Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis

Abstract

Many multicellular organisms rely on symbiotic associations for support of metabolic activity, protection, or energy. Understanding the mechanisms involved in controlling such interactions remains a major challenge. In an unbiased approach we identified key players that control the symbiosis between Hydra viridissima and its photosynthetic symbiont Chlorella sp. A99. We discovered significant up-regulation of Hydra genes encoding a phosphate transporter and glutamine synthetase suggesting regulated nutrition supply between host and symbionts. Interestingly, supplementing the medium with glutamine temporarily supports in vitro growth of the otherwise obligate symbiotic Chlorella, indicating loss of autonomy and dependence on the host. Genome sequencing of Chlorella sp. A99 revealed a large number of amino acid transporters and a degenerated nitrate assimilation pathway, presumably as consequence of the adaptation to the host environment. Our observations portray ancient symbiotic interactions as a codependent partnership in which exchange of nutrients appears to be the primary driving force.

Functions of the Microbiota for the Physiology of Animal Metaorganisms

“…Extensive gene transfer accompanied organelle endosymbiosis over the course of evolution. Similar yet less extensive phenomena can be observed in other cases of endosymbiosis including Aphid-Buchnera , Hydra-Chlorella , and Coral-Symbiodinium symbiosis [54-56]. In all these cases, nitrogen and carbon are exchanged in the form of amino acids in one or both directions.…”

“…This nitrogen is provided in the form of glutamine. In exchange for glutamine, the algae provide photosynthetically fixed carbon in the form of maltose [54]. …”

Promoting synthetic symbiosis under environmental disturbances

“…Communities of bacteria are usually the pioneers in harsh environments, from newly formed volcanic rock to hyper-arid deserts [38, 39, 40]. Some members of the consortia survive by feeding off inorganic matter, but most of the community survives in a cross-feeding network [41]. In such cases, it would be useful to know how the communities function, and especially their fates when the environment has changed due to their presence .…”

Evolutionary “Experiments” in Symbiosis: The Study of Model Animals Provides Insights into the Mechanisms Underlying the Diversity of Host–Microbe Interactions

“…The work has contributed to a paradigm shift in evolutionary immunology: components of the innate immune system with its host-specific antimicrobial peptides appear to have evolved in early branching metazoans because of the need to control the resident beneficial microbes rather than because of www.advancedsciencenews.com www.bioessays-journal.com invasive pathogens. [9] In the Hydra viridissima species, a long-term persistence of symbiotic associations is prevalent not only in two-party interactions of Hydra and symbiotic algae, [39] but also in more complex systems including stably associated bacteria. [36] While so far the epithelial cells of Hydra were considered as prime regulators of the microbiome, recent studies uncovered a previously underappreciated role of the nervous system with its rich repertoire of neuropeptides in controlling resident beneficial microbes.…”