Inducing novel endosymbioses by implanting bacteria in fungi

Gabriel H. Giger, Chantal Ernst, Ingrid Richter, Thomas Gassler, Christopher M. Field, Anna Sintsova, Patrick Kiefer, Christoph G. Gäbelein, Orane Guillaume–Gentil, Kirstin Scherlach, Miriam Bortfeld-Miller, Tomaso Zambelli, Shinichi Sunagawa, Markus Künzler, Christian Hertweck and Julia A. Vorholt ()
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Gabriel H. Giger: ETH Zurich
Chantal Ernst: ETH Zurich
Ingrid Richter: HKI
Thomas Gassler: ETH Zurich
Christopher M. Field: ETH Zurich
Anna Sintsova: ETH Zurich
Patrick Kiefer: ETH Zurich
Christoph G. Gäbelein: ETH Zurich
Orane Guillaume–Gentil: ETH Zurich
Kirstin Scherlach: HKI
Miriam Bortfeld-Miller: ETH Zurich
Tomaso Zambelli: ETH Zurich
Shinichi Sunagawa: ETH Zurich
Markus Künzler: ETH Zurich
Christian Hertweck: HKI
Julia A. Vorholt: ETH Zurich

Nature, 2024, vol. 635, issue 8038, 415-422

Abstract: Abstract Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification1,2. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect3–5. Here we implant bacteria into the filamentous fungus Rhizopus microsporus to follow the fate of artificially induced endosymbioses. Whereas Escherichia coli implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis, Mycetohabitans rhizoxinica was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.

Date: 2024
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DOI: 10.1038/s41586-024-08010-x

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