Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.

Burkholderia sensu lato is a large and complex group, containing pathogenic, phytopathogenic, symbiotic and non-symbiotic strains from a very wide range of environmental (soil, water, plants, fungi) and clinical (animal, human) habitats. Its taxonomy has been evaluated several times through the analysis of 16S rRNA sequences, concantenated 4?7 housekeeping gene sequences, and lately by genome sequences. Currently, the division of this group into Burkholderia, Caballeronia, Paraburkholderia, and Robbsia is strongly supported by genome analysis. These new genera broadly correspond to the various habitats/lifestyles of Burkholderia s.l., e.g., all the plant beneficial and environmental (PBE) strains are included in Paraburkholderia (which also includes all the N2-fixing legume symbionts) and Caballeronia, while most of the human and animal pathogens are retained in Burkholderia sensu stricto. However, none of these genera can accommodate two important groups of species. One of these includes the closely related Paraburkholderia rhizoxinica and Paraburkholderia endofungorum, which are both symbionts of the fungal phytopathogen Rhizopus microsporus. The second group comprises the Mimosa-nodulating bacterium Paraburkholderia symbiotica, the phytopathogen Paraburkholderia caryophylli, and the soil bacteria Burkholderia dabaoshanensis and Paraburkholderia soli. In order to clarify their positions within Burkholderia sensu lato, a phylogenomic approach based on a maximum likelihood analysis of conserved genes from more than 100 Burkholderia sensu lato species was carried out. Additionally, the average nucleotide identity (ANI) and amino acid identity (AAI) were calculated. The data strongly supported the existence of two distinct and unique clades, which in fact sustain the description of two novel genera Mycetohabitans gen. nov. and Trinickia gen. nov. The newly proposed combinations are Mycetohabitans endofungorum comb. nov., Mycetohabitansrhizoxinica comb. nov., Trinickia caryophylli comb. nov., Trinickiadabaoshanensis comb. nov., Trinickia soli comb. nov., and Trinickiasymbiotica comb. nov. Given that the division between the genera that comprise Burkholderia s.l. in terms of their lifestyles is often complex, differential characteristics of the genomes of these new combinations were investigated. In addition, two important lifestyle-determining traits?diazotrophy and/or symbiotic nodulation, and pathogenesis?were analyzed in depth i.e., the phylogenetic positions of nitrogen fixation and nodulation genes in Trinickia via-à-vis other Burkholderiaceae were determined, and the possibility of pathogenesis in Mycetohabitans and Trinickia was tested by performing infection experiments on plants and the nematode Caenorhabditis elegans. It is concluded that (1) T. symbiotica nif and nod genes fit within the wider Mimosa-nodulating Burkholderiaceae but appear in separate clades and that T. caryophyllinif genes are basal to the free-living Burkholderia s.l. strains, while with regard to pathogenesis (2) none of the Mycetohabitans and Trinickia strains tested are likely to be pathogenic, except for the known phytopathogen T. caryophylli.

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Main Authors: ESTRADA DE LOS DANTOS, P., PALMER, M., CHAVEZ-RAMIREZ, B., BEUKES, C., STEENKAMP, E. T., BRISCOE, L., KHAN, N., MALUK, M., LAFOS, M., HUMM, E., ARRABIT, M., CROOK, M., GROSS, E., SIMON, M. F., REIS JUNIOR, F. B. dos, WHITMAN, W. B., SHAPIRO, N., POOLE, P. S., HIRSCH, A. M., VENTER, S. N., JAMES, E. K.
Other Authors: Paulina Estrada-de los Santos, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológica; Marike Palmer, University of Pretoria; Belén Chávez-Ramírez, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas; Chrizelle Beukes, University of Pretoria; Emma T. Steenkamp, University of Pretoria; Leah Briscoe, University of California; Noor Khan, University of California; Marta Maluk, The James Hutton Institute; Marcel Lafos, The James Hutton Institute; Ethan Humm, University of California; Monique Arrabit, University of California; Matthew Crook, Weber State University; Eduardo Gross, Santa Cruz State University; MARCELO FRAGOMENI SIMON, Cenargen; FABIO BUENO DOS REIS JUNIOR, CPAC; William B. Whitman, University of Georgia; Nicole Shapiro, Walnut Creek; Philip S. Poole, University of Oxford; Ann M. Hirsch, University of California; Stephanus N. Venter, University of Pretoria; Euan K. James, The James Hutton Institute.
Format: Artigo de periódico biblioteca
Language:English
eng
Published: 2018-09-27
Subjects:Genes conservados, Filogenia, Análise Comparativa, Genoma, Burkholderiaceae,
Online Access:http://www.alice.cnptia.embrapa.br/alice/handle/doc/1096511
https://doi.org/10.3390/genes9080389
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libraryname Sistema de bibliotecas de EMBRAPA
language English
eng
topic Genes conservados
Filogenia
Análise Comparativa
Genoma
Burkholderiaceae
Genes conservados
Filogenia
Análise Comparativa
Genoma
Burkholderiaceae
spellingShingle Genes conservados
Filogenia
Análise Comparativa
Genoma
Burkholderiaceae
Genes conservados
Filogenia
Análise Comparativa
Genoma
Burkholderiaceae
ESTRADA DE LOS DANTOS, P.
PALMER, M.
CHAVEZ-RAMIREZ, B.
BEUKES, C.
STEENKAMP, E. T.
BRISCOE, L.
KHAN, N.
MALUK, M.
LAFOS, M.
HUMM, E.
ARRABIT, M.
CROOK, M.
GROSS, E.
SIMON, M. F.
REIS JUNIOR, F. B. dos
WHITMAN, W. B.
SHAPIRO, N.
POOLE, P. S.
HIRSCH, A. M.
VENTER, S. N.
JAMES, E. K.
Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
description Burkholderia sensu lato is a large and complex group, containing pathogenic, phytopathogenic, symbiotic and non-symbiotic strains from a very wide range of environmental (soil, water, plants, fungi) and clinical (animal, human) habitats. Its taxonomy has been evaluated several times through the analysis of 16S rRNA sequences, concantenated 4?7 housekeeping gene sequences, and lately by genome sequences. Currently, the division of this group into Burkholderia, Caballeronia, Paraburkholderia, and Robbsia is strongly supported by genome analysis. These new genera broadly correspond to the various habitats/lifestyles of Burkholderia s.l., e.g., all the plant beneficial and environmental (PBE) strains are included in Paraburkholderia (which also includes all the N2-fixing legume symbionts) and Caballeronia, while most of the human and animal pathogens are retained in Burkholderia sensu stricto. However, none of these genera can accommodate two important groups of species. One of these includes the closely related Paraburkholderia rhizoxinica and Paraburkholderia endofungorum, which are both symbionts of the fungal phytopathogen Rhizopus microsporus. The second group comprises the Mimosa-nodulating bacterium Paraburkholderia symbiotica, the phytopathogen Paraburkholderia caryophylli, and the soil bacteria Burkholderia dabaoshanensis and Paraburkholderia soli. In order to clarify their positions within Burkholderia sensu lato, a phylogenomic approach based on a maximum likelihood analysis of conserved genes from more than 100 Burkholderia sensu lato species was carried out. Additionally, the average nucleotide identity (ANI) and amino acid identity (AAI) were calculated. The data strongly supported the existence of two distinct and unique clades, which in fact sustain the description of two novel genera Mycetohabitans gen. nov. and Trinickia gen. nov. The newly proposed combinations are Mycetohabitans endofungorum comb. nov., Mycetohabitansrhizoxinica comb. nov., Trinickia caryophylli comb. nov., Trinickiadabaoshanensis comb. nov., Trinickia soli comb. nov., and Trinickiasymbiotica comb. nov. Given that the division between the genera that comprise Burkholderia s.l. in terms of their lifestyles is often complex, differential characteristics of the genomes of these new combinations were investigated. In addition, two important lifestyle-determining traits?diazotrophy and/or symbiotic nodulation, and pathogenesis?were analyzed in depth i.e., the phylogenetic positions of nitrogen fixation and nodulation genes in Trinickia via-à-vis other Burkholderiaceae were determined, and the possibility of pathogenesis in Mycetohabitans and Trinickia was tested by performing infection experiments on plants and the nematode Caenorhabditis elegans. It is concluded that (1) T. symbiotica nif and nod genes fit within the wider Mimosa-nodulating Burkholderiaceae but appear in separate clades and that T. caryophyllinif genes are basal to the free-living Burkholderia s.l. strains, while with regard to pathogenesis (2) none of the Mycetohabitans and Trinickia strains tested are likely to be pathogenic, except for the known phytopathogen T. caryophylli.
author2 Paulina Estrada-de los Santos, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológica; Marike Palmer, University of Pretoria; Belén Chávez-Ramírez, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas; Chrizelle Beukes, University of Pretoria; Emma T. Steenkamp, University of Pretoria; Leah Briscoe, University of California; Noor Khan, University of California; Marta Maluk, The James Hutton Institute; Marcel Lafos, The James Hutton Institute; Ethan Humm, University of California; Monique Arrabit, University of California; Matthew Crook, Weber State University; Eduardo Gross, Santa Cruz State University; MARCELO FRAGOMENI SIMON, Cenargen; FABIO BUENO DOS REIS JUNIOR, CPAC; William B. Whitman, University of Georgia; Nicole Shapiro, Walnut Creek; Philip S. Poole, University of Oxford; Ann M. Hirsch, University of California; Stephanus N. Venter, University of Pretoria; Euan K. James, The James Hutton Institute.
author_facet Paulina Estrada-de los Santos, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológica; Marike Palmer, University of Pretoria; Belén Chávez-Ramírez, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas; Chrizelle Beukes, University of Pretoria; Emma T. Steenkamp, University of Pretoria; Leah Briscoe, University of California; Noor Khan, University of California; Marta Maluk, The James Hutton Institute; Marcel Lafos, The James Hutton Institute; Ethan Humm, University of California; Monique Arrabit, University of California; Matthew Crook, Weber State University; Eduardo Gross, Santa Cruz State University; MARCELO FRAGOMENI SIMON, Cenargen; FABIO BUENO DOS REIS JUNIOR, CPAC; William B. Whitman, University of Georgia; Nicole Shapiro, Walnut Creek; Philip S. Poole, University of Oxford; Ann M. Hirsch, University of California; Stephanus N. Venter, University of Pretoria; Euan K. James, The James Hutton Institute.
ESTRADA DE LOS DANTOS, P.
PALMER, M.
CHAVEZ-RAMIREZ, B.
BEUKES, C.
STEENKAMP, E. T.
BRISCOE, L.
KHAN, N.
MALUK, M.
LAFOS, M.
HUMM, E.
ARRABIT, M.
CROOK, M.
GROSS, E.
SIMON, M. F.
REIS JUNIOR, F. B. dos
WHITMAN, W. B.
SHAPIRO, N.
POOLE, P. S.
HIRSCH, A. M.
VENTER, S. N.
JAMES, E. K.
format Artigo de periódico
topic_facet Genes conservados
Filogenia
Análise Comparativa
Genoma
Burkholderiaceae
author ESTRADA DE LOS DANTOS, P.
PALMER, M.
CHAVEZ-RAMIREZ, B.
BEUKES, C.
STEENKAMP, E. T.
BRISCOE, L.
KHAN, N.
MALUK, M.
LAFOS, M.
HUMM, E.
ARRABIT, M.
CROOK, M.
GROSS, E.
SIMON, M. F.
REIS JUNIOR, F. B. dos
WHITMAN, W. B.
SHAPIRO, N.
POOLE, P. S.
HIRSCH, A. M.
VENTER, S. N.
JAMES, E. K.
author_sort ESTRADA DE LOS DANTOS, P.
title Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
title_short Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
title_full Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
title_fullStr Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
title_full_unstemmed Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae.
title_sort whole genome analyses suggests that burkholderiasensu lato contains two additional novel genera (mycetohabitans gen. nov., and trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the burkholderiaceae.
publishDate 2018-09-27
url http://www.alice.cnptia.embrapa.br/alice/handle/doc/1096511
https://doi.org/10.3390/genes9080389
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spelling dig-alice-doc-10965112018-09-28T00:38:39Z Whole genome analyses suggests that Burkholderiasensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. ESTRADA DE LOS DANTOS, P. PALMER, M. CHAVEZ-RAMIREZ, B. BEUKES, C. STEENKAMP, E. T. BRISCOE, L. KHAN, N. MALUK, M. LAFOS, M. HUMM, E. ARRABIT, M. CROOK, M. GROSS, E. SIMON, M. F. REIS JUNIOR, F. B. dos WHITMAN, W. B. SHAPIRO, N. POOLE, P. S. HIRSCH, A. M. VENTER, S. N. JAMES, E. K. Paulina Estrada-de los Santos, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológica; Marike Palmer, University of Pretoria; Belén Chávez-Ramírez, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas; Chrizelle Beukes, University of Pretoria; Emma T. Steenkamp, University of Pretoria; Leah Briscoe, University of California; Noor Khan, University of California; Marta Maluk, The James Hutton Institute; Marcel Lafos, The James Hutton Institute; Ethan Humm, University of California; Monique Arrabit, University of California; Matthew Crook, Weber State University; Eduardo Gross, Santa Cruz State University; MARCELO FRAGOMENI SIMON, Cenargen; FABIO BUENO DOS REIS JUNIOR, CPAC; William B. Whitman, University of Georgia; Nicole Shapiro, Walnut Creek; Philip S. Poole, University of Oxford; Ann M. Hirsch, University of California; Stephanus N. Venter, University of Pretoria; Euan K. James, The James Hutton Institute. Genes conservados Filogenia Análise Comparativa Genoma Burkholderiaceae Burkholderia sensu lato is a large and complex group, containing pathogenic, phytopathogenic, symbiotic and non-symbiotic strains from a very wide range of environmental (soil, water, plants, fungi) and clinical (animal, human) habitats. Its taxonomy has been evaluated several times through the analysis of 16S rRNA sequences, concantenated 4?7 housekeeping gene sequences, and lately by genome sequences. Currently, the division of this group into Burkholderia, Caballeronia, Paraburkholderia, and Robbsia is strongly supported by genome analysis. These new genera broadly correspond to the various habitats/lifestyles of Burkholderia s.l., e.g., all the plant beneficial and environmental (PBE) strains are included in Paraburkholderia (which also includes all the N2-fixing legume symbionts) and Caballeronia, while most of the human and animal pathogens are retained in Burkholderia sensu stricto. However, none of these genera can accommodate two important groups of species. One of these includes the closely related Paraburkholderia rhizoxinica and Paraburkholderia endofungorum, which are both symbionts of the fungal phytopathogen Rhizopus microsporus. The second group comprises the Mimosa-nodulating bacterium Paraburkholderia symbiotica, the phytopathogen Paraburkholderia caryophylli, and the soil bacteria Burkholderia dabaoshanensis and Paraburkholderia soli. In order to clarify their positions within Burkholderia sensu lato, a phylogenomic approach based on a maximum likelihood analysis of conserved genes from more than 100 Burkholderia sensu lato species was carried out. Additionally, the average nucleotide identity (ANI) and amino acid identity (AAI) were calculated. The data strongly supported the existence of two distinct and unique clades, which in fact sustain the description of two novel genera Mycetohabitans gen. nov. and Trinickia gen. nov. The newly proposed combinations are Mycetohabitans endofungorum comb. nov., Mycetohabitansrhizoxinica comb. nov., Trinickia caryophylli comb. nov., Trinickiadabaoshanensis comb. nov., Trinickia soli comb. nov., and Trinickiasymbiotica comb. nov. Given that the division between the genera that comprise Burkholderia s.l. in terms of their lifestyles is often complex, differential characteristics of the genomes of these new combinations were investigated. In addition, two important lifestyle-determining traits?diazotrophy and/or symbiotic nodulation, and pathogenesis?were analyzed in depth i.e., the phylogenetic positions of nitrogen fixation and nodulation genes in Trinickia via-à-vis other Burkholderiaceae were determined, and the possibility of pathogenesis in Mycetohabitans and Trinickia was tested by performing infection experiments on plants and the nematode Caenorhabditis elegans. It is concluded that (1) T. symbiotica nif and nod genes fit within the wider Mimosa-nodulating Burkholderiaceae but appear in separate clades and that T. caryophyllinif genes are basal to the free-living Burkholderia s.l. strains, while with regard to pathogenesis (2) none of the Mycetohabitans and Trinickia strains tested are likely to be pathogenic, except for the known phytopathogen T. caryophylli. 2018-09-28T00:38:32Z 2018-09-28T00:38:32Z 2018-09-27 2018 2018-11-21T11:11:11Z Artigo de periódico Genes, v. 9, n. 8, article 389, 2018. http://www.alice.cnptia.embrapa.br/alice/handle/doc/1096511 https://doi.org/10.3390/genes9080389 en eng openAccess