Cross-talk in host–parasite associations: What do past and recent proteomics approaches tell us?

Chetouhi, Cherif; Panek, Johan; Bonhomme, Ludovic; ElAlaoui, Hicham; Texier, Catherine; Langin, Thierry; Bekker, Charissa de; Urbach, Serge; Demettre, Edith; Missé, Dorothée; Holzmüller, Philippe; Hughes, David; Zanzoni, Andreas; Brun, Catherine; Biron, David

doi:10.1016/j.meegid.2015.04.015

Cited by 12 publications

(6 citation statements)

References 107 publications

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“…According to various “-omics” studies, parasitic traits, such as host invasion and overcoming the immune system, rely on molecular strategies that share many commonalities across plant and animal parasite species 21 . One would thus expect to observe something similar when investigating possible strategies that fungal parasites use to manipulate the behavior of their animal hosts.…”

Section: Introductionmentioning

confidence: 99%

Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins

Bekker

Ohm

Evans

et al. 2017

Sci Rep

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Much can be gained from revealing the mechanisms fungal entomopathogens employ. Especially intriguing are fungal parasites that manipulate insect behavior because, presumably, they secrete a wealth of bioactive compounds. To gain more insight into their strategies, we compared the genomes of five ant-infecting Ophiocordyceps species from three species complexes. These species were collected across three continents, from five different ant species in which they induce different levels of manipulation. A considerable number of (small) secreted and pathogenicity-related proteins were only found in these ant-manipulating Ophiocordyceps species, and not in other ascomycetes. However, few of those proteins were conserved among them, suggesting that several different methods of behavior modification have evolved. This is further supported by a relatively fast evolution of previously reported candidate manipulation genes associated with biting behavior. Moreover, secondary metabolite clusters, activated during biting behavior, appeared conserved within a species complex, but not beyond. The independent co-evolution between these manipulating parasites and their respective hosts might thus have led to rather diverse strategies to alter behavior. Our data indicate that specialized, secreted enterotoxins may play a major role in one of these strategies.

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Section: Introductionmentioning

confidence: 99%

Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins

Bekker

Ohm

Evans

et al. 2017

Sci Rep

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“…These ancient interactions are often multifaceted (Thomas et al, 2010), with the parasite able to exert control over the host's immune system and endocrine system as well as its behaviour (Beckage and Gelman, 2002). How parasites alter host behaviour remains poorly understood (Adamo, 2013;van Houte et al, 2013;Chetouhi et al, 2015). However, recent evidence suggests that changes in host behaviour require multiple parasitic effects on host physiology (e.g.…”

Section: Introductionmentioning

confidence: 99%

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

Adamo

Kovalko

Turnbull

et al. 2016

Journal of Experimental Biology

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Some parasites alter the behaviour of their hosts. The larvae of the parasitic wasp Cotesia congregata develop within the body of the caterpillar Manduca sexta. During the initial phase of wasp development, the host's behaviour remains unchanged. However, once the wasps begin to scrape their way out of the caterpillar, the caterpillar host stops feeding and moving spontaneously. We found that the caterpillar also temporarily lost sensation around the exit hole created by each emerging wasp. However, the caterpillars regained responsiveness to nociception in those areas within 1 day. The temporary reduction in skin sensitivity is probably important for wasp survival because it prevents the caterpillar from attacking the emerging wasp larvae with a defensive strike. We also found that expression of plasmatocyte spreading peptide (PSP) and spätzle genes increased in the fat body of the host during wasp emergence. This result supports the hypothesis that the exiting wasps induce a cytokine storm in their host. Injections of PSP suppressed feeding, suggesting that an augmented immune response may play a role in the suppression of host feeding. Injection of wasp larvae culture media into non-parasitized caterpillars reduced feeding, suggesting that substances secreted by the wasp larvae may help alter host behaviour.

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“…Part of the mechanisms involved in manipulation of ant behavior might, therefore, be species specific (de Bekker et al 2017a). However, convergently evolved and conserved mechanisms are likely also shared among these specialized Ophiocordyceps fungi as they have common evolutionary histories (Araújo and Hughes 2019) and are confronted with similar ecological obstacles (i.e., the modification of ant behavior to attach to elevated transmission sites) (Chetouhi et al 2015;Loreto et al 2018). Investigating these shared mechanisms across Ophiocordyceps and their host ant species would elucidate the common elements involved and aid in the identification of candidate genes and compounds that are key to establishing manipulation.…”

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confidence: 99%

Genetic Underpinnings of Host Manipulation byOphiocordycepsas Revealed by Comparative Transcriptomics

Will

Das

Trinh

et al. 2020

G3 Genes|Genomes|Genetics

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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 onto vegetation, which positions the manipulated ant in a site beneficial for fungal growth and transmission. We investigated the genetic underpinnings of host manipulation by: (i) producing a high-quality hybrid assembly and annotation of the Ophiocordyceps camponoti-floridani genome, (ii) conducting laboratory infections coupled with RNAseq of O. camponoti-floridani and its host, Camponotus floridanus, and (iii) comparing these data to RNAseq data of Ophiocordyceps kimflemingiae and Camponotus castaneus as a powerful method to identify gene expression patterns that suggest shared behavioral manipulation mechanisms across Ophiocordyceps-ant species interactions. We propose differentially expressed genes tied to ant neurobiology, odor response, circadian rhythms, and foraging behavior may result by activity of putative fungal effectors such as enterotoxins, aflatrem, and mechanisms disrupting feeding behaviors in the ant.

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Cross-talk in host–parasite associations: What do past and recent proteomics approaches tell us?

Cited by 12 publications

References 107 publications

Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins

Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

Genetic Underpinnings of Host Manipulation byOphiocordycepsas Revealed by Comparative Transcriptomics

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