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Impact of N-processes in animal-bacterium associations


Supervisor: Silvia Bulgheresi    

PhD student: Gabriela Paredes

Group: Environmental Cell Biology, Division of Archaea Biology and Ecogenomics, Department of Ecogenomics and Systems Biology




S, C and N Metabolism in Chemosynthetic Marine Nematode Symbioses

My PhD  project explored a fascinating animal-bacterium symbiosis, the one engaging interstitial marine nematodes belonging to the Stilbonematinae. They are unique in the sense that every worm species carries on its surface a “pure culture” of a single Candidatus Thiosymbion phylotype, thereby establishing a one-to-one (binary) ectosymbiosis. Despite being globally distributed in marine sediments and at such high abundances as to potentially influence sediment geochemical cycles, the raison d'être of these symbioses is still eluding us. Also, ironically, although key discoveries have been made researching host immunology and symbiont cell division, we still have not identified which molecules do the partners exchange and whether it is because of this metabolic exchange that the partners associate. Based on their phylogenetic placement and on seminal ecological studies, it has long been hypothesized that the symbionts associate with the nematodes to exploit their vertical migrations through the redox zone, that is to alternatively access O(e- acceptor) in the upper sand layers and sulfide (e- donor) in the deeper ones. Additionally, it has been shown that the symbionts can use nitrate instead of oxygen as e- acceptor. During my PhD I have been testing the “host migrations” hypothesis by subjecting Laxus oneistus to deep sand- and superficial sand-like conditions and comparing their transcripts, proteins, lipids and storage compounds. To this aim, I applied a broad array of techniques including comparative transcriptomics, lipidomics (in cooperation with Y. Chen, Warwick), proteomics (in cooperation with S. Markert, Greifswald) and metabolomics (in cooperation with N. Dubilier, Bremen), comparative RAMAN microscopy, qPCR, stable isotope-based techniques (e.g. 13C and 15N2 incorporation tracking via mass spectrometry and NanoSIMS) and in situ measurements (oxygen, sulfide, DIN, etc.).


Concerning the symbiont, S oxidation and denitrification genes were upregulated under anoxic conditions relative to oxic or hypoxic conditions, whereas stress-related genes were downregulated. Surprisingly, anoxia also enhanced energy metabolism genes such as respiratory chain complexes, II, III and ATP synthesis. As for chemosynthesis, the small subunit of RuBisCo and its regulators were upregulated in hypoxia. Consistently, mass spectrometry data indicated highest 13CO2 incorporation in hypoxia, suggesting that the energy derived from anoxic S oxidation is not exclusively channeled into carbon fixation. Equally surprising was the upregulation of N fixation genes under oxic conditions, given that oxygen is known to inhibit nitrogenase activity. Finally, the symbiont is transcriptionally equipped to take up and exploit carboxylic acids, protons and urea that likely percolate from the nematode cuticle as a consequence of anaerobic fermentation and protein catabolism. All in all, while our data suggest that the symbiont has the metabolic versatility to survive across the redox zone, its metabolism appears optimized to exploit low oxygen concentrations. Thus, we propose that Ca. T. oneisti associates to its host not to take advantage of its migrations through the chemocline, but to exploit its anaerobic fermentation and nitrogen waste products. In return, by detoxifying the sand and possibly serving as energy storage, the symbiont would endow its host to thrive for extended periods in oligotrophic, sulfide-rich and oxygen-depleted environments, typically prohibitive for metazoans. The results I gained on symbiont physiology are about to be submitted for publication (Paredes GF, Viehboeck T, Lee R, Volland JM, Siegfried R, Schintlmeister A, Wagner M, Bulgheresi S, König L. Physiologic and metabolic response of marine nematode symbioses to oxygen. In preparation).

Importantly, my studies on Candidatus Thiosymbion oneisti physiology allow us to make sense of the extraordinary reproductive strategy this symbiont evolved (longitudinal division) and of its invariable spatial disposition (epithelium-like). In this respect, to grasp how symbiont physiology and cell biology are intertwined, I learned how to visualize chromosomal loci in cooperation with N. Dubilier, Bremen and contributed to determine Ca. T. oneisti chromosome configuration (Weber, PM, Moessel F, Paredes GF, Viehboeck T, Fischer N, Bulgheresi S. Symbionts maintain their chromosome orientation toward their host through a bidimensional segregation mode. 2019. Current Biology, in revision).

As for the host physiology, I will analyze it in the last months of my PhD and I expect that knowledge on the holobiont (host plus symbiont) will help us to understand how marine nematode symbioses could contribute to the cycling of S, C, and N in marine shallow water sediments.


The DK+ program: Microbial Nitrogen Cycling from Microbial Nitrogen Cycling - From Single Cells to Ecosystems has personally offered me the great opportunity to broaden my education by: (i) gaining further insight into new microbe-host working systems during my Secondments at the University of the French West Indies (Guadeloupe-France) and at the Max Planck Institute for Marine Microbiology (Bremen, Germany), (ii) allowing my participation in over six conferences around the world, where I interacted and networked with the leading scientist on the symbiotic community and (iii) financing and encouraging the use of cutting-edge techniques such as Nanoscale secondary ion mass spectrometry (NanoSIMS), among others.


Please find a list of publications here.

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