Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants

Fredericksen, Maridel; Zhang, Yizhe; Hazen, Missy L.; Loreto, Raquel G.; Mangold, Colleen A.; Chen, Danny Z.; Hughes, David

doi:10.1073/pnas.1711673114

Cited by 76 publications

(88 citation statements)

References 37 publications

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“…The increased activation of the Ophiocordyceps secretome during manipulation by both species suggests a critical role for secreted compounds in modifying host behavior. This is in line with microscopy evidence demonstrating that fungal cells do not grow invasively into the ant's brain Fredericksen, 2017), but rather likely manipulate behavior peripherally by secreting neuroactive compounds. However, the specific functions of many putatively secreted proteins, upregulated during manipulation, have yet to be determined.…”

Section: Differentially Expressed Putative Fungal Effector Genessupporting

confidence: 87%

“…A metabolomic study identified that the neuroprotectant ergothionine appears to be secreted by O. kimflemingiae during manipulation of C. castaneus . Indeed, neural tissues appear to be among the last tissues to be severely degraded , FREDERICKSEN & al. 2017.…”

Section: Discussionmentioning

confidence: 99%

“…Besides the modification of nutritional physiology, tissue destruction also occurs during infection. Notably, the ants' muscles are affected, leading to muscle atrophy and hypercontraction , FREDERICKSEN & al. 2017, MANGOLD & al.…”

Section: Host Gene Expression Patterns Related To Starvation and Tissmentioning

confidence: 99%

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Genetic underpinnings of host manipulation byOphiocordycepsas revealed by comparative transcriptomics

Will

Das

Trinh

et al. 2020

Preprint

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AbstractThe ant-infecting Ophiocordyceps fungi are globally distributed, host manipulating, specialist parasites that drive aberrant behaviors in infected ants, at a lethal cost to the host. An apparent increase in activity and wandering behaviors precedes a final summiting and biting behavior on to vegetation, positioning the manipulated ant in a site beneficial for fungal growth and transmission. Notably, across Ophiocordyceps species and other known host manipulators, the molecular mechanisms underlying behavioral changes remain largely unclear. We explored possible genetic underpinnings of host manipulation by: (i) producing a hybrid assembly of the Ophiocordyceps camponoti-floridani genome, (ii) conducting laboratory infections coupled with RNAseq of both O. camponoti-floridani and its host, Campontous floridanus, and (iii) using these data for a comparative analysis to similar work performed in Ophiocordyceps kimflemingiae and Camponotus castaneus. We propose differentially expressed genes tied to ant neurobiology, odor response, circadian rhythms, and foraging behavior may be the result of putative fungal effectors such as enterotoxins, aflatrem, and mechanisms disrupting nutrition-sensing or caste-identity pathways.

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Section: Differentially Expressed Putative Fungal Effector Genessupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

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Genetic underpinnings of host manipulation byOphiocordycepsas revealed by comparative transcriptomics

Will

Das

Trinh

et al. 2020

Preprint

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“…Fungi form diverse relationships with viruses, algae, plants, animals, insects, and bacteria, and are critical to human health [15][16][17][18][19][20][21] . Filamentous fungi, in particular, are distinguished by their multinucleate such as Coprinopsis cinera for mushroom genetics, Agaricus bisporus for food, Schizophyllum commune for mushroom morphogenesis, and Phanerochaete chrysosporium for lignocellulosic biomass degradation, are different from the organisms that are used by industry, such as Ganoderma lucidum and Trametes versicolor 11,[58][59][60][61][62][63][64][65][66] .…”

Section: Introductionmentioning

confidence: 99%

Enabling community-based metrology for wood-degrading fungi

Perez

Luccioni

Gaut

et al. 2019

Preprint

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Lignocellulosic biomass could support a greatly-expanded bioeconomy. Current strategies for using biomass typically rely on single-cell organisms and extensive ancillary equipment to produce precursors for downstream manufacturing processes. Alternative forms of bioproduction based on solid-state fermentation and wood-degrading fungi can enable more direct means of manufacture. However, such practices are often ad hoc and not readily reproducible. We sought to develop standard reference strains, substrates, measurements, and methods sufficient to begin to enable reliable reuse of mycological materials and products. Specifically, we show that a widely-available and globallyregularized consumer product (Pringles™) can support the growth of wood-degrading fungi, and that growth on Pringles™ can be correlated with growth on a fully-traceable and compositionally characterized substrate (NIST Reference Material 8492 Eastern Cottonwood Biomass). So established, five laboratories were able to compare measurements of wood-fungus performance via a simple radial extension growth rate assay. Reliable reuse of materials, measures, and methods is necessary to enable distributed bioproduction processes that can be adopted at all scales, from local to industrial. cells, known as hyphae, chitinous-composite cell walls, vast repertoire of degradative enzymes and secondary metabolites, and interconnected networks of cells, known as mycelium, that form through a combination of apical growth, hyphal branching, and regulated self-fusion 22-31 . Growing mycelium penetrate and degrade the substrate upon which the organism lives and uptake and shuttle nutrients throughout complex hyphal networks 23 .Mushrooms, the reproductive structures of wood-degrading filamentous fungi, are widely-used as foodstuffs and as a source of medicines and are consequentially revered by many cultures [30][31][32] .Additionally, mycological materials made from the tissues of mushrooms are used in meat replacements, filtration and remediation of contaminated water, packaging materials, furniture, textiles for the fashion industry, architectural design, art, materials for super capacitors and batteries, anti-viral therapeutics for bees, and nanoparticle synthesis 35,36,45,46,[37][38][39][40][41][42][43][44] . Most commercial mycological materials are fabricated by placing an organism and substrate mixture into a preformed mold and allowing the mycelium to process the substrate via solid-state fermentation. The process itself is typically halted via thermal inactivation followed by downstream processing.Recent studies have elucidated the impacts that choice of organism, genetic modification, substrate composition, and environmental conditions have on the macroscopic properties of mycelium-based materials [47][48][49][50][51][52][53][54] . Most organisms now used to produce mycelium materials are of the class Agaricomycete in the division Basidiomycota. The Agaricomycete are less-extensively studied and developed as some of their Ascomycota counterparts, such as ...

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“…These ants are prone to move to locations favourable to the development of the fungi, and move like robots: the 'zombie ants' (Hughes et al, 2011). The scariest and probably most interesting fact to be investigated is that it was shown that the brain of the ant is unaltered, so as the ant is able to move properly to the location chosen by the fungi (Fredericksen et al, 2017). Other examples have been also described.…”

mentioning

confidence: 99%

Stories of the future: manipulating RNA and Intra/Interkingdom communication

Arraiano

2018

Microbial Biotechnology

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Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants

Cited by 76 publications

References 37 publications

Genetic underpinnings of host manipulation byOphiocordycepsas revealed by comparative transcriptomics

Genetic underpinnings of host manipulation byOphiocordycepsas revealed by comparative transcriptomics

Enabling community-based metrology for wood-degrading fungi

Stories of the future: manipulating RNA and Intra/Interkingdom communication

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