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.

Bacterial endosymbionts influence fungal transcriptional profiles with implications for host response in the human fungal pathogensRhizopus microsporusandRhizopus delemar

“…To better understand their relationship to one another, we compared the gene content to explore the similarity and differences between the two species. Previous work has established that the R. delemar genome (45.3 Mb, 17,513 genes) is larger, and contains an increased number of genes, compared to R. microsporus genome (26 Mb, 10,959 genes) (Ma et al 2009; Mondo et al 2017). Our results show that, compared to R. microsporus, the genome of R. delemar is enriched for genes with protein domains (PFAM) associated with ion binding, carbohydrate derivative binding, nucleic acid binding, cytoskeletal protein binding, poly(A) binding, NAD+ ADP-ribosyltransferase activity, protein kinase C activity, translation initiation factor binding and inorganic phosphate transmembrane transporter activity (Supplemental Figure S1, Figure 1d).…”

Environmental interactions with amoebae as drivers of bacterial-fungal endosymbiosis and pathogenicity

“…Fungi harbor a wide diversity of bacterial endosymbionts that are specifically adapted to colonize their fungal hosts and significantly influence host-relevant fungal phenotypes, including metabolism, cell wall organization, development, and plant host colonization 35,58,59,81,90,94,96-106 . Additionally, endobacteria are a source of potent mycotoxins that can influence fungal pathogenesis in plants and insects 59,60,81,90,107,108 .…”

“…We also observed reduced sporulation and overall fitness in this strain after repeated passage of fungal growth on SDA plates with cirpofloxacin. Mondo et al ., showed that bacterial endosymbionts can impact fungal sporulation and development through controlling ras2 , a key GTPase that regulates fungal sexual reproduction 58 . In our companion work examining the response of Rhizopus microsporus to the presence of the endosymbiont_we observed very few changes at the transcriptional level during growth in DMEM.…”

“…Mucormycete plant pathogens, including the Mucorales, are colonized by bacterial endosymbionts of the genera Burkholderia and Ralstonia , closely related to the Pseudomonas genus 35,56 . These endosymbionts influence fungal behavior such as growth and sporulation, and also mediate plant pathogenesis 57,58 . The endotoxin Rhizoxin inhibits plant defenses and is secreted by Burkholderia rhizoxina during mutualism with its fungal host Rhizopus microsporus 59,60 .…”

A TAL effector-like protein of symbioticMycetohabitansincreases stress tolerance and alters the transcriptome of the fungal hostRhizopus microsporus

“…R. microsporus isolates that harbor M. rhizoxinica or other Mycetohabitans spp. require their bacterial partner for asexual and sexual sporulation, while non-host isolates sporulate without bacteria (Partida-Martinez et al, 2007;Lackner et al, 2009;Mondo et al, 2017). As is true for many gram-negative bacterial pathogens and mutualists of plants and animals, M. rhizoxinica requires a type III secretion system (T3SS) to invade its host (He et al, 2004;Lackner et al, 2011a).…”