P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana

ENA1 and ENA2 are P-type IID/ENA Na+/K+-ATPases required for cellular homeostasis in yeasts but remain poorly understood in filamentous fungal insect pathogens. Here, we characterized seven genes encoding five ENA1/2 homologues (ENA1a–c and ENA2a/b) and two P-type IIC/NK Na+/K+-ATPases (NK1/2) in Be...

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Autores principales:	Ya-Ni Mou, Ben-Jie Gao, Kang Ren, Sen-Miao Tong, Sheng-Hua Ying, Ming-Guang Feng
Formato:	article
Lenguaje:	EN
Publicado:	Taylor & Francis Group 2020
Materias:	entomopathogenic fungi na+/k+ pump genes cellular cation homeostasis vacuolar acidification culture acidification stress response virulence Infectious and parasitic diseases RC109-216
Acceso en línea:	https://doaj.org/article/276837a09f564e1f856c393a3e13f7d9
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spelling	oai:doaj.org-article:276837a09f564e1f856c393a3e13f7d92021-11-17T14:21:59ZP-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana2150-55942150-560810.1080/21505594.2020.1836903https://doaj.org/article/276837a09f564e1f856c393a3e13f7d92020-12-01T00:00:00Zhttp://dx.doi.org/10.1080/21505594.2020.1836903https://doaj.org/toc/2150-5594https://doaj.org/toc/2150-5608ENA1 and ENA2 are P-type IID/ENA Na+/K+-ATPases required for cellular homeostasis in yeasts but remain poorly understood in filamentous fungal insect pathogens. Here, we characterized seven genes encoding five ENA1/2 homologues (ENA1a–c and ENA2a/b) and two P-type IIC/NK Na+/K+-ATPases (NK1/2) in Beauveria bassiana, an insect-pathogenic fungus serving as a main source of fungal insecticides worldwide. Most of these genes were highly responsive to alkaline pH and Na+/K+ cues at transcription level. Cellular Na+, K+ and H+ homeostasis was disturbed only in the absence of ena1a or ena2b. The disturbed homeostasis featured acceleration of vacuolar acidification, elevation of cytosolic Na+/K+ level at pH 5.0 to 9.0, and stabilization of extracellular H+ level to initial pH 7.5 during a 5-day period of submerged incubation. Despite little defect in hyphal growth and asexual development, the Δena1a and Δena2b mutants were less tolerant to metal cations (Na+, K+, Li+, Zn2+, Mn2+ and Fe3+), cell wall perturbation, oxidation, non-cation hyperosmolarity and UVB irradiation, severely compromised in insect pathogenicity via normal cuticle infection, and attenuated in virulence via hemocoel injection. The deletion mutants of five other ENA and NK genes showed little change in vacuolar pH and all examined phenotypes. Therefore, only ENA1a and ENA2b evidently involved in both transmembrane and vacuolar activities are essential for cellular cation homeostasis, insect pathogenicity and multiple stress tolerance in B. bassiana. These findings provide a novel insight into ENA1a- and ENA2b-dependent vacuolar pH stability, cation-homeostatic process and fungal fitness to host insect and environment.Ya-Ni MouBen-Jie GaoKang RenSen-Miao TongSheng-Hua YingMing-Guang FengTaylor & Francis Grouparticleentomopathogenic fungina+/k+ pump genescellular cation homeostasisvacuolar acidificationculture acidificationstress responsevirulenceInfectious and parasitic diseasesRC109-216ENVirulence, Vol 11, Iss 1, Pp 1415-1431 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	entomopathogenic fungi na+/k+ pump genes cellular cation homeostasis vacuolar acidification culture acidification stress response virulence Infectious and parasitic diseases RC109-216
spellingShingle	entomopathogenic fungi na+/k+ pump genes cellular cation homeostasis vacuolar acidification culture acidification stress response virulence Infectious and parasitic diseases RC109-216 Ya-Ni Mou Ben-Jie Gao Kang Ren Sen-Miao Tong Sheng-Hua Ying Ming-Guang Feng P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
description	ENA1 and ENA2 are P-type IID/ENA Na+/K+-ATPases required for cellular homeostasis in yeasts but remain poorly understood in filamentous fungal insect pathogens. Here, we characterized seven genes encoding five ENA1/2 homologues (ENA1a–c and ENA2a/b) and two P-type IIC/NK Na+/K+-ATPases (NK1/2) in Beauveria bassiana, an insect-pathogenic fungus serving as a main source of fungal insecticides worldwide. Most of these genes were highly responsive to alkaline pH and Na+/K+ cues at transcription level. Cellular Na+, K+ and H+ homeostasis was disturbed only in the absence of ena1a or ena2b. The disturbed homeostasis featured acceleration of vacuolar acidification, elevation of cytosolic Na+/K+ level at pH 5.0 to 9.0, and stabilization of extracellular H+ level to initial pH 7.5 during a 5-day period of submerged incubation. Despite little defect in hyphal growth and asexual development, the Δena1a and Δena2b mutants were less tolerant to metal cations (Na+, K+, Li+, Zn2+, Mn2+ and Fe3+), cell wall perturbation, oxidation, non-cation hyperosmolarity and UVB irradiation, severely compromised in insect pathogenicity via normal cuticle infection, and attenuated in virulence via hemocoel injection. The deletion mutants of five other ENA and NK genes showed little change in vacuolar pH and all examined phenotypes. Therefore, only ENA1a and ENA2b evidently involved in both transmembrane and vacuolar activities are essential for cellular cation homeostasis, insect pathogenicity and multiple stress tolerance in B. bassiana. These findings provide a novel insight into ENA1a- and ENA2b-dependent vacuolar pH stability, cation-homeostatic process and fungal fitness to host insect and environment.
format	article
author	Ya-Ni Mou Ben-Jie Gao Kang Ren Sen-Miao Tong Sheng-Hua Ying Ming-Guang Feng
author_facet	Ya-Ni Mou Ben-Jie Gao Kang Ren Sen-Miao Tong Sheng-Hua Ying Ming-Guang Feng
author_sort	Ya-Ni Mou
title	P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
title_short	P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
title_full	P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
title_fullStr	P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
title_full_unstemmed	P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana
title_sort	p-type na+/k+ atpases essential and nonessential for cellular homeostasis and insect pathogenicity of beauveria bassiana
publisher	Taylor & Francis Group
publishDate	2020
url	https://doaj.org/article/276837a09f564e1f856c393a3e13f7d9
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P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana

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