Plasmids of the Rhizobiaceae and Their Role in Interbacterial and Transkingdom Interactions

Pappas, Katherine M.; Cevallos, Miguel A.

doi:10.1007/978-3-642-14512-4_12

Cited by 12 publications

(6 citation statements)

References 208 publications

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“…S1 in the supplemental material), strain CCNWGS0286 belongs to Agrobacterium tumefaciens biovar I. In addition, protelomerase, which is responsible for generating the hairpin ends in the linear DNA, was reported to be present only in biovar I strains (33). A gene encoding protelomerase (ATCR1_05421) was identified in the CCNWGS0286 genome, supporting the finding that this strain belongs to Agrobacterium tumefaciens biovar I.…”

Section: Isolation and Identification Of Agrobacterium Tumefaciens CCsupporting

confidence: 55%

Genome Sequence and Mutational Analysis of Plant-Growth-Promoting Bacterium Agrobacterium tumefaciens CCNWGS0286 Isolated from a Zinc-Lead Mine Tailing

Hao

Xie

Johnstone

et al. 2012

Appl Environ Microbiol

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The plant-growth-promoting bacterium Agrobacterium tumefaciens CCNWGS0286, isolated from the nodules of Robinia pseudoacacia growing in zinc-lead mine tailings, both displayed high metal resistance and enhanced the growth of Robinia plants in a metal-contaminated environment. Our goal was to determine whether bacterial metal resistance or the capacity to produce phytohormones had a larger impact on the growth of host plants under zinc stress. Eight zinc-sensitive mutants and one zinc-sensitive mutant with reduced indole-3-acetic acid (IAA) production were obtained by transposon mutagenesis. Analysis of the genome sequence and of transcription via reverse transcriptase PCR (RT-PCR) combined with transposon gene disruptions revealed that ZntA-4200 and the transcriptional regulator ZntR1 played important roles in the zinc homeostasis of A. tumefaciens CCNWGS0286. In addition, interruption of a putative oligoketide cyclase/lipid transport protein reduced IAA synthesis and also showed reduced zinc and cadmium resistance but had no influence on copper resistance. In greenhouse studies, R. pseudoacacia inoculated with A. tumefaciens CCNWGS0286 displayed a significant increase in biomass production over that without inoculation, even in a zinc-contaminated environment. Interestingly, the differences in plant biomass improvement among A. tumefaciens CCNWGS0286, A. tumefaciens C58, and zinc-sensitive mutants 12-2 (zntA::Tn5) and 15-6 (low IAA production) revealed that phytohormones, rather than genes encoding zinc resistance determinants, were the dominant factor in enhancing plant growth in contaminated soil. P lant-growth-promoting bacteria (PGPB) play a key role in host plant adaptation to metal-contaminated environments through triggering physiological changes in plant cell metabolism so that growing plants can tolerate high concentrations of transition or heavy metals (7,26). PGPB have been isolated from various plants in heavy-metal-contaminated environments (3, 47-49). They were able to enhance plant growth, make plants more tolerant to heavy and transition metals, and thus accelerate phytoremediation by mechanisms including nitrogen fixation, nitrogen and phosphorus metabolism, and the production of siderophores, organic acids, 1-aminocyclopropane-1-carboxylate deaminase (ACC), and phytohormones such as indole-3-acetic acid (IAA), cytokinins, acetoin, and 2,3-butanediol (21, 41, 54). It was reported previously that the existence of high concentrations of metals selected for more metal resistant PGPB to resist these adverse environmental conditions (20,26). However, it is often not known which trait of the PGPB, e.g., tolerance to heavy and transition metals, phytohormones, or a combination of the two, plays the dominant role in the survival of a given plant in a metal-contaminated environment.Agrobacterium tumefaciens is a soilborne alphaproteobacterium belonging to the family Rhizobiaceae whose ability to induce crown gall tumors on dicotyledonous plants makes it of great concern worldwide. Recently, many nonpath...

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Section: Isolation and Identification Of Agrobacterium Tumefaciens CCsupporting

confidence: 55%

Genome Sequence and Mutational Analysis of Plant-Growth-Promoting Bacterium Agrobacterium tumefaciens CCNWGS0286 Isolated from a Zinc-Lead Mine Tailing

Hao

Xie

Johnstone

et al. 2012

Appl Environ Microbiol

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“…In addition to stimulating the production of lipochitooligosaccharides in rhizobia, nod-gene inducing flavonoids also cause changes in the cell surface, including the structural modification of exopolysaccharides (EPS) and lipopolysaccharides (LPS) (Dunn et al 1992;Krishnan et al 2003;Broughton et al 2006;Simsek et al 2009;Ardissone et al 2011;Acosta-Jurado et al 2016). Flavonoids also induce the expression of Type III and Type IV secretion systems in some rhizobia (Pappas and Cevallos 2011). In R. etli, EPS and LPS are important for resistance to coumestrans produced by bean roots and may also suppress plant defense responses (González-Pasayo and Martínez-Romero 2000).…”

Section: Exoproteome Proteins Differentially Expressed In Response To...mentioning

confidence: 99%

The naringenin-induced exoproteome of Rhizobium etli CE3

et al. 2017

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Flavonoids excreted by legume roots induce the expression of symbiotically essential nodulation (nod) genes in rhizobia, as well as that of specific protein export systems. In the bean microsymbiont Rhizobium etli CE3, nod genes are induced by the flavonoid naringenin. In this study, we identified 693 proteins in the exoproteome of strain CE3 grown in minimal medium with or without naringenin, with 101 and 100 exoproteins being exclusive to these conditions, respectively. Four hundred ninety-two (71%) of the extracellular proteins were found in both cultures. Of the total exoproteins identified, nearly 35% were also present in the intracellular proteome of R. etli bacteroids, 27% had N-terminal signal sequences and a significant number had previously demonstrated or possible novel roles in symbiosis, including bacterial cell surface modification, adhesins, proteins classified as MAMPs (microbe-associated molecular patterns), such as flagellin and EF-Tu, and several normally cytoplasmic proteins as Ndk and glycolytic enzymes, which are known to have extracellular "moonlighting" roles in bacteria that interact with eukaryotic cells. It is noteworthy that the transmembrane ß (1,2) glucan biosynthesis protein NdvB, an essential symbiotic protein in rhizobia, was found in the R. etli naringenin-induced exoproteome. In addition, potential binding sites for two nod-gene transcriptional regulators (NodD) occurred somewhat more frequently in the promoters of genes encoding naringenin-induced exoproteins in comparison to those ofexoproteins found in the control condition.

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“…RepABC-type plasmids play a crucial role for the multipartite genome organization and the lifestyle of rhizobia (Pappas and Cevallos, 2011 ). Long-known examples are the pathogenic tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens and the symbiotic nodulation (pSym) plasmids of the genus Rhizobium .…”

Section: Introductionmentioning

confidence: 99%

“…Long-known examples are the pathogenic tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens and the symbiotic nodulation (pSym) plasmids of the genus Rhizobium . RepABC-type plasmids comprise up to 50% of the rhizobial genome and represent the by far most abundant replicon type of these soil bacteria (Pappas and Cevallos, 2011 ). Rhizobium etli CFN42 harbors eight RepABC operons that are located on six extrachromosomal replicons (ECRs; González et al, 2006 ).…”

Section: Introductionmentioning

confidence: 99%

The Composite 259-kb Plasmid of Martelella mediterranea DSM 17316T–A Natural Replicon with Functional RepABC Modules from Rhodobacteraceae and Rhizobiaceae

et al. 2017

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A multipartite genome organization with a chromosome and many extrachromosomal replicons (ECRs) is characteristic for Alphaproteobacteria. The best investigated ECRs of terrestrial rhizobia are the symbiotic plasmids for legume root nodulation and the tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens. RepABC plasmids represent the most abundant alphaproteobacterial replicon type. The currently known homologous replication modules of rhizobia and Rhodobacteraceae are phylogenetically distinct. In this study, we surveyed type-strain genomes from the One Thousand Microbial Genomes (KMG-I) project and identified a roseobacter-specific RepABC-type operon in the draft genome of the marine rhizobium Martelella mediterranea DSM 17316T. PacBio genome sequencing demonstrated the presence of three circular ECRs with sizes of 593, 259, and 170-kb. The rhodobacteral RepABC module is located together with a rhizobial equivalent on the intermediate sized plasmid pMM259, which likely originated in the fusion of a pre-existing rhizobial ECR with a conjugated roseobacter plasmid. Further evidence for horizontal gene transfer (HGT) is given by the presence of a roseobacter-specific type IV secretion system on the 259-kb plasmid and the rhodobacteracean origin of 62% of the genes on this plasmid. Functionality tests documented that the genuine rhizobial RepABC module from the Martelella 259-kb plasmid is only maintained in A. tumefaciens C58 (Rhizobiaceae) but not in Phaeobacter inhibens DSM 17395 (Rhodobacteraceae). Unexpectedly, the roseobacter-like replication system is functional and stably maintained in both host strains, thus providing evidence for a broader host range than previously proposed. In conclusion, pMM259 is the first example of a natural plasmid that likely mediates genetic exchange between roseobacters and rhizobia.

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Plasmids of the Rhizobiaceae and Their Role in Interbacterial and Transkingdom Interactions

Cited by 12 publications

References 208 publications

Genome Sequence and Mutational Analysis of Plant-Growth-Promoting Bacterium Agrobacterium tumefaciens CCNWGS0286 Isolated from a Zinc-Lead Mine Tailing

Genome Sequence and Mutational Analysis of Plant-Growth-Promoting Bacterium Agrobacterium tumefaciens CCNWGS0286 Isolated from a Zinc-Lead Mine Tailing

The naringenin-induced exoproteome of Rhizobium etli CE3

The Composite 259-kb Plasmid of Martelella mediterranea DSM 17316T–A Natural Replicon with Functional RepABC Modules from Rhodobacteraceae and Rhizobiaceae

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