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Metabolic diversity in the chemoautotrophic Riftia pachyptila symbiont

Subject Area Metabolism, Biochemistry and Genetics of Microorganisms
Microbial Ecology and Applied Microbiology
Term from 2014 to 2018
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 268708926
 
Final Report Year 2020

Final Report Abstract

“Candidatus Endoriftia persephone”, thioautotrophic bacterial endosymbiont of the deep-sea tubeworm Riftia pachyptila, has a remarkably versatile repertoire of metabolic capacities. It employs two CO2 fixation pathways, generates energy by oxidizing sulfide, thiosulfate and hydrogen, and it can use both, oxygen and nitrate, as terminal electron acceptors. Seeing all of these routes expressed simultaneously in the symbiont population of the same tubeworm host in previous studies, we asked whether these pathways could occur in the same symbiont cell, or rather in separate symbiont subpopulations. As Riftia symbionts were known to exist in different cell shapes and sizes, depending on the stage of their life cycle, we hypothesized that these “morphotypes” might correspond to metabolically distinct subpopulations in the symbiont-containing host tissue, the trophosome. To evaluate this hypothesis, we used gradient centrifugation to selectively enrich symbiont cells of different sizes. This approach allowed us to perform metaproteomic analyses on individual symbiont size classes. Our analyses revealed that, inside its host’s cells, Endoriftia undergoes a gradual differentiation or aging process from small, actively dividing cells to large, nondividing symbionts, which produce large amounts of organic material and are subsequently digested by the host. We observed a “division of labor” between these small and large Riftia symbionts. Small symbionts presumably function as stem cells of the symbiont population. Their proteome is particularly devoted to cell division, stress response and host interaction, and their gene expression is tightly regulated, focusing only on the most essential pathways, similar to the situation in exponentially growing free-living bacteria. In contrast, gene expression in large Riftia symbionts is dedicated to biomass production using both CO2 fixation pathways and all of the available energygenerating mechanisms, and seems to be less stringently regulated. Constantly supplied with all necessary substrates by the host, Endoriftia cells do not seem to reach stationary phase; on the contrary, they can apparently afford to employ much of their metabolic repertoire at the same time. In conclusion, the previously observed metabolic diversity in mixtures of Riftia symbionts from the same host is probably due to an “advantageous deregulation” of gene expression in large Endoriftia, which leads to a high degree of metabolic redundancy within the same symbiont cells, and which likely presents a symbiosis-specific adaptation that benefits the symbiosis as a whole. Additional symbiosis-specific adaptations in the Riftia holobiont were revealed by our metaproteomic comparison of symbiont-containing and symbiont-free Riftia tissues. We found a variety of molecular level interaction processes and strategies, which facilitate coexistence of symbiont and host. For instance, Riftia not only digests its symbionts for nutrition, but also invests a considerable share of its proteome to transferring CO2, H2S and O2 to the symbiont, thus promoting bacterial biomass production, whereas the symbiont provides the host with ammonium. To maintain its symbiont population, the host furthermore appears to create relatively low oxygen levels in the trophosome, which may benefit the microaerophilic symbiont. At the same time, Riftia’s immune system appears to be involved in restricting the symbionts to their compartments, i.e., to control symbiont population size. The symbiont’s eukaryote-like proteins and a highly abundant porin may, in turn, enable the symbiont to communicate with the host and to evade host digestion or interference, thus allowing Endoriftia to persist inside the eukaryotic cells. Striking similarities of the eukaryote-like proteins to virulence-associated proteins of pathogens suggest that mutualistic and pathogenic bacteria employ common strategies of microbe-host interactions. Interactions in Riftia are notably influenced by the energy regime, as exemplified by the observation that symbiont biomass is drastically reduced during energy limitation. Under these circumstances, i) the host digests more symbionts to cover its energy demands, ii) the symbionts are less productive, and iii) the symbionts divide less frequently. Interestingly, while carbon fixation by the Calvin cycle decreases markedly upon energy limitation, CO2 fixation by the rTCA cycle does not, suggesting that metabolic versatility may be particularly advantageous during adverse environmental conditions.

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