Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi
Abstract
Many heritable mutualisms, in which beneficial symbionts are transmitted vertically between host generations, originate as antagonisms with parasite dispersal constrained by the host. Only after the parasite gains control over its transmission is the symbiosis expected to transition from antagonism to mutualism. Here, we explore this prediction in the mutualism between the fungus Rhizopus microsporus (Rm, Mucoromycotina) and a beta-proteobacterium Burkholderia, which controls host asexual reproduction. We show that reproductive addiction of Rm to endobacteria extends to mating, and is mediated by the symbiont gaining transcriptional control of the fungal ras2 gene, which encodes a GTPase central to fungal reproductive development. We also discover candidate G-protein-coupled receptors for the perception of trisporic acids, mating pheromones unique to Mucoromycotina. Our results demonstrate that regulating host asexual proliferation and modifying its sexual reproduction are sufficient for the symbiont's control of its own transmission, needed for antagonism-to-mutualism transition in heritable symbioses. These properties establish the Rm-Burkholderia symbiosis as a powerful system for identifying reproductive genes in Mucoromycotina.
- Authors:
-
- Cornell Univ., Ithaca, NY (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Cornell Univ., Ithaca, NY (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1543744
- Alternate Identifier(s):
- OSTI ID: 1619081
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Science & Technology; Other Topics
Citation Formats
Mondo, Stephen J., Lastovetsky, Olga A., Gaspar, Maria L., Schwardt, Nicole H., Barber, Colin C., Riley, Robert, Sun, Hui, Grigoriev, Igor V., and Pawlowska, Teresa E. Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi. United States: N. p., 2017.
Web. doi:10.1038/s41467-017-02052-8.
Mondo, Stephen J., Lastovetsky, Olga A., Gaspar, Maria L., Schwardt, Nicole H., Barber, Colin C., Riley, Robert, Sun, Hui, Grigoriev, Igor V., & Pawlowska, Teresa E. Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi. United States. https://doi.org/10.1038/s41467-017-02052-8
Mondo, Stephen J., Lastovetsky, Olga A., Gaspar, Maria L., Schwardt, Nicole H., Barber, Colin C., Riley, Robert, Sun, Hui, Grigoriev, Igor V., and Pawlowska, Teresa E. Wed .
"Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi". United States. https://doi.org/10.1038/s41467-017-02052-8. https://www.osti.gov/servlets/purl/1543744.
@article{osti_1543744,
title = {Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi},
author = {Mondo, Stephen J. and Lastovetsky, Olga A. and Gaspar, Maria L. and Schwardt, Nicole H. and Barber, Colin C. and Riley, Robert and Sun, Hui and Grigoriev, Igor V. and Pawlowska, Teresa E.},
abstractNote = {Many heritable mutualisms, in which beneficial symbionts are transmitted vertically between host generations, originate as antagonisms with parasite dispersal constrained by the host. Only after the parasite gains control over its transmission is the symbiosis expected to transition from antagonism to mutualism. Here, we explore this prediction in the mutualism between the fungus Rhizopus microsporus (Rm, Mucoromycotina) and a beta-proteobacterium Burkholderia, which controls host asexual reproduction. We show that reproductive addiction of Rm to endobacteria extends to mating, and is mediated by the symbiont gaining transcriptional control of the fungal ras2 gene, which encodes a GTPase central to fungal reproductive development. We also discover candidate G-protein-coupled receptors for the perception of trisporic acids, mating pheromones unique to Mucoromycotina. Our results demonstrate that regulating host asexual proliferation and modifying its sexual reproduction are sufficient for the symbiont's control of its own transmission, needed for antagonism-to-mutualism transition in heritable symbioses. These properties establish the Rm-Burkholderia symbiosis as a powerful system for identifying reproductive genes in Mucoromycotina.},
doi = {10.1038/s41467-017-02052-8},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {Wed Nov 29 00:00:00 EST 2017},
month = {Wed Nov 29 00:00:00 EST 2017}
}
Web of Science
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