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.
Highlights
Many heritable mutualisms, in which beneficial symbionts are transmitted vertically between host generations, originate as antagonisms with parasite dispersal constrained by the host
The role of endobacteria in asexual proliferation of Rm was evidenced by the loss of sporulation in mycelia treated with antibiotics that eradicate Burkholderia[3]
To test the hypothesis that Burkholderia endobacteria control sexual reproduction of Rm, we examined the interactions of wild-type B(+) strains that harbored endobacteria and B(−) isolates that were cured of endosymbionts: (1) ATCC 52813 sex plus (sexP) with ATCC 52814 sex minus (sexM), (2) ATCC 52813 sexP with ATCC 52811 sexM, and (3) ATCC 62417 sexP with ATCC 52811 sexM
Summary
In which beneficial symbionts are transmitted vertically between host generations, originate as antagonisms with parasite dispersal constrained by the host. 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-tomutualism transition in heritable symbioses These properties establish the Rm-Burkholderia symbiosis as a powerful system for identifying reproductive genes in Mucoromycotina. Partner recognition and progression of mating are mediated by trisporic acids and their precursors[8, 9], which act as sex pheromones and are synthesized in a cooperative manner from intermediates provided by the complementary mating partner[10] Due to their recalcitrance to genetic analysis and manipulation, Mucoromycotina are one of the least explored major lineages of fungi, with only few reproductive genes characterized functionally far[11]. We discovered that endobacteria modify sexual reproduction of Rm, and generated insights into the reproductive biology of Mucoromycotina
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