Description of a novel species of Leclercia, Leclercia tamurae sp. nov. and proposal of a novel genus Silvania gen. nov. containing two novel species Silvania hatchlandensis sp. nov. and Silvania confinis sp. nov. isolated from the rhizosphere of oak

Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disea...

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Published inBMC microbiology Vol. 22; no. 1; pp. 289 - 18
Main Authors Maddock, Daniel, Arnold, Dawn, Denman, Sandra, Brady, Carrie
Format Journal Article
LanguageEnglish
Published London BioMed Central 02.12.2022
BioMed Central Ltd
BMC
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ISSN1471-2180
1471-2180
DOI10.1186/s12866-022-02711-x

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Abstract Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed ‘healthy’ trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia , of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Results Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Conclusion Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3 T  = LMG 32609 T  = CCUG 76176 T ), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6 T  = LMG 32608 T  = CCUG 76185 T ) and Silvania confinis sp. nov. (type strain H4N4 T  = LMG 32607 T  = CCUG 76175 T ). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
AbstractList Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed 'healthy' trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3.sup.T = LMG 32609.sup.T = CCUG 76176.sup.T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6.sup.T = LMG 32608.sup.T = CCUG 76185.sup.T) and Silvania confinis sp. nov. (type strain H4N4.sup.T = LMG 32607.sup.T = CCUG 76175.sup.T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
Abstract Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed ‘healthy’ trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Results Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Conclusion Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3T = LMG 32609T = CCUG 76176T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6T = LMG 32608T = CCUG 76185T) and Silvania confinis sp. nov. (type strain H4N4T = LMG 32607T = CCUG 76175T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed 'healthy' trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Results Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Conclusion Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3.sup.T = LMG 32609.sup.T = CCUG 76176.sup.T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6.sup.T = LMG 32608.sup.T = CCUG 76185.sup.T) and Silvania confinis sp. nov. (type strain H4N4.sup.T = LMG 32607.sup.T = CCUG 76175.sup.T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health. Keywords: Acute oak decline, Rhizosphere, Leclercia, Plant growth promoting bacteria, Plant growth-promoting traits, Enterobacteriaceae, Silvania
Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed 'healthy' trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere.BACKGROUNDAcute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed 'healthy' trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere.Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation.RESULTSPartial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation.Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3T = LMG 32609T = CCUG 76176T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6T = LMG 32608T = CCUG 76185T) and Silvania confinis sp. nov. (type strain H4N4T = LMG 32607T = CCUG 76175T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.CONCLUSIONBased on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3T = LMG 32609T = CCUG 76176T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6T = LMG 32608T = CCUG 76185T) and Silvania confinis sp. nov. (type strain H4N4T = LMG 32607T = CCUG 76175T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed 'healthy' trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3  = LMG 32609  = CCUG 76176 ), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6  = LMG 32608  = CCUG 76185 ) and Silvania confinis sp. nov. (type strain H4N4  = LMG 32607  = CCUG 76175 ). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed ‘healthy’ trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia , of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Results Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Conclusion Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3 T  = LMG 32609 T  = CCUG 76176 T ), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6 T  = LMG 32608 T  = CCUG 76185 T ) and Silvania confinis sp. nov. (type strain H4N4 T  = LMG 32607 T  = CCUG 76175 T ). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the Middle East, indicate that the distribution and host range is increasing at an alarming rate. The stem weeping symptoms of the disease partially develop due to polymicrobial-host interaction, caused by several members of the order Enterobacterales. While investigating the rhizosphere soil of AOD-unaffected trees, termed ‘healthy’ trees, and diseased oaks suffering from Acute Oak Decline (AOD), an enrichment method designed for enhanced recovery of Enterobacterales led to the recovery of several isolates that could not be classified as any existing species. These isolates showed a close relationship to the genus Leclercia, of which both species are of clinical importance, but the type species Leclercia adecarboxylata also displays plant growth-promoting properties in the rhizosphere. Results Partial sequencing of four housekeeping genes revealed similarity to the genus Leclercia with varying degrees of relatedness. As such a complete polyphasic approach was used to determine the true taxonomic position of these isolates. This involved whole genome sequencing, phylogenomic analysis, phylogenetic analysis of both the 16S rRNA and four housekeeping gene sequences, combined with phenotypic testing and fatty acid analysis. Both the phylogenomic and phylogenetic analyses separated the isolates into four clusters, two of which were contained in the Leclercia clade. The remaining two clusters formed a separate lineage far removed from any currently defined species. Further investigation into the role of the isolates as plant growth-promoting bacteria as well as plant pathogens was investigated computationally, revealing a number of plant growth-promoting traits as well as virulence genes related to motility, adhesion and immune modulation. Conclusion Based on the genotypic and phenotypic data presented here, these isolates could be differentiated from each other and their closest neighbours. As such we propose the description of Leclercia tamurae sp. nov. (type strain H6S3T = LMG 32609T = CCUG 76176T), Silvania gen. nov., Silvania hatchlandensis sp. nov. (type strain H19S6T = LMG 32608T = CCUG 76185T) and Silvania confinis sp. nov. (type strain H4N4T = LMG 32607T = CCUG 76175T). Due to their interesting protein annotations and alignments, these species warrant further investigation for their role in relation to plant health.
ArticleNumber 289
Audience Academic
Author Arnold, Dawn
Maddock, Daniel
Brady, Carrie
Denman, Sandra
Author_xml – sequence: 1
  givenname: Daniel
  surname: Maddock
  fullname: Maddock, Daniel
  organization: Centre for Research in Bioscience, School of Applied Sciences, University of the West of England
– sequence: 2
  givenname: Dawn
  surname: Arnold
  fullname: Arnold, Dawn
  organization: Harper Adams University
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  givenname: Sandra
  surname: Denman
  fullname: Denman, Sandra
  organization: Centre for Ecosystems, Society and Biosecurity, Forest Research
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  givenname: Carrie
  surname: Brady
  fullname: Brady, Carrie
  email: carrie.brady@uwe.ac.uk
  organization: Centre for Research in Bioscience, School of Applied Sciences, University of the West of England
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36460957$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_1016_j_jbiotec_2024_08_004
crossref_primary_10_1099_ijsem_0_005812
crossref_primary_10_1099_ijsem_0_005923
crossref_primary_10_3389_fpls_2024_1437947
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Issue 1
Keywords Acute oak decline
Plant growth promoting bacteria
Rhizosphere
Plant growth-promoting traits
Silvania
Leclercia
Enterobacteriaceae
Language English
License 2022. The Author(s).
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Snippet Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe...
Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe and the...
Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such as Europe...
Abstract Background Acute Oak Decline (AOD) is a decline disease first reported on native oaks in the UK, but in recent years reports from further afield such...
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StartPage 289
SubjectTerms Acute oak decline
Annotations
Bacteria
Bacteria, Phytopathogenic
Biological Microscopy
Biomedical and Life Sciences
Clusters
Composition
Decline
Disease
Diseases and pests
Enterobacter
Enterobacterales
Enterobacteriaceae
Enterobacteriaceae - genetics
Environmental aspects
Fatty acids
Gammaproteobacteria
Gene sequencing
Genes
Genetic aspects
Genetic diversity
Genomes
Host range
Identification and classification
Immunomodulation
Leclercia
Life Sciences
Microbiology
Mycology
New species
Oak
Parasitology
Parks & recreation areas
Phylogenetics
Phylogeny
Physiological aspects
Plant growth
Plant growth promoting bacteria
Plant growth-promoting traits
Quercus
Recovery
Rhizosphere
RNA, Ribosomal, 16S - genetics
rRNA 16S
Signs and symptoms
Species classification
Taxonomy
Trees
Virology
Virulence
Virulence (Microbiology)
Whole genome sequencing
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Title Description of a novel species of Leclercia, Leclercia tamurae sp. nov. and proposal of a novel genus Silvania gen. nov. containing two novel species Silvania hatchlandensis sp. nov. and Silvania confinis sp. nov. isolated from the rhizosphere of oak
URI https://link.springer.com/article/10.1186/s12866-022-02711-x
https://www.ncbi.nlm.nih.gov/pubmed/36460957
https://www.proquest.com/docview/2755548753
https://www.proquest.com/docview/2746388548
https://pubmed.ncbi.nlm.nih.gov/PMC9716735
https://doaj.org/article/773ea828db2044ebb1c62e892bdd2e89
Volume 22
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