Contributes to Nitrogen Utilization, Stress Tolerance, and Virulence in

Overview

Journal Microorganisms

Specialty Microbiology

Date 2023 Mar 29

PMID 36985340

Authors

Dehua Liu

Mei Zhao

Pei Qiao

Zhanhong Li

Gong Chen

Wei Guan

Qingrong Bai

Ron Walcott

Yuwen Yang

Tingchang Zhao

Affiliations

Soon will be listed here.

Abstract

Bacterial fruit blotch (BFB), caused by , severely damages watermelon, melon, and other cucurbit crops worldwide. Nitrogen, one of the most important limiting elements in the environment, is necessary for the growth and reproduction of bacteria. As a nitrogen-regulating gene, plays an important role in maintaining bacterial nitrogen utilization and biological nitrogen fixation. However, the role of has not been determined for . In this study, we constructed a deletion mutant and a corresponding complementary strain in the background of the wild-type strain, Aac5. Through phenotype assays and qRT-PCR analysis, we investigated the role of in in nitrogen utilization, stress tolerance, and virulence against watermelon seedlings. Our results showed that the Aac5 deletion mutant lost the ability to utilize nitrate. The mutant strain also exhibited significantly decreased virulence, in vitro growth, in vivo colonization ability, swimming motility, and twitching motility. In contrast, it displayed significantly enhanced biofilm formation and tolerance to stress induced by oxygen, high salt, and copper ions. The qRT-PCR results showed that the nitrate utilization gene ; the Type III secretion system-related genes , and ; and the pili-related gene were significantly downregulated in the deletion mutant. The nitrate utilization gene , and the flagellum-related genes , and were significantly upregulated in the deletion mutant. The expression levels of gene in the MMX-q and XVM2 media were significantly higher than in the KB medium. These results suggest that the gene plays a pivotal role in the nitrogen utilization, stress tolerance, and virulence of .

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References

Wosten M, van Dijk L, Veenendaal A, de Zoete M, Bleumink-Pluijm N, van Putten J . Temperature-dependent FlgM/FliA complex formation regulates Campylobacter jejuni flagella length. Mol Microbiol. 2010; 75(6):1577-91. DOI: 10.1111/j.1365-2958.2010.07079.x. View

Alford M, Baghela A, Yeung A, Pletzer D, Hancock R . NtrBC Regulates Invasiveness and Virulence of During High-Density Infection. Front Microbiol. 2020; 11:773. PMC: 7214821. DOI: 10.3389/fmicb.2020.00773. View

Qiao P, Zhao M, Guan W, Walcott R, Ye Y, Yang Y . A putative multi-sensor hybrid histidine kinase, BarA , inhibits the expression of the type III secretion system regulator HrpG in . Front Microbiol. 2022; 13:1064577. PMC: 9748350. DOI: 10.3389/fmicb.2022.1064577. View

Battesti A, Majdalani N, Gottesman S . The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol. 2011; 65:189-213. PMC: 7356644. DOI: 10.1146/annurev-micro-090110-102946. View

Cheng A, Zamorano-Sanchez D, Teschler J, Wu D, Yildiz F . NtrC Adds a New Node to the Complex Regulatory Network of Biofilm Formation and Expression in Vibrio cholerae. J Bacteriol. 2018; 200(15). PMC: 6040197. DOI: 10.1128/JB.00025-18. View

Jiang J, Zhao M, Zhang X, Yang L, Fei N, Ji W . Effector AopV Suppresses Plant Immunity and Interacts with Aromatic Dehydratase ADT6 in Watermelon. Int J Mol Sci. 2022; 23(19). PMC: 9570411. DOI: 10.3390/ijms231911719. View

Yeom S, Yeom J, Park W . NtrC-sensed nitrogen availability is important for oxidative stress defense in Pseudomonas putida KT2440. J Microbiol. 2010; 48(2):153-9. DOI: 10.1007/s12275-010-0075-0. View

Zheng S, Bawazir M, Dhall A, Kim H, He L, Heo J . Implication of Surface Properties, Bacterial Motility, and Hydrodynamic Conditions on Bacterial Surface Sensing and Their Initial Adhesion. Front Bioeng Biotechnol. 2021; 9:643722. PMC: 7907602. DOI: 10.3389/fbioe.2021.643722. View

Ji W, Zhao M, Fei N, Yang L, Qiao P, Walcott R . Essential Virulence Gene Activates Host Immune Response against Pathogen. Int J Mol Sci. 2022; 23(16). PMC: 9409176. DOI: 10.3390/ijms23169144. View

10.

Zhang X, Zhao M, Jiang J, Yang L, Yang Y, Yang S . Identification and Functional Analysis of AopN, an Effector that Induces Programmed Cell Death in Plants. Int J Mol Sci. 2020; 21(17). PMC: 7504669. DOI: 10.3390/ijms21176050. View

11.

Gusso C, de Souza E, Rigo L, de Oliveira Pedrosa F, Yates M, de M Rego F . Effect of an ntrC mutation on amino acid or urea utilization and on nitrogenase switch-off in Herbaspirillum seropedicae. Can J Microbiol. 2008; 54(3):235-9. DOI: 10.1139/w07-135. View

12.

Houry A, Briandet R, Aymerich S, Gohar M . Involvement of motility and flagella in Bacillus cereus biofilm formation. Microbiology (Reading). 2009; 156(Pt 4):1009-1018. DOI: 10.1099/mic.0.034827-0. View

13.

Reitzer L . Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol. 2003; 57:155-76. DOI: 10.1146/annurev.micro.57.030502.090820. View

14.

Jiang J, Zou H, Li Y, Chen G . [Expression of the hrcC, hrpE and hpa3 genes is not regulated by the hrpG and hrpX genes in a rice pathogen Xanthomonas oryzae pv. oryzicola]. Wei Sheng Wu Xue Bao. 2009; 49(8):1018-25. View

15.

Yu L, Wu J, Zheng Z, Zhan X, Lin C . Changes of curdlan biosynthesis and nitrogenous compounds utilization characterized in ntrC mutant of Agrobacterium sp. ATCC 31749. Curr Microbiol. 2011; 63(1):60-7. DOI: 10.1007/s00284-011-9942-0. View

16.

Fei N, Ji W, Yang L, Yu C, Qiao P, Yan J . Hcp of the Type VI Secretion System (T6SS) in Group II Strain Aac5 Has a Dual Role as a Core Structural Protein and an Effector Protein in Colonization, Growth Ability, Competition, Biofilm Formation, and Ferric Iron Absorption. Int J Mol Sci. 2022; 23(17). PMC: 9456162. DOI: 10.3390/ijms23179632. View

17.

Cheng B, Meng Y, Cui Y, Li C, Tao F, Yin H . Alkaline Response of a Halotolerant Alkaliphilic Halomonas Strain and Functional Diversity of Its Na+(K+)/H+ Antiporters. J Biol Chem. 2016; 291(50):26056-26065. PMC: 5207076. DOI: 10.1074/jbc.M116.751016. View

18.

Shimizu K . Metabolic Regulation and Coordination of the Metabolism in Bacteria in Response to a Variety of Growth Conditions. Adv Biochem Eng Biotechnol. 2015; 155:1-54. DOI: 10.1007/10_2015_320. View

19.

Lorenz C, Hausner J, Buttner D . HrcQ provides a docking site for early and late type III secretion substrates from Xanthomonas. PLoS One. 2012; 7(11):e51063. PMC: 3511370. DOI: 10.1371/journal.pone.0051063. View

20.

Drepper T, Wiethaus J, Giaourakis D, Gross S, Schubert B, Vogt M . Cross-talk towards the response regulator NtrC controlling nitrogen metabolism in Rhodobacter capsulatus. FEMS Microbiol Lett. 2006; 258(2):250-6. DOI: 10.1111/j.1574-6968.2006.00228.x. View