduction 19 Results 20 Discussion 30 Experimental procedures 33 References 35 3 Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae) 39 ————————————————————————————— Abstract 39 Introduction 40 Results 43 Discussion 51 Experimental procedures 54 References 57 4 Are symbionts of flagellates responsible for nitrogen fixation in the gut of dry-wood termites (Kalotermitidae)? 62 ————————————————————————————— Abstract 62 Introduction 62 Results 64 Discussion 73 Experimental procedures 75 References 78 5 Hydrogen partial pressures in the gut of dry-wood termites (Kalotermitidae) 82 ————————————————————————————— Abstract 82 Introduction 82 Results and discussion 83 Experimental procedures 85 References 86 6 General discussion 87 ————————————————————————————— Kalotermitidae and devescovinid flagellates: cospeciation or host switching? 87 Coevolutionary history of devescovinids and Bacteroidales ectosymbionts 89 Why are nitrogenase gene expression profiles species-specific? 91 References 93 Summary 97 Zusammenfassung 99 Curriculum vitae 101 Acknowledgement 102 Appendix 103 1General introduction Biology of lower termites Termites are terrestrial, social insects that have gained attention both ecologically and commercially owing to their high abundance and pest nature (Collins, 1989; Lax and Osbrink, 2003). Termites (order: Isoptera) are phylogenetically closely related to cockroaches (Deitz et al., 2003; Inward et al., 2007) and are divided into seven families (Fig. 1) (Abe et al., 2000). Depending on the presence/absence of cellulolytic flagellate protozoa in the hindgut, termites are further distinguished into phylogenetically lower and higher termites, respectively. While higher termites can be fungus-cultivating, wood-feeding or soil-feeding (Abe et al., 2000), lower termites are strictly wood-feeding and depend on their flagellate symbionts for the degradation of lignocellulose (Cleveland, 1926). 1/1 Mastotermitidae Cockroaches 21/448 Kalotermitidae 3/19 Hodotermitidae Isoptera (termites) Flagellates (lower termites) 5/21 Termopsidae 13/359 Rhinotermitidae 2/3 Serritermitidae 247/2007 No flagellates Termitidae (Higher termites) Figure 1. A simplified scheme of the phylogeny of different termite families and closely related cockroaches (modified from Abe et al., 2000). The lower termites harbor flagellates. The numbers on the lines represent the number of genera/species in the different families. The relationship between the lower termites and their gut flagellates is a textbook example of symbiosis. Given the high diversity of lower termites, hardly any species of these termites are thoroughly studied. Notably, termite species of the family Kalotermitidae are very ill studied. Kalotermitidae—found mainly in the tropics—colloquially known as “dry-wood termites” and “primitive termites of General introduction 2 warm region”—live entirely within the single piece of dry wood, and obtain water adsorbed onto wood fibers and by metabolic processes (Noirot, 1970; Abe et al., 2000). Despite being primitive and unique, only a few studies have been performed on the behavioral biology and gut microbial ecology of Kalotermitidae (Fuchs et al., 2003; Korb and Lenz, 2004; Pester and Brune, 2006; Pester and Brune, 2007). Termite hindgut: a structured environment The gut of lower termite consists of foregut, midgut and hindgut (Escherich, 1909). The enlarged hindgut, also known as paunch, is considered as the “hotspot” of the microbial activity (Breznak, 2000; Brune, 2005, and references therein). In the hindgut, the symbiotic microbiota polymerizes cellulose and hemicellulose, which are further fermented to short-chain fatty acids; these short- chain fatty acids are then used as the main energy source by the host termite (Breznak and Brune, 1994). While other studies assumed the termite hindgut to be a completely anoxic fermenter, microelectrode measurements showed steep gradients of oxygen and hydrogen in the hindgut periphery (Fig. 2) (Brune et al., 1995; Ebert and Brune, 1997). Figure 2. Oxygen and hydrogen profiles in the hindgut of the lower termite Reticulitermes flavipes. Employing the microsensor electrodes, both the gases were measured radially in an agarose-embedded hindgut. Oxygen (blue) penetrating into the gut periphery is rapidly consumed by the respiratory activity of the gut microbiota. Hydrogen (red) concentration is the highest at the centre of the gut. (Figure from Brune and Friedrich, 2000). General introduction 3 The rapid removal of oxygen by the respiratory activity of the bacteria creates a microoxic periphery (50-200 µm) around the anoxic centre (Fig. 2). Since termite guts have a high surface area per unit volume, it seems that more than 40% of the paunch is oxic; this clearly makes oxygen an important electron acceptor in the paunch (Brune, 1998). Hydrogen, produced by the anaerobic parabasalid flagellates, is another important metabolite in the paunch. Depending on the termite species, hydrogen concentration can reach up to 70 kPa (Pester and Brune, 2007). The concentration curve of hydrogen shows a steep gradient (Fig. 2). Altogether, the structured environment in the microliter-scaled paunch contains several microhabitats (Brune, 1998). Flagellate symbionts: diversity and functions The hindgut of lower termites is filled with numerous species of oxygen-sensitive flagellates (numbers up to 600,000 per gut), which make up to 33% of the total fresh weight of a termite (Hungate, 1955). 430 described species of flagellates unique to lower termites and wood-feeding cockroach Cryptocercus were listed by Yamin (1979). Electron microscope studies have improved the previously reported classifications of flagellates (Radek, 1992; Brugerolle, 2000 and references therein). Additionally, construction of molecular phylogenies of flagellates from several marker genes has helped to better understand their classification and evolution. (Ohkuma et al., 2000, 2005, 2007; Stingl and Brune, 2003; Gerbod et al., 2004). These flagellates belong to the phylum Parabasalia or the order Oxymonadida (phylum: Preaxostyla) and are believed to be specific to host termites (Kirby, 1937; Kirby, 1949; Honigberg, 1970; Kitade, 2004). The reason behind the host-specificity of flagellates is their supposed vertical transmission, which occurs by the process of proctodeal trophallaxis (Kitade, 2004). Molecular phylogenetic congruence between rhinotermitid termites and their Psuedotrichonympha flagellates supported the notion of vertical transmission (Noda et al. 2007). Furthermore, a recent study showed that the common ancestor of termites and cockroaches acquired flagellate symbionts, and flagellates codiversified with their host termites and cockroaches (Ohkuma et al., 2008). General
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