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Comparative and genetic analysis of the four sequenced Paenibacillus polymyxa genomes reveals a diverse metabolism and conservation of genes relevant to plant-growth promotion and competitiveness.

Eastman AW, Heinrichs DE, Yuan ZC - BMC Genomics (2014)

Bottom Line: Although a variety of plant-growth promoting traits are encoded by all strains, only P. polymyxa CR1 encodes the unique nitrogen fixation cluster found in other Paenibacillus sp.This study provides an in-depth understanding of the genome architecture of this species, thus facilitating future genetic engineering and applications in agriculture, industry and medicine.Furthermore, this study highlights the current gap in our understanding of complex plant biomass metabolism in Gram-positive bacteria.

View Article: PubMed Central - PubMed

Affiliation: Southern Crop Protection & Food Research Centre, Agriculture & Agri-Food Canada, 1391 Sandford Street, London, Ontario N5V 4 T3, Canada. zyuan27@uwo.ca.

ABSTRACT

Background: Members of the genus Paenibacillus are important plant growth-promoting rhizobacteria that can serve as bio-reactors. Paenibacillus polymyxa promotes the growth of a variety of economically important crops. Our lab recently completed the genome sequence of Paenibacillus polymyxa CR1. As of January 2014, four P. polymyxa genomes have been completely sequenced but no comparative genomic analyses have been reported.

Results: Here we report the comparative and genetic analyses of four sequenced P. polymyxa genomes, which revealed a significantly conserved core genome. Complex metabolic pathways and regulatory networks were highly conserved and allow P. polymyxa to rapidly respond to dynamic environmental cues. Genes responsible for phytohormone synthesis, phosphate solubilization, iron acquisition, transcriptional regulation, σ-factors, stress responses, transporters and biomass degradation were well conserved, indicating an intimate association with plant hosts and the rhizosphere niche. In addition, genes responsible for antimicrobial resistance and non-ribosomal peptide/polyketide synthesis are present in both the core and accessory genome of each strain. Comparative analyses also reveal variations in the accessory genome, including large plasmids present in strains M1 and SC2. Furthermore, a considerable number of strain-specific genes and genomic islands are irregularly distributed throughout each genome. Although a variety of plant-growth promoting traits are encoded by all strains, only P. polymyxa CR1 encodes the unique nitrogen fixation cluster found in other Paenibacillus sp.

Conclusions: Our study revealed that genomic loci relevant to host interaction and ecological fitness are highly conserved within the P. polymyxa genomes analysed, despite variations in the accessory genome. This work suggets that plant-growth promotion by P. polymyxa is mediated largely through phytohormone production, increased nutrient availability and bio-control mechanisms. This study provides an in-depth understanding of the genome architecture of this species, thus facilitating future genetic engineering and applications in agriculture, industry and medicine. Furthermore, this study highlights the current gap in our understanding of complex plant biomass metabolism in Gram-positive bacteria.

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Representation ofPaenibacillus polymyxastrain plasmids. Plasmids from strains M1 (left) and SC2 (right) were annotated in Artemis and visualized using DNAPlotter. Labelled from outside to centre. Outermost ring shows the scale in Mbps, 1st ring; plus-strand CDS (cyan), 2nd ring; minus-strand CDS (cyan), 3rd ring; plus-strand strain specific CDS (purple), 4th ring; minus-strand strain specific CDS (purple), 5th ring; tRNA genes (green), 6th ring; GC-plot where black and grey correspond to above and below average GC content respectively, 7th ring; GC-skew where black and grey correspond to above and below average skew respectively. Strain specific genes were identified using mGenomeSubtractor with an H-value cut off of 0.42. Annotation was obtained from the NCBI GeneBank database. Phage genes, tandem repeats and transposons were identified using PHAST and IS Finder, respectively. rRNA and tRNA genes were obtained from available annotations.
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Fig6: Representation ofPaenibacillus polymyxastrain plasmids. Plasmids from strains M1 (left) and SC2 (right) were annotated in Artemis and visualized using DNAPlotter. Labelled from outside to centre. Outermost ring shows the scale in Mbps, 1st ring; plus-strand CDS (cyan), 2nd ring; minus-strand CDS (cyan), 3rd ring; plus-strand strain specific CDS (purple), 4th ring; minus-strand strain specific CDS (purple), 5th ring; tRNA genes (green), 6th ring; GC-plot where black and grey correspond to above and below average GC content respectively, 7th ring; GC-skew where black and grey correspond to above and below average skew respectively. Strain specific genes were identified using mGenomeSubtractor with an H-value cut off of 0.42. Annotation was obtained from the NCBI GeneBank database. Phage genes, tandem repeats and transposons were identified using PHAST and IS Finder, respectively. rRNA and tRNA genes were obtained from available annotations.

Mentions: Genomic islands (GIs) are thought to be genetic elements acquired during evolution from distantly related organisms and such horizontally transferred genes contribute to genome flux and variation [53, 58]. Initially identified and established as important mediators of virulence in pathogenic bacteria, GIs were subsequently identified in non-pathogenic bacteria from niches such as the rhizosphere [53]. Many GIs encode traits that enhance bacterial fitness including iron-uptake systems, polyketide synthesis clusters, resistance cassettes, symbiosis genes, xenobiotic compound degradation and primary metabolism pathways [58]. The locations of identified genomic islands and their encoded genes are provided in Additional file 2. The majority of CDS in the identified genomic islands are annotated as hypothetical genes although many genomic islands include antibiotic synthesis and resistance genes. Some of the most interesting features encoded within identified genomic islands include a bacitracin synthase in E681 and CR1, bacillorin and β-lactamase in SC2, multidrug efflux pumps and sugar hydrolases in M1, as well as a minimal nif cluster in CR1. In addition, insertion sequences were identified using IS Finder [58] (Figure 5) and their genome locations are provided in Additional file 3. The P. polymyxa strains harbour between 3 and 11 IS elements, and between 1 and 15 transposase containing genomic islands (Figure 5). A large number of transposons, insertion elements, prophages and tandem repeats are contained within genomic islands suggesting P. polymyxa is a common phage target. The plasmids pM1 and pSC2 were visualized using the same method described above (Figure 6). Since the majority of genes encoded by the plasmids have unknown functions only plus and minus strand CDS, strain-specific genes and tRNA genes are presented.Figure 6


Comparative and genetic analysis of the four sequenced Paenibacillus polymyxa genomes reveals a diverse metabolism and conservation of genes relevant to plant-growth promotion and competitiveness.

Eastman AW, Heinrichs DE, Yuan ZC - BMC Genomics (2014)

Representation ofPaenibacillus polymyxastrain plasmids. Plasmids from strains M1 (left) and SC2 (right) were annotated in Artemis and visualized using DNAPlotter. Labelled from outside to centre. Outermost ring shows the scale in Mbps, 1st ring; plus-strand CDS (cyan), 2nd ring; minus-strand CDS (cyan), 3rd ring; plus-strand strain specific CDS (purple), 4th ring; minus-strand strain specific CDS (purple), 5th ring; tRNA genes (green), 6th ring; GC-plot where black and grey correspond to above and below average GC content respectively, 7th ring; GC-skew where black and grey correspond to above and below average skew respectively. Strain specific genes were identified using mGenomeSubtractor with an H-value cut off of 0.42. Annotation was obtained from the NCBI GeneBank database. Phage genes, tandem repeats and transposons were identified using PHAST and IS Finder, respectively. rRNA and tRNA genes were obtained from available annotations.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4209062&req=5

Fig6: Representation ofPaenibacillus polymyxastrain plasmids. Plasmids from strains M1 (left) and SC2 (right) were annotated in Artemis and visualized using DNAPlotter. Labelled from outside to centre. Outermost ring shows the scale in Mbps, 1st ring; plus-strand CDS (cyan), 2nd ring; minus-strand CDS (cyan), 3rd ring; plus-strand strain specific CDS (purple), 4th ring; minus-strand strain specific CDS (purple), 5th ring; tRNA genes (green), 6th ring; GC-plot where black and grey correspond to above and below average GC content respectively, 7th ring; GC-skew where black and grey correspond to above and below average skew respectively. Strain specific genes were identified using mGenomeSubtractor with an H-value cut off of 0.42. Annotation was obtained from the NCBI GeneBank database. Phage genes, tandem repeats and transposons were identified using PHAST and IS Finder, respectively. rRNA and tRNA genes were obtained from available annotations.
Mentions: Genomic islands (GIs) are thought to be genetic elements acquired during evolution from distantly related organisms and such horizontally transferred genes contribute to genome flux and variation [53, 58]. Initially identified and established as important mediators of virulence in pathogenic bacteria, GIs were subsequently identified in non-pathogenic bacteria from niches such as the rhizosphere [53]. Many GIs encode traits that enhance bacterial fitness including iron-uptake systems, polyketide synthesis clusters, resistance cassettes, symbiosis genes, xenobiotic compound degradation and primary metabolism pathways [58]. The locations of identified genomic islands and their encoded genes are provided in Additional file 2. The majority of CDS in the identified genomic islands are annotated as hypothetical genes although many genomic islands include antibiotic synthesis and resistance genes. Some of the most interesting features encoded within identified genomic islands include a bacitracin synthase in E681 and CR1, bacillorin and β-lactamase in SC2, multidrug efflux pumps and sugar hydrolases in M1, as well as a minimal nif cluster in CR1. In addition, insertion sequences were identified using IS Finder [58] (Figure 5) and their genome locations are provided in Additional file 3. The P. polymyxa strains harbour between 3 and 11 IS elements, and between 1 and 15 transposase containing genomic islands (Figure 5). A large number of transposons, insertion elements, prophages and tandem repeats are contained within genomic islands suggesting P. polymyxa is a common phage target. The plasmids pM1 and pSC2 were visualized using the same method described above (Figure 6). Since the majority of genes encoded by the plasmids have unknown functions only plus and minus strand CDS, strain-specific genes and tRNA genes are presented.Figure 6

Bottom Line: Although a variety of plant-growth promoting traits are encoded by all strains, only P. polymyxa CR1 encodes the unique nitrogen fixation cluster found in other Paenibacillus sp.This study provides an in-depth understanding of the genome architecture of this species, thus facilitating future genetic engineering and applications in agriculture, industry and medicine.Furthermore, this study highlights the current gap in our understanding of complex plant biomass metabolism in Gram-positive bacteria.

View Article: PubMed Central - PubMed

Affiliation: Southern Crop Protection & Food Research Centre, Agriculture & Agri-Food Canada, 1391 Sandford Street, London, Ontario N5V 4 T3, Canada. zyuan27@uwo.ca.

ABSTRACT

Background: Members of the genus Paenibacillus are important plant growth-promoting rhizobacteria that can serve as bio-reactors. Paenibacillus polymyxa promotes the growth of a variety of economically important crops. Our lab recently completed the genome sequence of Paenibacillus polymyxa CR1. As of January 2014, four P. polymyxa genomes have been completely sequenced but no comparative genomic analyses have been reported.

Results: Here we report the comparative and genetic analyses of four sequenced P. polymyxa genomes, which revealed a significantly conserved core genome. Complex metabolic pathways and regulatory networks were highly conserved and allow P. polymyxa to rapidly respond to dynamic environmental cues. Genes responsible for phytohormone synthesis, phosphate solubilization, iron acquisition, transcriptional regulation, σ-factors, stress responses, transporters and biomass degradation were well conserved, indicating an intimate association with plant hosts and the rhizosphere niche. In addition, genes responsible for antimicrobial resistance and non-ribosomal peptide/polyketide synthesis are present in both the core and accessory genome of each strain. Comparative analyses also reveal variations in the accessory genome, including large plasmids present in strains M1 and SC2. Furthermore, a considerable number of strain-specific genes and genomic islands are irregularly distributed throughout each genome. Although a variety of plant-growth promoting traits are encoded by all strains, only P. polymyxa CR1 encodes the unique nitrogen fixation cluster found in other Paenibacillus sp.

Conclusions: Our study revealed that genomic loci relevant to host interaction and ecological fitness are highly conserved within the P. polymyxa genomes analysed, despite variations in the accessory genome. This work suggets that plant-growth promotion by P. polymyxa is mediated largely through phytohormone production, increased nutrient availability and bio-control mechanisms. This study provides an in-depth understanding of the genome architecture of this species, thus facilitating future genetic engineering and applications in agriculture, industry and medicine. Furthermore, this study highlights the current gap in our understanding of complex plant biomass metabolism in Gram-positive bacteria.

Show MeSH
Related in: MedlinePlus