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Article

Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae

by
Paulina Estrada-de los Santos
1,*,†,
Marike Palmer
2,†,
Belén Chávez-Ramírez
1,
Chrizelle Beukes
2,
Emma T. Steenkamp
2,
Leah Briscoe
3,
Noor Khan
3,
Marta Maluk
4,
Marcel Lafos
4,
Ethan Humm
3,
Monique Arrabit
3,
Matthew Crook
5,
Eduardo Gross
6,
Marcelo F. Simon
7,
Fábio Bueno Dos Reis Junior
8,
William B. Whitman
9,
Nicole Shapiro
10,
Philip S. Poole
11,
Ann M. Hirsch
3,*,
Stephanus N. Venter
2,* and
Euan K. James
4,*add Show full author list remove Hide full author list
1
Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, 11340 Cd. de Mexico, Mexico
2
Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0083, South Africa
3
Department of Molecular, Cell, and Developmental Biology and Molecular Biology Institute, University of California, Los Angeles, CA 90095, USA
4
The James Hutton Institute, Dundee DD2 5DA, UK
5
450G Tracy Hall Science Building, Weber State University, Ogden, 84403 UT, USA
6
Center for Electron Microscopy, Department of Agricultural and Environmental Sciences, Santa Cruz State University, 45662-900 Ilheus, BA, Brazil
7
Embrapa CENARGEN, 70770-917 Brasilia, Distrito Federal, Brazil
8
Embrapa Cerrados, 73310-970 Planaltina, Distrito Federal, Brazil
9
Department of Microbiology, University of Georgia, Athens, GA 30602, USA
10
DOE Joint Genome Institute, Walnut Creek, CA 94598, USA
11
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK
 
add Show full affiliation list
 
remove Hide full affiliation list
*
Authors to whom correspondence should be addressed.
†
These authors made an equal contribution.
Genes 2018, 9(8), 389; https://doi.org/10.3390/genes9080389
Submission received: 24 May 2018 / Revised: 19 July 2018 / Accepted: 24 July 2018 / Published: 1 August 2018
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Abstract

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.
Keywords: Burkholderia; Paraburkholderia; Caballeronia; Robbsia; Mimosa; Rhizopus; symbionts; diazotrophy; root nodulation Burkholderia; Paraburkholderia; Caballeronia; Robbsia; Mimosa; Rhizopus; symbionts; diazotrophy; root nodulation

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MDPI and ACS Style

Estrada-de los Santos, P.; Palmer, M.; Chávez-Ramírez, B.; Beukes, C.; Steenkamp, E.T.; Briscoe, L.; Khan, N.; Maluk, M.; Lafos, M.; Humm, E.; et al. Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae. Genes 2018, 9, 389. https://doi.org/10.3390/genes9080389

AMA Style

Estrada-de los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Briscoe L, Khan N, Maluk M, Lafos M, Humm E, et al. Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae. Genes. 2018; 9(8):389. https://doi.org/10.3390/genes9080389

Chicago/Turabian Style

Estrada-de los Santos, Paulina, Marike Palmer, Belén Chávez-Ramírez, Chrizelle Beukes, Emma T. Steenkamp, Leah Briscoe, Noor Khan, Marta Maluk, Marcel Lafos, Ethan Humm, and et al. 2018. "Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae" Genes 9, no. 8: 389. https://doi.org/10.3390/genes9080389

APA Style

Estrada-de los Santos, P., Palmer, M., Chávez-Ramírez, 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., Dos Reis Junior, F. B., Whitman, W. B., Shapiro, N., Poole, P. S., Hirsch, A. M., ... James, E. K. (2018). Whole Genome Analyses Suggests that Burkholderia sensu lato Contains Two Additional Novel Genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implications for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae. Genes, 9(8), 389. https://doi.org/10.3390/genes9080389

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