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NopD of Bradyrhizobium sp. XS1150 Possesses SUMO Protease Activity.

ABSTRACT: Effectors secreted by the type III protein secretion system (T3SS) of rhizobia are host-specific determinants of the nodule symbiosis. Here, we have characterized NopD, a putative type III effector of Bradyrhizobium sp. XS1150. NopD was found to possess a functional N-terminal secretion signal sequence that could replace that of the NopL effector secreted by Sinorhizobium sp. NGR234. Recombinant NopD and the C-terminal domain of NopD alone can process small ubiquitin-related modifier (SUMO) proteins and cleave SUMO-conjugated proteins. Activity was abolished in a NopD variant with a cysteine-to-alanine substitution in the catalytic core (NopD-C972A). NopD recognizes specific plant SUMO proteins (AtSUMO1 and AtSUMO2 of Arabidopsis thaliana; GmSUMO of Glycine max; PvSUMO of Phaseolus vulgaris). Subcellular localization analysis with A. thaliana protoplasts showed that NopD accumulates in nuclear bodies. NopD, but not NopD-C972A, induces cell death when expressed in Nicotiana tabacum. Likewise, inoculation tests with constructed mutant strains of XS1150 indicated that nodulation of Tephrosia vogelii is negatively affected by the protease activity of NopD. In conclusion, our findings show that NopD is a symbiosis-related protein that can process specific SUMO proteins and desumoylate SUMO-conjugated proteins.

SUBMITTER: Xiang QW

PROVIDER: S-EPMC7098955 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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NopD of Bradyrhizobium sp. XS1150 Possesses SUMO Protease Activity.

Xiang Qi-Wang QW Bai Juan J Cai Jie J Huang Qin-Ying QY Wang Yan Y Liang Ying Y Zhong Zhi Z Wagner Christian C Xie Zhi-Ping ZP Staehelin Christian C

Frontiers in microbiology 20200320

Effectors secreted by the type III protein secretion system (T3SS) of rhizobia are host-specific determinants of the nodule symbiosis. Here, we have characterized NopD, a putative type III effector of Bradyrhizobium sp. XS1150. NopD was found to possess a functional N-terminal secretion signal sequence that could replace that of the NopL effector secreted by Sinorhizobium sp. NGR234. Recombinant NopD and the C-terminal domain of NopD alone can process small ubiquitin-related modifi ...[more]

PMID: 32265858

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Project description:Strains of the genus Bradyrhizobium associated with agronomically important crops such as soybean (Glycine max) are increasingly studied; however, information about symbionts of wild Glycine species is scarce. Australia is a genetic centre of wild Glycine species and we performed a polyphasic analysis of three Bradyrhizobium strains-CNPSo 4010T, CNPSo 4016T, and CNPSo 4019T-trapped from Western Australian soils with Glycine clandestina, Glycine tabacina and Glycine max, respectively. The phylogenetic tree of the 16S rRNA gene clustered all strains into the Bradyrhizobium japonicum superclade; strains CNPSo 4010T and CNPSo 4016T had Bradyrhizobium yuanmingense CCBAU 10071T as the closest species, whereas strain CNPSo 4019T was closer to Bradyrhizobium liaoningense LMG 18230T. The multilocus sequence analysis (MLSA) with five housekeeping genes-dnaK, glnII, gyrB, recA and rpoB-confirmed the same clusters as the 16S rRNA phylogeny, but indicated low similarity to described species, with nucleotide identities ranging from 93.6 to 97.6% of similarity. Considering the genomes of the three strains, the average nucleotide identity and digital DNA-DNA hybridization values were lower than 94.97 and 59.80 %, respectively, with the closest species. In the nodC phylogeny, strains CNPSo 4010T and CNPSo 4019T grouped with Bradyrhizobium zhanjiangense and Bradyrhizobium ganzhouense, respectively, while strain CNPSo 4016T was positioned separately from the all symbiotic Bradyrhizobium species. Other genomic (BOX-PCR), phenotypic and symbiotic properties were evaluated and corroborated with the description of three new lineages of Bradyrhizobium. We propose the names of Bradyrhizobium agreste sp. nov. for CNPSo 4010T (=WSM 4802T=LMG 31645T) isolated from Glycine clandestina, Bradyrhizobium glycinis sp. nov. for CNPSo 4016T (=WSM 4801T=LMG 31649T) isolated from Glycine tabacina and Bradyrhizobium diversitatis sp. nov. for CNPSo 4019T (=WSM 4799T=LMG 31650T) isolated from G. max.

Project description:The type strain of the prospective 10.1601/nm.30737 sp. nov. ERR11T, was isolated from a nodule of the leguminous tree Erythrina brucei native to Ethiopia. The type strain 10.1601/nm.1463 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+10071 T, was isolated from the nodules of Lespedeza cuneata in Beijing, China. The genomes of ERR11T and 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+10071 T were sequenced by DOE-JGI and deposited at the DOE-JGI genome portal as well as at the European Nucleotide Archive. The genome of ERR11T is 9,163,226 bp in length and has 102 scaffolds, containing 8548 protein-coding and 86 RNA genes. The 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+10071 T genome is arranged in 108 scaffolds and consists of 8,201,522 bp long and 7776 protein-coding and 85 RNA genes. Both genomes contain symbiotic genes, which are homologous to the genes found in the complete genome sequence of 10.1601/nm.24498 10.1601/strainfinder?urlappend=%3Fid%3DUSDA+110 T. The genes encoding for nodulation and nitrogen fixation in ERR11T showed high sequence similarity with homologous genes found in the draft genome of peanut-nodulating 10.1601/nm.27386 10.1601/strainfinder?urlappend=%3Fid%3DLMG+26795 T. The nodulation genes nolYA-nodD2D1YABCSUIJ-nolO-nodZ of ERR11T and 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+10071 T are organized in a similar way to the homologous genes identified in the genomes of 10.1601/strainfinder?urlappend=%3Fid%3DUSDA+110 T, 10.1601/nm.25806 10.1601/strainfinder?urlappend=%3Fid%3DUSDA+4 and 10.1601/nm.1462 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+05525. The genomes harbor hupSLCFHK and hypBFDE genes that code the expression of hydrogenase, an enzyme that helps rhizobia to uptake hydrogen released by the N2-fixation process and genes encoding denitrification functions napEDABC and norCBQD for nitrate and nitric oxide reduction, respectively. The genome of ERR11T also contains nosRZDFYLX genes encoding nitrous oxide reductase. Based on multilocus sequence analysis of housekeeping genes, the novel species, which contains eight strains formed a unique group close to the 10.1601/nm.25806 branch. Genome Average Nucleotide Identity (ANI) calculated between the genome sequences of ERR11T and closely related sequences revealed that strains belonging to 10.1601/nm.25806 branch (10.1601/strainfinder?urlappend=%3Fid%3DUSDA+4 and 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+15615), were the closest strains to the strain ERR11T with 95.2% ANI. Type strain ERR11T showed the highest DDH predicted value with 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+15615 (58.5%), followed by 10.1601/strainfinder?urlappend=%3Fid%3DUSDA+4 (53.1%). Nevertheless, the ANI and DDH values obtained between ERR11T and 10.1601/strainfinder?urlappend=%3Fid%3DCCBAU+15615 or 10.1601/strainfinder?urlappend=%3Fid%3DUSDA+4 were below the cutoff values (ANI???96.5%; DDH???70%) for strains belonging to the same species, suggesting that ERR11T is a new species. Therefore, based on the phylogenetic analysis, ANI and DDH values, we formally propose the creation of 10.1601/nm.30737 sp. nov. with strain ERR11T (10.1601/strainfinder?urlappend=%3Fid%3DHAMBI+3532 T=10.1601/strainfinder?urlappend=%3Fid%3DLMG+30162 T) as the type strain.

Dataset Information

NopD of Bradyrhizobium sp. XS1150 Possesses SUMO Protease Activity.

Publications

NopD of <i>Bradyrhizobium</i> sp. XS1150 Possesses SUMO Protease Activity.

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