Neural mechanisms of parasite-induced summiting behavior in “zombie”Drosophila DOI Creative Commons
Carolyn Elya, Danylo Lavrentovich,

Emily Lee

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: Dec. 1, 2022

Abstract For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced mind-controlling parasites. Despite this interest, mechanistic bases of these uncanny processes remained mostly a mystery. Here, we leverage recently established Entomophthora muscae - Drosophila melanogaster “zombie fly” system to reveal molecular and cellular underpinnings summit disease, manipulated behavior evoked many fungal Using new, high-throughput assay measure summiting, discovered that summiting is characterized burst locomotion requires host circadian neurosecretory systems, specifically DN1p neurons, pars intercerebralis corpora allata projecting (PI-CA) neurons (CA), who are solely responsible for juvenile hormone (JH) synthesis release. Summiting fleeting phenomenon, posing challenge physiological biochemical experiments requiring tissue from flies. We addressed with machine learning classifier identify animals in real time. PI-CA CA appear be intact animals, despite E. cells invading brain, particularly superior medial protocerebrum (SMP), neuropil contains axons dendrites. The blood-brain barrier flies late their infection was significantly permeabilized, suggesting factors hemolymph may greater access central nervous during summiting. Metabolomic analysis revealed differential abundance several compounds compared non-summiting Transfusing into recipients locomotion, demonstrating factor(s) likely cause behavior. Altogether, our work reveals neuro-mechanistic model wherein perturb fly’s hemolymph, activating neurohormonal pathway linking clock production CA, ultimately inducing locomotor activity host.

Language: Английский

Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila DOI Creative Commons
Carolyn Elya, Danylo Lavrentovich,

Emily Lee

et al.

eLife, Journal Year: 2023, Volume and Issue: 12

Published: May 15, 2023

For at least two centuries, scientists have been enthralled by the "zombie" behaviors induced mind-controlling parasites. Despite this interest, mechanistic bases of these uncanny processes remained mostly a mystery. Here, we leverage

Language: Английский

Citations

22
Using machine learning to predict protein–protein interactions between a zombie ant fungus and its carpenter ant host DOI Creative Commons
Ian Will, William C. Beckerson, Charissa de Bekker

et al.

Scientific Reports, Journal Year: 2023, Volume and Issue: 13(1)

Published: Aug. 24, 2023

Parasitic fungi produce proteins that modulate virulence, alter host physiology, and trigger responses. These proteins, classified as a type of "effector," often act via protein-protein interactions (PPIs). The fungal parasite Ophiocordyceps camponoti-floridani (zombie ant fungus) manipulates Camponotus floridanus (carpenter ant) behavior to promote transmission. most striking aspect this behavioral change is summit disease phenotype where infected hosts ascend attach an elevated position. Plausibly, interspecific PPIs drive aspects infection manipulation. Machine learning PPI predictions offer high-throughput methods mechanistic hypotheses on how manipulation occurs. Using D-SCRIPT predict host-parasite PPIs, we found ca. 6000 involving 2083 129 which are encoded by genes upregulated during manipulated behavior. We identified multiple overrepresentations functional annotations among these proteins. strongest signals in the highlighted neuromodulatory G-protein coupled receptors oxidation-reduction processes. also detected structural gene-regulatory In parasite, enrichment proteases frequent involvement novel small secreted with unknown functions. From results, provide new potential effectors targets underlying zombie

Language: Английский

Citations

8
Multiomic interpretation of fungus-infected ant metabolomes during manipulated summit disease DOI Creative Commons
Ian Will, Geoffrey M. Attardo, Charissa de Bekker

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Jan. 20, 2023

Abstract Camponotus floridanus ants show altered behaviors followed by a fatal summiting phenotype when infected with manipulating Ophiocordyceps camponoti-floridani fungi. Host as strategy to increase transmission is also observed parasite taxa beyond fungi, including aquatic and terrestrial helminths baculoviruses. The drastic phenotypic changes can sometimes reflect significant physiological within host cells that span molecular levels from metabolites nucleic acids. Nevertheless, the underlying mechanisms still need be fully characterized. To investigate small molecules producing behavior, we C. O. sampled their heads for LC-MS/MS characteristic phenotype. We link this metabolomic data our previous genomic transcriptomic propose underlie manipulated behavior in “zombie ants.” This “multiomic” evidence points toward dysregulation of neurotransmitter neuronal signaling. these processes are during infection manipulation based on 1) differential expression synthesis receptor genes, 2) abundance neurotransmitters (or precursors) known behavioral effects other insects, 3) possible suppression connected immunity pathway. additionally report signals metabolic activity related primary metabolism, detoxification, anti-stress protectants.

Language: Английский

Citations

1
Using machine learning to predict protein-protein interactions between a zombie ant fungus and its carpenter ant host DOI Creative Commons
Ian Will, William C. Beckerson, Charissa de Bekker

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: Sept. 10, 2022

Abstract Parasitic fungi produce proteins that modulate virulence, alter host physiology, and trigger responses. These proteins, classified as a type of “effector,” often act via protein-protein interactions (PPIs). The fungal parasite Ophiocordyceps camponoti-floridani (zombie ant fungus) manipulates Camponotus floridanus (carpenter ant) behavior to promote transmission. most striking aspect this behavioral change is summit disease phenotype where infected hosts ascend attach an elevated position. Plausibly, interspecific PPIs drive aspects infection manipulation. Machine learning PPI predictions offer high-throughput methods mechanistic hypotheses on how manipulation occurs. Using D-SCRIPT predict host-parasite PPIs, we found ca. 6,000 involving 2,083 129 which are encoded by genes upregulated during manipulated behavior. We identified multiple overrepresentations functional annotations among these proteins. strongest signals in the highlighted neuromodulatory G-protein coupled receptors oxidation-reduction processes. also detected structural gene-regulatory In parasite, enrichment proteases frequent involvement novel small secreted with unknown functions. From results, provide new potential effectors targets underlying zombie

Language: Английский

Citations

1
Neural mechanisms of parasite-induced summiting behavior in “zombie”Drosophila DOI Creative Commons
Carolyn Elya, Danylo Lavrentovich,

Emily Lee

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: Dec. 1, 2022

Abstract For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced mind-controlling parasites. Despite this interest, mechanistic bases of these uncanny processes remained mostly a mystery. Here, we leverage recently established Entomophthora muscae - Drosophila melanogaster “zombie fly” system to reveal molecular and cellular underpinnings summit disease, manipulated behavior evoked many fungal Using new, high-throughput assay measure summiting, discovered that summiting is characterized burst locomotion requires host circadian neurosecretory systems, specifically DN1p neurons, pars intercerebralis corpora allata projecting (PI-CA) neurons (CA), who are solely responsible for juvenile hormone (JH) synthesis release. Summiting fleeting phenomenon, posing challenge physiological biochemical experiments requiring tissue from flies. We addressed with machine learning classifier identify animals in real time. PI-CA CA appear be intact animals, despite E. cells invading brain, particularly superior medial protocerebrum (SMP), neuropil contains axons dendrites. The blood-brain barrier flies late their infection was significantly permeabilized, suggesting factors hemolymph may greater access central nervous during summiting. Metabolomic analysis revealed differential abundance several compounds compared non-summiting Transfusing into recipients locomotion, demonstrating factor(s) likely cause behavior. Altogether, our work reveals neuro-mechanistic model wherein perturb fly’s hemolymph, activating neurohormonal pathway linking clock production CA, ultimately inducing locomotor activity host.

Language: Английский

Citations

1