Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi

Zhang, Jian; Miao, Youzhi; Rahimi, Mohammad Javad; Zhu, Hong; Steindorff, Andrei; Schiessler, Sabine; Cai, Feng; Pang, Guan; Chenthamara, Komal; Xu, Yu; Kubicek, Christian P.; Shen, Qirong; Druzhinina, Irina S.

doi:10.1111/1462-2920.14575

Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi

Journal Article · Wed Feb 27 00:00:00 UTC 2019 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.14575· OSTI ID:1591810

Zhang, Jian ^[1]; ^[2]; Rahimi, Mohammad Javad ^[3]; Zhu, Hong ^[2]; Steindorff, Andrei ^[4]; Schiessler, Sabine ^[3]; Cai, Feng ^[1]; Pang, Guan ^[2]; Chenthamara, Komal ^[3]; Xu, Yu ^[2]; Kubicek, Christian P. ^[5]; Shen, Qirong ^[2]; ^[1]

Nanjing Agricultural Univ. (China); Inst. of Chemical, Environmental and Bioscience Engineering (ICEBE), Vienna (Austria)
Nanjing Agricultural Univ. (China)
Inst. of Chemical, Environmental and Bioscience Engineering (ICEBE), Vienna (Austria)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Inst. of Chemical, Environmental and Bioscience Engineering (ICEBE), Vienna (Austria); Steinschoetelgasse, Vienna (Austria)

When resources are limited, the hypocrealean fungus Trichoderma guizhouense can overgrow another hypocrealean fungus Fusarium oxysporum, cause sporadic cell death and arrest growth. A transcriptomic analysis of this interaction shows that T. guizhouense undergoes a succession of metabolic stresses while F. oxysporum responded relatively neutrally but used the constitutive expression of several toxin-encoding genes as a protective strategy. Because of these toxins, T. guizhouense cannot approach it is potential host on the substrate surface and attacks F. oxysporum from above. The success of T. guizhouense is secured by the excessive production of hydrogen peroxide (H₂O₂), which is stored in microscopic bag-like guttation droplets hanging on the contacting hyphae. The deletion of NADPH oxidase nox1 and its regulator, nor1 in T. guizhouense led to a substantial decrease in H₂O₂ formation with concomitant loss of antagonistic activity. We envision the role of NOX proteins in the antagonism of T. guizhouense as an example of metabolic exaptation evolved in this fungus because the primary function of these ancient proteins was probably not linked to interfungal relationships. In support of this, F. oxysporum showed almost no transcriptional response to T. guizhouense Δnox1 strain indicating the role of NOX/H₂O₂ in signalling and fungal communication.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Australian Science Foundation; China Postdoctoral Science Foundation; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1591810

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 8 Vol. 21; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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