The roles of actin cytoskeleton and actin-associated protein Crn1p in trap formation of Arthrobotrys oligospora

Zhang, Donghua; Zhu, Xin; Sun, Fengrui; Zhang, Ke‐Qin; Niu, Shanzhuang; Huang, Xiaowei

doi:10.1016/j.resmic.2017.05.001

Cited by 11 publications

(8 citation statements)

References 29 publications

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“…For example, a recent work has generated a strain lacking the signaling scaffold protein Soft and shown that cell-cell fusion is required for ring closure in Duddingtonia flagrans (40). In A. oligospora, ATCC24927-background trapping-deficient mutations have been isolated: adhesin protein Mad1 (41), autophagy protein Atg8 (42), mitogen-activated protein kinase Slt2 (43), pH sensor PalH (44), NADPH oxidase NoxA (45), low-affinity calcium uptake system proteins (46), Rab GTPase Rab7A (38), actin-associated protein Crn1 (47), Woronin body component Hex1 (48), malate synthase Mls (49), glycogen phosphorylase Gph1 (50), transcription factors VelB (51) and StuA (52), and microRNAprocessing protein Qde2 (53), to which we add the G-protein β-subunit Gpb1. However, a mechanistic view of how these and other molecular players are interconnected during the interaction of A. oligospora with their prey is totally lacking.…”

Section: Resultsmentioning

confidence: 99%

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

Yang

Ulzurrun

Gonçalves

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Nematode-trapping fungi (NTF) are a group of specialized microbial predators that consume nematodes when food sources are limited. Predation is initiated when conserved nematode ascaroside pheromones are sensed, followed by the development of complex trapping devices. To gain insights into the coevolution of this interkingdom predator–prey relationship, we investigated natural populations of nematodes and NTF that we found to be ubiquitous in soils.Arthrobotrysspecies were sympatric with various nematode species and behaved as generalist predators. The ability to sense prey among wild isolates ofArthrobotrys oligosporavaried greatly, as determined by the number of traps after exposure toCaenorhabditis elegans. While some strains were highly sensitive toC. elegansand the nematode pheromone ascarosides, others responded only weakly. Furthermore, strains that were highly sensitive to the nematode prey also developed traps faster. The polymorphic nature of trap formation correlated with competency in prey killing, as well as with the phylogeny ofA. oligosporanatural strains, calculated after assembly and annotation of the genomes of 20 isolates. A chromosome-level genome assembly and annotation were established for one of the most sensitive wild isolates, and deletion of the only G-protein β-subunit–encoding gene ofA. oligosporanearly abolished trap formation. In summary, our study establishes a highly responsiveA. oligosporawild isolate as a model strain for the study of fungus–nematode interactions and demonstrates that trap formation is a fitness character in generalist predators of the nematode-trapping fungus family.

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Section: Resultsmentioning

confidence: 99%

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

Yang

Ulzurrun

Gonçalves

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, a recent work has generated a strain lacking the signaling scaffold protein Soft and shown that cell-cell fusion is required for ring closure in Duddingtonia flagrans (41). In A. oligospora , ATCC24927-background trapping-deficient mutants have been isolated: adhesin protein Mad1 (42), autophagy protein Atg8 (43), mitogen-activated protein kinase Slt2 (44), pH sensor PalH (45), NADPH oxidase NoxA (46), low-affinity calcium uptake system proteins Fig1 and Fig2 (47), Rab GTPase Rab7A (48), actin-associated protein Crn1 (49), Woronin body component Hex1 (50), malate synthase Mls (51), glycogen phosphorylase Gph1 (52), transcription factors VelB (53) and StuA (54), and microRNA processing protein Qde2 (55), to which we add the G-protein β subunit Gpb1. However, a mechanistic view of how these and other molecular players are interconnected during the interaction of A. oligospora with their prey is totally lacking.…”

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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“…Deletion of Aog185 may influence the reorganization of actin cytoskeleton, which further results in growth retardation and sporulation capacity reduction, and eventually causes cells to be more sensitive to chemical stressors. In addition, it has been reported that the actin cytoskeleton and actin-associated protein Crn1p are 6 Cellular Microbiology involved in the trap formation of A. oligospora [28]. ADF/ cofilin proteins play important roles in controlling the temporal and spatial extent of actin dynamics, which play key roles in mediating host-pathogen interactions [29].…”

Section: Discussionmentioning

confidence: 99%

Deletion of a Putative GPI-Anchored Protein-Encoding Gene Aog185 Impedes the Growth and Nematode-Trapping Efficiency of Arthrobotrys oligospora by Disrupting Transmembrane Transport Homeostasis

Peng

Dong

et al. 2022

Cellular Microbiology

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Nematode-trapping fungus (NTF) is a crucial predator of nematodes, which can capture nematodes by developing specific trapping devices. However, there is limited understanding of the role and mechanism of cell surface proteins attached to the surface of mycelia or trapping cells. Here, the effects of a putative GPI-anchored protein-encoding gene Aog185 on the growth and nematode-trapping efficiency of A. oligospora were investigated. Compared to the wild-type (WT) strain, the ΔAog185 mutant grew more slowly, exhibited a 20% decrease in conidiation, delayed conidial germination, generated fewer traps, attenuated nematode trapping efficiency, and was more sensitive to chemical stressors. Transcriptomic analysis indicated that a large number of transmembrane transport-related genes were differentially expressed between the WT and ΔAog185 mutant strains. Aog185 deletion could damage the intrinsic components of the membrane and cytoskeleton. Specifically, knockout of Aog185 disrupted transmembrane transport homeostasis during the phagocytosis, cell autophagy, and oxidative phosphorylation processes, which were associated with the fusion of cells and organelle membranes, transport of ions and substrates, and energy metabolism. Hence, the putative GPI-anchored protein-encoding gene Aog185 may contribute to the lifestyle switch of NTF and nematode capture, and the effect of Aog185 gene on cell transmembrane transport is considered key to this process. Our findings provide new insights into the mechanism of Aog185 gene during the process of nematode trapping by NTF.

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The roles of actin cytoskeleton and actin-associated protein Crn1p in trap formation of Arthrobotrys oligospora

Cited by 11 publications

References 29 publications

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

Natural diversity in the predatory behavior facilitates the establishment of a 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

Deletion of a Putative GPI-Anchored Protein-Encoding Gene Aog185 Impedes the Growth and Nematode-Trapping Efficiency of Arthrobotrys oligospora by Disrupting Transmembrane Transport Homeostasis

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