The lifestyle transition of Arthrobotrys oligospora is mediated by microRNA-like RNAs

Abstract

The lifestyle transition of fungi, defined as switching from taking organic material as nutrients to pathogens, is a fundamental phenomenon in nature. However, the mechanisms of such transition remain largely unknown. Here we show microRNA-like RNAs (milRNAs) play a key role in fungal lifestyle transition for the first time. We identified milRNAs by small RNA sequencing in Arthrobotrys oligospora, a known nematode-trapping fungus. Among them, 7 highly expressed milRNAs were confirmed by northern-blot analysis. Knocking out two milRNAs significantly decreased A. oligospora's ability to switch lifestyles. We further identified that two of these milRNAs were associated with argonaute protein QDE-2 by RNA-immunoprecipitation (RIP) analysis. Three of the predicted target genes of milRNAs were found in immunoprecipitation (IP) products of QDE-2. Disruption of argonaute gene qde-2 also led to serious defects in lifestyle transition. Interestingly, knocking out individual milRNAs or qde-2 lead to diverse responses under different conditions, and qde-2 itself may be targeted by the milRNAs. Collectively, it indicates the lifestyle transition of fungi is mediated by milRNAs through RNA interference (RNAi) machinery, revealing the wide existence of miRNAs in fungi kingdom and providing new insights into understanding the adaptation of fungi from scavengers to predators and the mechanisms underlying fungal infections.

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

“…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.…”

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

“…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.…”

AoPEX1 and AoPEX6 Are Required for Mycelial Growth, Conidiation, Stress Response, Fatty Acid Utilization, and Trap Formation in Arthrobotrys oligospora

“…They can trap and digest nematodes using specialized trapping devices (traps), such as adhesive networks and knobs and constricting rings. The development of these traps is a key indicator of their switch from saprophytic to predacious lifestyles ( 19 – 21 ). Arthrobotrys oligospora is a representative species of NT fungi that produces adhesive networks to capture nematodes ( 21 ).…”