Active invasion of bacteria into living fungal cells

Moebius, Nadine; Üzüm, Zerrin; Dijksterhuis, Jan; Lackner, Gerald; Hertweck, Christian

doi:10.7554/elife.03007

Cited by 118 publications

(113 citation statements)

References 60 publications

(103 reference statements)

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“…In these studies, bacteria were removed via antibiotic treatments and then were reintroduced into their fungal host through coculturing on agar medium or microinjected into the fungal cytoplasm via a laser microbeam (22,30). The production of bacterial chitinolytic enzymes may play an important role in the invasion of bacteria into fungal hyphae in this system (42). The present study demonstrates resynthesis of associations between EHB and foliar fungal endophytes in the Ascomycota, the phylum that includes the vast majority of endophytic and plantpathogenic fungi with relevance to agriculture and natural systems (17).…”

Section: Discussionmentioning

confidence: 99%

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Arendt

Hockett

Araldi-Brondolo

et al. 2016

Appl Environ Microbiol

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bEndohyphal bacteria (EHB) can influence fungal phenotypes and shape the outcomes of plant-fungal interactions. Previous work has suggested that EHB form facultative associations with many foliar fungi in the Ascomycota. These bacteria can be isolated in culture, and fungi can be cured of EHB using antibiotics. Here, we present methods for successfully introducing EHB into axenic mycelia of strains representing two classes of Ascomycota. We first establish in vitro conditions favoring reintroduction of two strains of EHB (Luteibacter sp.) into axenic cultures of their original fungal hosts, focusing on fungi isolated from healthy plant tissue as endophytes: Microdiplodia sp. (Dothideomycetes) and Pestalotiopsis sp. (Sordariomycetes). We then demonstrate that these EHB can be introduced into a novel fungal host under the same conditions, successfully transferring EHB between fungi representing different classes. Finally, we manipulate conditions to optimize reintroduction in a focal EHB-fungal association. We show that EHB infections were initiated and maintained more often under low-nutrient culture conditions and when EHB and fungal hyphae were washed with MgCl 2 prior to reassociation. Our study provides new methods for experimental assessment of the effects of EHB on fungal phenotypes and shows how the identity of the fungal host and growth conditions can define the establishment of these widespread and important symbioses.A s appreciation for their diversity and importance grows, plant microbiomes are increasingly of interest for diverse medical, industrial, and agricultural applications (1, 2). However, many plant-associated microbes remain undescribed (3, 4) and/or are found in association with, or as symbionts of, other microorganisms (5-14, 49-52). One example of these microbial symbioses is that between plant-associated fungi and their bacterial endosymbionts (endobacteria, endofungal bacteria, or endohyphal bacteria [EHB]). Recent studies have indicated that EHB are widespread in rhizosphere fungi from diverse fungal phyla (e.g., mycorrhizal and pathogenic fungi from the Basidiomycota, Glomeromycota, and Mucoromycotina [6][7][8][9][10][11][12][13]) and in the highly diverse Ascomycota that infect roots, stems, and leaves as endophytes (14) (class 3 endophytes, sensu [15]). However, functional relationships have been studied for only a few associations, limiting inferences regarding the scope and potential importance of EHB-fungal associations in ecological interactions and human applications (but see references 16 and 17).Most studies aimed at understanding functional relationships between EHB and fungi have focused on root-associated fungi, especially arbuscular mycorrhizal fungi in the Glomeromycota and plant-pathogenic Rhizopus in the Mucoromycotina (6-11, 18-23). EHB in rhizosphere fungi are often vertically transmitted and host specific, and they frequently maintain obligate relationships with their hosts (18)(19)(20). Although EHB can alter the phenotypes of root-associated fungi and profoundly i...

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Section: Discussionmentioning

confidence: 99%

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Arendt

Hockett

Araldi-Brondolo

et al. 2016

Appl Environ Microbiol

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“…In contrast, axenic cultivation of this macroalga resulted in slowgrowing, callus-like colonies with aberrant cell walls (Grueneberg et al 2016). Another example is the rice seedling blight fungus Rhizopus microsporus and its endosymbiont Burkholderia rhizoxinica that together form an unusual, highly specific alliance that produces the highly potent antimitotic phytotoxin rhizoxin (Moebius et al 2014).…”

Section: Studying Biochemical and Ecological Interactionsmentioning

confidence: 99%

Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions

Garcia¹

2016

Aquat. Microb. Ecol.

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Even though thousands of microbial strains have now been successfully cultivated and described, these only represent a small fraction of global microbial diversity. Moreover, many of the ubiquitous and abundant environmental microorganisms still defy axenic cultivation. Here, I present mixed cultures as a powerful tool to cultivate and study ubiquitous but hard-to-cultivate microorganisms. A mixed culture is a subsample from a complex natural community that contains 2 or more microbial strains. When cultivated together with their metabolic partners, these ubiquitous microorganisms can mutually satisfy metabolic dependencies just as they do in the environment. By reducing the complexity while keeping some diversity, mixed cultures can then be used as model communities. Furthermore, by combining the relative simplicity of these model communities with molecular and bioinformatics tools, the complex natural interactions could be deciphered one model community at a time. Ultimately, mixed cultures can be used to generate a working hypothesis to explore the microbial ecology and genetic population structures of the unseen vast majority of microorganisms.

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“…The endobacteria, in turn, benefit from energy provision by the host (5). Several factors are known to contribute to the ability of Burkholderia endobacteria to form a stable association with the R. microsporus host (6)(7)(8). It remains an enigma, however, as to what fungal factors contribute to symbiosis formation.…”

mentioning

confidence: 99%

Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria

Lastovetsky

Gaspar

Mondo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The recent accumulation of newly discovered fungal-bacterial mutualisms challenges the paradigm that fungi and bacteria are natural antagonists. To understand the mechanisms that govern the establishment and maintenance over evolutionary time of mutualisms between fungi and bacteria, we studied a symbiosis of the fungus Rhizopus microsporus (Mucoromycotina) and its Burkholderia endobacteria. We found that nonhost R. microsporus, as well as other mucoralean fungi, interact antagonistically with endobacteria derived from the host and are not invaded by them. Comparison of gene expression profiles of host and nonhost fungi during interaction with endobacteria revealed dramatic changes in expression of lipid metabolic genes in the host. Analysis of the host lipidome confirmed that symbiosis establishment was accompanied by specific changes in the fungal lipid profile. Diacylglycerol kinase (DGK) activity was important for these lipid metabolic changes, as its inhibition altered the fungal lipid profile and caused a shift in the host-bacterial interaction into an antagonism. We conclude that adjustments in host lipid metabolism during symbiosis establishment, mediated by DGKs, are required for the mutualistic outcome of the Rhizopus-Burkholderia symbiosis. In addition, the neutral and phospholipid profiles of R. microsporus provide important insights into lipid metabolism in an understudied group of oleaginous Mucoromycotina. Lastly, our study revealed that the DGKs involved in the symbiosis form a previously uncharacterized clade of DGK domain proteins. mutualism evolution | antagonism | Mucoromycotina | oleaginous fungi |

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Active invasion of bacteria into living fungal cells

Cited by 118 publications

References 60 publications

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions

Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria

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