CZT-1 Is a Novel Transcription Factor Controlling Cell Death and Natural Drug Resistance in <i>Neurospora crassa</i>

Gonçalves, A. Pedro; Hall, Charles R.; Kowbel, David; Glass, N. Louise; Videira, Arnaldo

doi:10.1534/g3.114.011312

Cited by 16 publications

(29 citation statements)

References 57 publications

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“…Phenotypic diversity is commonly observed in natural populations of fungi. For example, variations in stress sensitivity have been observed in Saccharomyces cerevisiae (18) and Neurospora crassa (19). Two previous studies have surveyed A. oligospora in the wild (20, 21) but no phenotypical characterization has been performed.…”

Section: Resultsmentioning

confidence: 99%

Natural diversity in the predatory behavior facilitates the establishment of a new robust model strain for nematode-trapping fungi

Yang

Ulzurrun

Gonçalves

et al. 2019

Preprint

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33Nematode-trapping fungi (NTF) are a group of specialized microbial predators that consume 34 nematodes when food sources are limited. Predation is initiated when conserved nematode 35 ascaroside pheromones are sensed, followed by the development of complex trapping devices. 36To gain insights into the co-evolution of this inter-kingdom predator-prey relationship, we 37 investigated natural populations of nematodes and NTF, that we found to be ubiquitous in soils. 38Arthrobotrys species were sympatric with various nematode species and behaved as generalist 39 predators. The ability to sense prey amongst wild isolates of A. oligospora varied greatly, as 40 determined by the number of traps after exposure to Caenorhabditis elegans. While some strains 41 were highly sensitive to C. elegans and the nematode pheromone ascarosides, others responded 42 only weakly. Furthermore, strains that were highly sensitive to the nematode prey also developed 43 traps faster. The polymorphic nature of trap formation correlated with competency in prey 44 killing, as well as with the phylogeny of A. oligospora natural strains, calculated after assembly 45 and annotation of the genomes of twenty isolates. A chromosome level genome assembly and 46 annotation was established for one of the most sensitive wild isolate, and deletion of the only G 47 protein b subunit-encoding gene of A. oligospora nearly abolished trap formation, implicating G 48 protein signaling in predation. In summary, our study establishes a highly responsive A. 49 oligospora wild isolate as a novel model strain for the study of fungal-nematode interactions and 50 demonstrates that trap formation is a fitness character in generalist predators of the NTF family. 51 52 Significance statement 53Nematode-trapping fungi (NTF) are carnivorous microbes that hold potential to be used 54 as biological control agents due to their ability to consume nematodes. In this work we show that 55 NTF are ubiquitous generalist predators found in sympatry with their prey in soil samples. Wild 56 isolates of NTF displayed a naturally diverse ability to execute their predatory lifestyle. We 57 generated a large whole genome sequencing dataset for many of the fungal isolates that will 58 serve as the basis of future projects isolates. In particular, we establish TWF154, a highly 59 responsive strain of Arthrobotrys oligospora, as a model strain to study the genetics of NTF. 60Lastly, we provide evidence that G-protein signaling is necessary for trap induction in NTF. 61 62 63 64The living component of soils are in permanent interaction and play central roles in 65 various aspects of biogeochemistry, including nutrient cycling and transport across distances (1). 66Specifically, nematodes are the most abundant animals in nature, amounting to a staggering 0.3 67 gigatonnes or 4.5 x 10 20 individuals, many of which are devastating parasites of plants, animals 68 and humans (2). Although available, nematicide chemicals pose severe environmental and health 69 risks and therefore, biological cont...

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Section: Resultsmentioning

confidence: 99%

Natural diversity in the predatory behavior facilitates the establishment of a new robust model strain for nematode-trapping fungi

Yang

Ulzurrun

Gonçalves

et al. 2019

Preprint

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“…rotenone and staurosporine) also increase levels of intracellular oxidative stress associated with subsequent cellular death. 35,36 Increase in associated ROS by chitosan could induce plasma membrane free fatty acid oxidation and formation of oxylipins. 37 These would damage plasma membrane and cause its subsequent permeabilization.…”

Section: Resultsmentioning

confidence: 99%

Neurospora crassa transcriptomics reveals oxidative stress and plasma membrane homeostasis biology genes as key targets in response to chitosan

et al. 2016

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Chitosan is a natural polymer with antimicrobial activity. Chitosan causes plasma membrane permeabilization and induction of intracellular reactive oxygen species (ROS) in Neurospora crassa. We have determined the transcriptional profile of N. crassa to chitosan and identified the main gene targets involved in the cellular response to this compound. Global network analyses showed membrane, transport and oxidoreductase activity as key nodes affected by chitosan. Activation of oxidative metabolism indicates the importance of ROS and cell energy together with plasma membrane homeostasis in N. crassa response to chitosan. Deletion strain analysis of chitosan susceptibility pointed, NCU03639 encoding a class 3 lipase, involved in plasma membrane repair by lipid replacement and NCU04537 a MFS monosaccharide transporter related with assimilation of simple sugars, as main gene targets of chitosan. NCU10521, a glutathione S-transferase-4 involved in the generation of reducing power for scavenging intracellular ROS is also a determinant chitosan gene target. Ca2+ increased tolerance to chitosan in N. crassa. Growth of NCU10610 (fig 1 domain) and SYT1 (a synaptotagmin) deletion strains was significantly increased by Ca2+ in presence of chitosan. Both genes play a determinant role in N. crassa membrane homeostasis. Our results are of paramount importance for developing chitosan as antifungal.

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“…In summary, we show that the effects of the antifungal 1314151650 and anticancer 51 agent staurosporine are robustly modulated by the accessibility to Ca 2+ in the culture medium. The amount of extracellular Ca 2+ affects staurosporine-triggered intracellular events like Ca 2+ signaling, the production of ROS and cell death.…”

Section: Discussionmentioning

confidence: 76%

Extracellular calcium triggers unique transcriptional programs and modulates staurosporine-induced cell death in Neurospora crassa

Gonçalves¹,

Monteiro

Lucchi

et al. 2014

MIC

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Alterations in the intracellular levels of calcium are a common response to cell death stimuli in animals and fungi and, particularly, in the Neurospora crassa response to staurosporine. We highlight the importance of the extracellular availability of Ca2+ for this response. Limitation of the ion in the culture medium further sensitizes cells to the drug and results in increased accumulation of reactive oxygen species (ROS). Conversely, an approximately 30-fold excess of external Ca2+ leads to increased drug tolerance and lower ROS generation. In line with this, distinct staurosporine-induced cytosolic Ca2+ signaling profiles were observed in the absence or presence of excessive external Ca2+. High-throughput RNA sequencing revealed that different concentrations of extracellular Ca2+ define distinct transcriptional programs. Our transcriptional profiling also pointed to two putative novel Ca2+-binding proteins, encoded by the NCU08524 and NCU06607 genes, and provides a reference dataset for future investigations on the role of Ca2+ in fungal biology.

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CZT-1 Is a Novel Transcription Factor Controlling Cell Death and Natural Drug Resistance in Neurospora crassa

Cited by 16 publications

References 57 publications

Natural diversity in the predatory behavior facilitates the establishment of a new robust model strain for nematode-trapping fungi

Natural diversity in the predatory behavior facilitates the establishment of a new robust model strain for nematode-trapping fungi

Neurospora crassa transcriptomics reveals oxidative stress and plasma membrane homeostasis biology genes as key targets in response to chitosan

Extracellular calcium triggers unique transcriptional programs and modulates staurosporine-induced cell death in Neurospora crassa

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