Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes

Araldi-Brondolo, Sarah J.; Spraker, Joseph E.; Shaffer, Justin P.; Woytenko, Emma H.; Baltrus, David A.; Gallery, Rachel E.; Arnold, A. Elizabeth

doi:10.1128/microbiolspec.funk-0056-2016

Cited by 32 publications

(38 citation statements)

References 145 publications

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“…A wide diversity of fungi harbor bacterial endosymbionts that influence fungal phenotypes related to growth, sporulation, and pathogenesis in plants. 94-98 Here we report for the first time a role for a bacterial endosymbiont in animals during infection with R. microsporus , a prevalent causative agent of fatal mucormycosis.…”

Section: Resultsmentioning

confidence: 84%

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

Itabangi

Pcs

Zhou

et al. 2019

Preprint

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Environmentally ubiquitous fungal spores of the Mucorales order cause acute invasive infections through germination and evasion of the mammalian host immune system. Early phagocyte control of spore germination plays a key role in controlling infection, yet swelling Mucorales spores evade phagocytosis through an unknown mechanism. Here we investigate fungal immune evasion in a clinical isolate of Rhizopus microsporus and reveal the role of a bacterial endosymbiont, Ralsonia pickettii, in fungal pathogenesis. Analysis of phagocytosis rates in wild type and cured fungal isolates demonstrates a role for the endosymbiont in immune cell evasion through disruption of the cytoskeleton and phagosome maturation. Further analysis of bacterial secreted products revealed the presence of a previously uncharacterized secondary metabolite whose production is induced by the presence of the fungus. Analysis of the bacterial genome and condition-dependent RNAseq implicate a cryptic type I polyketide synthase. Subsequent analysis of wild type and cured spores in a zebrafish larvae model of infection demonstrate a role for the endosymbiont in suppressing macrophage and neutrophil recruitment to the site of infection. Finally, we demonstrate that this has implications for fungal clearance in an immunocompetent murine model of infection. Together, these findings identify for the first time a role for a bacterial endosymbiont in the pathogenesis of Rhizopus microsporus during animal infection.

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Section: Resultsmentioning

confidence: 84%

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

Itabangi

Pcs

Zhou

et al. 2019

Preprint

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“…The function of a specific microbe or microbial consortia is dynamic and depends on the developmental stage of the host, its age, reproductive state, or physiological condition (4)(5)(6). Several studies have recently found specific host-associated microbiota to contribute to host metabolism (7,8), development (9), organ morphogenesis (10), pathogen protection and immunity (11,12), behavior (13), environmental sensing and adaptation (5,(14)(15)(16)(17)(18)(19), developmental transitions (20)(21)(22)(23), and reproduction (24,25). Conversely, in the absence of a proper microbial community, the functioning of the metaorganism may be compromised, which can result in various diseases; in humans, for instance, anxiety, depression, diabetes, cancer, obesity, and chronic inflammations are linked to microbiome imbalances (6,26,27).…”

mentioning

confidence: 99%

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

Weiland‐Bräuer

Pinnow

Langfeldt

et al. 2020

mBio

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All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita. A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. aurita. IMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita. Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism.

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“…Strains classified within the genus Luteibacter ( Gammaproteobacteria ) are yellow-pigmented members of microbiomes found in close association with plants (1–4). A subset of strains have also been characterized as endohyphal bacteria within a diverse set of ascomycete fungi (5–8). These bacterial/fungal complexes modulate diverse fungal phenotypes, including the potential for some fungi to act as plant growth promoters (5–8).…”

Section: Announcementmentioning

confidence: 99%

“…A subset of strains have also been characterized as endohyphal bacteria within a diverse set of ascomycete fungi (5–8). These bacterial/fungal complexes modulate diverse fungal phenotypes, including the potential for some fungi to act as plant growth promoters (5–8). To increase the amount of genomic information for strains in this genus, we have sequenced a species of Luteibacter originally isolated from rhizosphere soil of Pinus koraiensis (2).…”

Section: Announcementmentioning

confidence: 99%